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RethinkingMBrainEvol Deacon
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SYNOPSIS. A critical review of past and current theories of mammalian brain evolution
is presented in order to discuss conceptual problems that persist in the field. Problems
with the concept of homology arise because of the interaction of cell lineages and axonal
connectivity in the determination of structural features of the brain. Focusing on the
continuity of information represented by ontogenetic mechanisms as opposed to mor-
phological features avoids many of these problems and suggests homological relationships
that otherwise have gone unnoticed. Many apparently progressive trends and parallelisms
in mammalian brain evolution turn out to result from the influence of underlying devel-
opmental homologies. Confusions about evolutionary advancement, increasing architec-
tonic differentiation, and the evolution of new brain structures result from a failure to
appreciate how increasing brain size can bias developmental processes with respect to
axonal competition, increased cellular metabolic demands and decreased information
processing efficiency. Explanations of the evolution of novel structures and new connec-
tional patterns are criticized for their failure to consider the constraints of neural devel-
opmental processes. T h e correlations between structural neogenesis, functional special-
ization and size changes in brain evolution are explained by a theory of competitive
displacement of neural connections by others during development under the biasing
influences of differential allometry, cell death or axon-target affinity changes. T h e "dis-
placement hypothesis" is used to propose speculative accounts for the differential enlarge-
ment and multiplication of cortical areas, the origins of mammalian isocortex, the unusual
features of dolphin cortex and the dramatic structural and functional reorganizations that
characterize human brain evolution.
tures than that of Erinaceus. These authors tiation of the visual system and a corre-
conclude that Erinaceus is probably "not a spondingly heavy reliance on the olfactory
typical representative of a real basal insec- system. Evolutionary reduction or degen-
tivore" (Zilles a n d Rehkämper, 1988; eration of an essentially unused sense
emphasis in the original). Only in a context modality may induce dedifferentiation, but
where evolution is presumed to progress this does not likely follow an exactly
from simple to complex, from least en- reversed phyletic trend and may produce
cephalized to most encephalized, and from structural features that are quite distinct
generalized, inflexible and inefficient in from ancestral features. How can we be
function to specialized, flexible and highly sure that the relatively undifferentiated
efficient in function, can the search for the state of the cortex of these species is rep-
absolutely simplest mammalian brain be resentative of a retained primitive state
equated with the search for the ancestral rather than a recent specialization?
brain. Second, these exemplar species also rep-
There are two general attributes shared resent the very lowest limits of mammalian
b y essentially all the basal insectivores con- brain size. This is a problem because many
sidered primitive in brain organization that measures of structural complexity appear
should cause us to be cautious about gen- to be strongly correlated with brain size
eralizing from them. First, each of the can- (Tower, 1954; Haug, 1987; Deacon, 1990a;
didate exemplar species inhabits a noctur- and see the following section). Nearly all
nal-fossorial niche. This is probably no the attributes of "primitiveness" of mam-
accident. This adaptation has likely pro- malian brains are also typical attributes of
duced secondary reduction or dedifferen- very small brains, while those of "advance-
ment" are only expressed in relatively large ilar across a wider range of species than
brains. Progressivetrends measured with one exhibiting a number of easily discrim-
respect to these small insectivore species inated features. As a result, despite its
a r e significantly confounded with t h e apparently unbiased definition of polarity,
effects of differences of scale. Also if there the cladistic approach may be biased, so as
has been prolonged selection f o r size to pick out more generalized and less dif-
reduction in these species there may also ferentiated traits as characterizing a com-
be simplifications of brain structure of a mon ancestor. Evolutionary regression in
secondary character which d o not neces- certain lineages is potentially a source of
sarily follow a reverse phylogenetic trend. misleading bias as is the correlation of
absolute brain size with structural com-
Cladistic approaches plexity. Additionally, this approach is sen-
T h e cladistic approach to identifying sitive to the effects of convergent or par-
evolutionary trends offers some hope of allel evolution. It will be argued below that
resolving these ambiguities and avoiding parallelism is a major feature of mammal
the trap of implicit progressionism. By brain evolution.
replacing the assumption of evolutionary Nonetheless, the cladistic approach is in
deyelopment and increase in complexity some ways self-correcting in this regard. It
with a simpler empirically defined dichot- can be useful in discerning some of these
omy between conserved and derived con- biasing influences by using multiple sources
ditions one can arrive a t a relatively of information pooled to establish most
unbiased criterion for identifying evolu- parsimonious descent relationships and
tionary trends. T h e particular character- then reanalyzing individual trends. For
istics of the trait are irrelevant, only its example, the relative primitiveness of the
presence or absence in different groups is "basal insectivore" brain can be tested with
important. By pairwise comparison of the respect to three outgroups of mammals
presence o r absence of traits between whose phylogenetic affinities a r e well
species in progressively more distant out- known through other cladistic analyses: the
groups it is possible to decide which traits marsupials and the two living monotremes,
can be operationally defined as derived and t h e platypus Ornithorhinchus a n d t h e
which can be defined as ancestral o r con- echidna, or spiny anteater, Tachyglossus.
servative. Cladistic analysis has wide accep- Many of the characteristics of Erinaceus'
tance as a means for reconstructing phy- brain, including apparent adjacency of
ietic relationships between lineages, but it projection areas, minimal association cor-
has also been used extensively to trace the tex, high ratio of olfactory-limbic cortex
ancestry of specific traits. It has been par- to isocortex, poor laminar distinction, poor
ticularly useful for deciding between alter- granularization and poor differentiation of
native accounts of a trait's evolution architectonic areas, are not exhibited in
because it provides a measure of parsi- the brains of larger marsupials and mono-
mony. For example, Northcutt (1984) uses tremes. Have the apparently m o r e
the number of mutational events that must advanced traits also found in these out-
be postulated in order to explain the dis- groups evolved independently in the larger
tribution of certain vertebrate brain traits brains of all the mammalian lineages? T h e
according to different theories to decide more parsimonious interpretation is that
which of these theories provide the most many of these traits were present in some
parsimonious accounts. form in the common ancestor of all mam-
T h e Achilles heel of this approach with malian groups long before the recent
respect to brain evolution is that it will eutherian radiations. T h a t they fail to be
inevitably tend to favor identifying rela- exhibited by some of the brains in the
tively undifferentiated forms as more eutherian lineage (e.g., basal insectivoresj
primitive and differentiated forms as more and some brains in the marsupial lineage
derived. A structure lacking differentiat- (e.g., Didelphis virginiana) is not sufficient
ing features will tend to be glossed as sim- evidence to assume that they are derived.
Kaas (1989) applies an implicit cladistic Lack of positive evidence is not sufficient
approach to determine which cortical areas to deny homology but the availability of
in all mammals can be traced via descent positive evidence is sufficient to establish
from a common ancestor. He notes that in it.
all the major mammalian lineages (euthe- This can also be applied to questions con-
rian and metatherian) there are distinct cerning the origins of somato-motor areas.
visual, auditory and somato-motor projec- Lende (1969) demonstrated that in Didel-
tion areas within isocortex. H e concludes phis the somatosensory responsive cortex
that the common ancestor for all these lin- and the electrically excitable motor cortex
eages likely also possessed these differen- exhibited complete overlap and that in Eri-
tiated projection areas and not just an naceus there was a large region of overlap.
undifferentiated protoisocortex. Based on More recently some degree of overlap has
this evidence he rules out a widely cited also been demonstrated in rats (Donoghue
theory of cortical evolution proposed by et al., 1979). In carnivores and primates
Sanides (1970) that is based on the assump- (and probably ungulates) these areas are
tion that generalized undifferentiated iso- adjacent but completely segregated into
cortex preceded specialized sensory-motor distinct parallel somatotopic and muscu-
projection cortices in the course of cortical lotopic maps. Lende also argued that there
evolution. However, to be more explicit, was even some overlap of visual and audi-
what has been demonstrated is that dis- tory cortical areas in the opossum (although
crete somatic, auditory and visual projec- this finding has not been replicated). This
tion areas are expressed in mammal brains suggested to him that the ancestral state of
under all existing conditions and sizes, cortex was characterized by poor areal dif-
whereas some areas, particularly many ferentiation in which all the sensory modal-
association areas, fail to be expressed under ities exhibited nearly complete overlap with
many conditions, specifically in small brains. one another. However, at least one larger
T h e classic view that association cortex Australian marsupial, t h e brush-tailed
is new in comparison t o projection cortex opossum Trichosurus, exhibits considerable
in part derives from the apparent lack of segregation of somatic and motor fields
association cortex in basal insectivore brains (Haight and Neylon, 1978, 1979) and the
(but this assumption is criticized below) and monotremes appear to exhibit complete
its progressive domination of the cortical segregation of somatic and motor areas.
surface in "advanced" mammals. How- All of these facts- argue against assuming
ever, some of the larger marsupials and that the primitive condition was undiffer-
even the echidna appear to exhibit signif- entiated and completely overlapping and
icant expanses of association cortex in suggest that at least some degree of seg-
addition to primary sensory-motor projec- regation of these functional zones char-
tion areas. Apparently, under similar acterized the common ancestor of all mam-
developmental conditions- large brain ma1 groups.
size-this trait is expressed in every lin- But negative evidence can be cited to
eage of mammals. T h e common conditions support the view that the segregation of
required for expression of this trait in all somatic and motor modalities is a conver-
three lineages also lends confidence to the gent trait. This evidence comes from vari-
claim for homology as opposed to parallel ations in somatotopy of the sensory and
homoplasy. motor maps in the different groups. In most
T h e failure of basal insectivore brains to eutherian mammals studied the two fields
exhibit distinctly segregated association are arranged as mirror images of one
areas is not sufficient evidence to deny that another with respect to their common bor-
this trait is a shared ancestral trait. None- der, and exhibit this pattern even in species
theless the appearance of segregated visual, where there is considerable overlap of the
auditory and somato-motor areas in all two areas. However, in edentates and mar-
mammal brains is sufficient evidence to supials the two maps appear to be arranged
consider them as shared ancestral traits. in parallel as well as overlapped (Dom et
al., 1971; Lende, 1963, 1969; Magalhães- vastly increases the probability of conver-
Castro and Saraiva, 1971; Royce et al., gence and parallelism. In fact, many of the
1975; Saraiva a n d Magalhães-Castro, "advanced" traits of eutherian mammal
1975), and in a megachiropteran bat (Pter- brains could have been inherited from the
opus poliocephalus) the somatic map appears common ancestor of eutherian mammals
inverted from that typical of most other even if that ancestor failed to exhibit any of these
eutherian mammals (Calford et al., 1985). traits.
T h e monotremes appear to exhibit char- All three mammalian groups have likely
acteristics found both in some eutherian inherited neural developmental con-
and in som'e marsupial brains (Bohringer straints and tendencies from a common
and Rowe, 1977). Furthermore, the pat- ancestor that are expressed differentially
tern of thalamocortical connections to these in different contexts. It is possible that the
areas differs in eutherian and marsupial "initial" eutherian brain possessed the
brains. developmental information for these traits
This negative evidence is inconclusive but failed to express them because certain
because the differentiation of map orien- other conditions of their expression were
tation could occur independent of the seg- not met. Below it will be argued that the
regation of somatic and motor areas. T h e small size of these brains precludes the
unique status of the fox bat and edentate developmental expression of cortical par-
somatic maps in comparison to other mam- cellation processes necessary to produce
malian groups suggests that this is the case. multiple highly differentiated cortical
Map orientation appears to be a derived areas. Also the regression of the visual sys-
condition in these species. Variation of this tem in basal insectivores may f u r t h e r
trait occurs against the background of undermine these processes. Despite the fact
somatic and motor map segregation as an that ancestral traits might not be expressed
apparently older and more conservative in an intervening lineage there need be no
trait. T e only placental and marsupial interruption of their descent t o subsequent
mammals that do not exhibit segregation lineages, and their disappearance o r reap-
of somatic and motor projection areas also pearance in certain lineages cannot be
have relatively small brains. This further attributed to distinct mutation events and
suggests that this is a derived condition treated as distinct derived conditions. We
contingent on small size and not the ances- should be especially wary of this possibility
tral condition. in the choice of traits included for cladistic
Problems with these comparisons of cor- analysis.
tical areas stem from the fact that the traits This again underscores the importance
under consideration are not simple and the of thinking of homologies in informational
variables that correlate with the differen- terms. Even if we were to miraculously learn
tial expression of these complex traits have the details of morphology of the brain of
not been controlled for in the analysis. T h e the true eutherian ancestor we would per-
most important of these variables is brain haps still be a long way from understanding
size, but other factors are also clearly the initial conditions embodied in that initial
involved with regard to more subtle fea- brain that still influence the structure and
tures, such as map topography. Failure to the evolution of modern brains. What we
control for these factors inevitably leads to ultimately want to know is what information
their being confounded with descent rela- was embodied in the initial brain and in
tionships despite the fact that cladistic anal- the developmental mechanisms that built
ysis itself does not prejudge the primitive it.
or advanced status of a trait. T h e differ-
ential expression of a large number of traits Recapitulationism
with respect to brain size or the differential During embryogenesis there is a definite
expression of traits in brains with respect progression from smaller poorly differen-
to sensory specializations can be a serious tiated structures to larger highly differ-
problem for cladistic analyses because it entiated structures. Large species with rel-
atively differentiated brains must inevitably matured they passed through stages of cog-
pass through developmental stages in which nitive and emotional development that
their brains are small and poorly differ- corresponded to distinct "grades" of ani-
entiated. Consequently, t h e embryonic mal consciousness from reptilian to mam-
stages of larger more differentiated brains malian, from primitive mammal to pri-
will inevitably bear some superficial resem- mate, from primate to primitive human,
blance to the adult stage of small poorly and finally through the ascending stages
differentiated brains. Structures that dif- from "primitive savagery" to modern civ-
ferentiate later in development will thus ilization (e.g., Spencer, 1870; Baldwin,
appear to be added to an otherwise com- 1895). Various primitive human societies
mon substrate. Recapitulation assumes that and criminals were viewed as arrested at
adult structures in primitive species are some prior stage of development. Although
homologous to embryonic structures in the recapitulational structure of the brain
advanced species. Subsequent modifica- was assumed by many prominent 19th cen-
tions of brain structure have been added tury and early 20th century neurologists
in the more "advanced" species by extend- (e.g., Paul Broca, John Hughlings Jackson,
ing the ontogenetic process to include Ivan Pavlov, John Sherrington, and Sig-
additional later stages. This process of ter- mund Freud) probably the major catalyst
minal addition was presumed to link the for the formation of a comparative ana-
evolution of species to development in such tomical version of this theory came as a
a way that a scale of increasing complexity result of the synthesis of two sources of
in evolution was the inevitable outcome of neuroanatomical evidence just subsequent
a progressive increase of developmental to the turn of the 20th century.
information. Evolution is explained as an Paul Flechsig's (190 1) analysis of myelin-
augmentation of ontogenesis and more stained tissue from human fetuses at var-
"advanced" species are literally assumed to ious stages of development demonstrated
be further developed. a progression of myelination of isocortical
Despite the enormous theoretical power areas that began with primary sensory and
of this synthesis, the weight of comparative motor areas, continued to belt zones around
and ontogenetic evidence that has accu- these areas and culminated in relatively late
mulated against this doctrine in the last myelinating association areas (see Fig. 4).
century is overwhelming. Ontogenetic dif- This sequence was presumed to correlate
ferences that distinguish different lineages with developmental trends in which basic
may occur at any stage of development and sensory-motor abilities mature early in
are clearly not constrained to occur in lin- childhood and the "highest" intellectual
ear sequence with increasing phylogenetic abilities only appear late in developmeht.
.divergence. Although larger creatures tend It was also presumed to correlate with an
to exhibit longer ontogenesis than smaller evolutionary sequence from species with
creatures, larger creatures d o not have only crude sensory-motor habits a n d
additional stages added on and highly responses, to species with the capability of
derived members of a lineage d o not show complex and flexible associational learning
more developmental stages than highly abilities. T h e most developed associated
conservative members; differences in areas were assumed to be the newest in
development appear at many correspond- evolutionary terms and the last to develop
ing stages. However, despite the patent in ontogeny.
failure of this paradigm, numerous unrec- At roughly the same time .comparative
ognized recapitulationist assumptions still anatomists, using preparations that visu-
persist in the literature about brain evo- alized neuron cell bodies, produced maps
lution, primarily in the form of tacit ter- of the distinguishable cytoarchitectonic
minal addition assumptions. areas of the cerebral cortex for a number
Early recapitulationist theories of brain of mammalian species which appeared to
development suggested that as children demonstrate homologues for primary pro-
jection areas in all species, but no homo- lateral view
logues for many human association areas
in monkeys and no homologues for many
monkey association areas in other mam-
mals (e.g., Campbell, 1 905; Brodmann,
1909). It clearly appeared as though the
developmental t r e n d recapitulated a
sequence of additions of new cortical areas
leading up to the human brain. New, more
developed 'association areas were appar-
ently added to the brain of succeeding
species at the end of their maturational
development. T h e unusually long postna-
tal brain development of humans could also
be explained on the basis of the extra stages
of brain development that were appended
to, human ontogeny.
These assumptions corresponded with
the neuropsychological doctrine of the
time. It was assumed that the moment to
moment processing of sensory input
retraced this same hierarchy, developing
from the crude registration of sensory
information in projection areas, to the con-
struction of a perceptual gestalt in sensory
psychic areas, and finally to the elaboration
of multimodal associations with respect to
different remembered vercevtions, actions
and emotional experiences in association medial view
areas. Primitive animals and young chil- FIG. 4. Flechsig's myelogenesis figure of the human
dren only progressed through the initial brain is redrawn from the original leaving out Flech-
stages of this cognitive hierarchy. Although sig's numerical designation of myeloarchitectonic
the developmental recapitulation assump- fields. T h e darker areas represent the areas that mye-
tion has been abandoned, a more elaborate linate earliest in development and the white areas
represent the areas that myelinate latest. Insular cor-
version of this basic hierarchic functional tex is partially exposed. Note the progression from
interpretation remains the dominant con- primary to secondary to association areas of cortex.
temporary theory of sensory processing Note also the early myelination of limbic cortical areas
(e.g., Mishkin a n d Appenzeller, 1987; and pathways.
Maunsell and Van Essen, 1983), despite
many growing inconsistencies and t h e
availability of alternative interpretations
(e.g., Brown, 1988; Deacon, 1989a; Dia- will primarily address the issue of the
mond, 1982; Optican a n d Richmond, developmental sequence, but will return to
1987). the issue of the terminal addition of cor-
However, in hindsight we can see fun- tical areas in a later section.
damental flaws in both forms of evidence An alternative explanation for the pri-
for this correlation of ontogenetic devel- mary-secondary-tertiary hierarchy of my-
opment with apparent phylogenetic devel- elination of cortical areas can be derived
opment. Ultimately I will argue that both from a correlation between the total level
derived from a failure to control for factors of adult myelination achieved by these
having more to do with brain size than with structures and their apparent develop-
phylogenetic progression. In this section I mental schedule. T h e early myelinating
areas are also the most heavily myelinated tonic trend as well as other architectonic
in the adult and the latest myelinating areas trends led Sanides (1969, 1970, 1972) to
are the least myelinated in the adult propose that the terminal addition of cor-
(Bishop, 1959; Sanides, 1970). This rule tical areas in mammalian evolution might
also applies to noncortical structures: the actually be the reverse of that proposed by
relatively poorly myelinated reticular for- the traditional theorists—progressing from
mation of the midbrain exhibits one of the association areas to secondary areas t o pri-
latest and longest cycles of myelination of mary areas as the most highly developed.
any system (Yakovlev and Lecours, 1967) Although not a recapitulationist theory,
despite the fact that it is without doubt one because it makes no claims for develop-
of the most conserved structures in the ver- ment, it does nonetheless assume terminal
tebrate brain. This fact clearly contradicts addition in a phylogenetic sense, and an
the recapitulationist assumption. implicit progression from primitive t o
There are two possible interpretations advanced forms based upon the addition
of this correlation between total amount of more highly differentiated structures.
of myelination and the developmental time T h e neuropsychologist Jason Brown (1977,
course of myelination. First, since these 1988) has elaborated a self-consciously
assessments of myelination are based on recapitulationist theory of cortical func-
myelin-stained tissue sections in which more tion that is based upon Sanides' model of
densely myelinated tissue stains darker, phylogenetic progression, in which
there may be a level of nearly complete "microgenetic" processes of sensory anal-
staining opacity reached at an early devel- ysis proceed in a series of stages from lim-
opmental stage in areas that exhibit max- bic to association to specialized cortical
imal myelination whereas this level of areas rather than the other way around, as
staining opacity may never be achieved by is suggested in traditional models.
very poorly myelinated areas. In this case Both interpretations are based on mis-
the apparent heterochrony could be largely leading correlations that confound a num-
illusory. Alternatively, the deposit of my- ber of factors. T h e correlation between the
elin on axons destined to be heavily myelin- density of myelination in adults, the initi-
ated could take place at an absolutely faster ation and rate of myelination in develop-
rate (which appears to be indicated by the ment, and the overall level of myelination
data of Yakovlev and Lecours, 1967) and in brains of different sizes suggests that all
could begin earlier. It is probably an of these apparent comparative trends may
important corollary that the most heavily have less to do with any evolutionary
myelinated fibers are also often the largest sequence and more to do with certain con-
diameter axons that project relatively long servative functional and metabo1ic rela-
distances o r to highly specific targets. tionships between axons of differing sizes
There is also an important correlation and the glia that form their myelin sheaths.
between brain size and primitive-advanced T h e developmental differentiation of the
comparisons. Small insectivore and rodent brain occurs in the process of increasing
brains appear to be generally less myelin- the size of the brain. T h e evolution of
ated overall and exhibit less myeloarchi- increasingly differentiated mammal brains
tectonic differentiation from cortical area also correlates with t h e evolution of
to cortical area than the larger brains of increasing brain size. The similarities
primates (Sanides, 1970). Therefore if between brain development and brain evo-
myelination is to be used as a ruler of pro- lution may largely be the result of these
gression then the least myelinated areas parallelisms. In both, the confusing role of
should be considered the more primitive brain size and its many correlative struc-
areas and the most myelinated areas the tural scaling relationships underlies many
more advanced cortical areas (Bishop, of the misidentifications of evolutionary
1959). This runs exactly counter to the progress. T h e nature of some of these
apparent developmental progression. underlying correlations will be the subject
This apparent phyletic myeloarchitec- of the next section.
BRAIN SIZE the largest mammals on earth. If we think
of the brain as a computer and the body
The influence of anthropocentrism as the many users that are on line, vying
T h e significance of brain size is at once for processing time and memory storage,
the most broadly debated issue in the study then it becomes obvious that the effective
of brain evolution and probably also its most information processing capacity available
ubiquitous, misunderstood and troubling for any particular function is constrained
feature. More has been written about brain by the number of competing demands from
size than about any other topic concerning other sources. This has suggested to many
brain evolution. Like the notion of evo- that the ratio of brain to body is a more
lutionary progress, interest in brain size significant measure of available informa-
owes much to its apparent importance for tion processing capacity. Despite the fact
understanding human brain evolution. that they have absolutely larger brains, ele-
With a brain roughly three times larger phants and whales have a much lower ratio
than a primate of our size should possess, of brain to body than humans. But this
it is natural to assume that brain enlarge- observation is also unsatisfactory. Very
ment must hold the key to human unique- small birds and mammals have a higher
ness. But is brain enlargement symptom o r ratio of brain to body size than humans
cause in this transformation? Is relative and an even higher ratio of neuron num-
brain size alone the significant difference ber to body size.
o r is it a superficial consequence of more A satisfactory account of comparative
fundamental changes in brain organiza- brain size that ranked humans on top (and
tion? Size is also the easiest feature of the thereby preserved the intuition underlying
brain to study and so lends itself to broad the Anthropocentric Maxim) was discov-
comparative studies and studies of other ered at the end of the 19th century in the
possible correlates to brain size that might form of allometric analysis. Since that time
be of interest to researchers who otherwise the use of "subtraction criteria" based on
have little neuroscientific training. But the empirical brain and body size trends have
tendency to terminate the analysis of brain been assumed t o define that portion of the
difference with measurements of brain size brain mass that is functionally correlated
is a significant impediment to progress in with information processing demands of
the investigation of brain evolution, pre- the body. Deviations from these trends have
cisely because issues of brain size are insep- been assumed to respectively indicate
arable from issues of function and internal excess o r dearth of mental capacity (but
organization in some very fundamental see criticisms below). T h e importance of
ways. allometric analysis for the investigation of
T h e role of brain size in brain evolution patterns of relative growth and the sec-
appears deceptively simple. If the brain is ondary correlates of differences in size is
a computing device of some kind, then an paramount, not just as a criterion of sub-
increase in component processing ele- traction, but as a tool for drawing attention
ments should correlate with an increase in to the ways that biological processes can
information processing capacity. This intu- be affected by changes of scale. Allometric
ition appears to be borne out by the unsys- analysis has produced some remarkable
tematic observation that species with brains insights into the problem of relative growth
at the small end of the size range for ver- and has demonstrated some remarkably
tebrates exhibit mostly simple and stereo- regular patterns of size-related brain vari-
typic behaviors compared to those with ation from species to species and from evo-
brains toward the large end of the spec- lutionary epoch to epoch.
trum. This observation is not totally sat- T h e more detailed pursuit of allometric
isfactory. Some mammal brains exceed the relationships has shown that differences of
human brain in total volume and neuron brain size have consequences at every level
number-for example, elephant and whale of neuroanatomical and neurophysiologi-
brains. However, these species represent cal organization. Not all features of the
brain scale isometrically with size changes ative brain size and intelligence is open to
in brain evolution. This has serious func- serious question. T h e r e are distinctly dif-
tional consequences that have yet to be ferent brain-body trends for different
appreciated-much less understood-and mammalian taxa that can all provide equally
serious methodological consequences for valid-but not concordant-measures of
comparative studies because it immensely encephalization for an individual, t h e
complicates t h e task of determining somatic fraction of brain size that is pre-
homology. A failure to appreciate the sumed to be allometrically "subtracted" in
numerous architectonic and functional the estimation of encephalization cannot
consequences of differences in brain size be a simple linear factor as is often assumed,
lies at the heart of numerous misunder- and deviations from the empirical trend
standings about brain evolution, including cannot automatically be assumed t o cor-
issues of progression and the question of relate with mental adaptation as opposed
brain size evolution itself. to metabolic, ontogenetic o r somatic adap-
tations (Deacon, 1990a, b). More impor-
Is there a trend toward increasing tantly, the assumption that intelligence—
encephalization? much less comparative intelligence-is a
One of the earliest discoveries concern- single measurable scalar quantity is highly
ing brain evolution in mammals was that dubious from either a neurological o r an
mean brain size and relative brain size have evolutionary perspective and has never
increased with respect to our reptilian been adequately supported by comparative
ancestors and have increased since the intelligence testing (MacPhail, 1982; Gard-
beginning of the great eutherian mammal ner, 1983; Hodos, 1988; Deacon, 1990a).
radiations. This seems to be a clearly pro- This issue has been extensively discussed
gressive trend and suggests that brain size and debated elsewhere and so will not be
itself may be an adaptation under selection. reviewed here, except to point out both
But is it? If it is, then is there selection for the obvious progressionist and anthropo-
total brain size o r for relative brain size? centric assumptions that are inextricably
And what kind of evidence would be nec- bound up with the entire enterprise. Only
essary to demonstrate one o r the other? the issues surrounding phylogenetic inter-
T h e accepted answers to these questions pretations will be considered here.
have been phrased in terms of the evolu- Since the appearance of the first verte-
tion of intelligence, and have changed little brates, brains and bodies in many lineages
in form since well before the turn of the have enlarged by orders of magnitude. T h e
century. relative sizes of brains and bodies have also
Brain enlargement, both in absolute and changed. For an animal of a given body size
relative terms, has typically been referred the ratio of brain to body size has also
to as encephalization. Beginning with the increased in a number of lineages, though
work of Dubois (191 3) the term became not all. These general trends are capped
associated with a specific mathematical by the evolution of mammal brains. T h e
index: the measure of the relative devia- largest brains ever to have existed are now
tion of the ratio of brain to body size in a possessed by whales and the most extreme
species from the expected ratio for an aver- values of encephalization ever to have
age animal of the same body size, based on existed are now exhibited by dolphins and
trends for a given taxonomic group or for primates-particularly humans. Within any
some baseline comparison group (Bonin, taxonomic group of living vertebrates there
1937; Dubois, 19 13; Gould, 1966; Jerison, is a negative allometric relationship
1973: Stephan, 1969). Two major appli- between brain size and body size, such that
cations of these measures of encephaliza- adult individuals with larger body sizes tend
tion are the assessment of taxonomic and to exhibit lower ratios of brain to body size
phylogenetic differences of relative brain than smaller individuals. T h e scaling rela-
size and the assessment of species differ- tionship is approximately linear when ren-
ences in intelligence. Whether or not there dered in logarithmic coordinates but the
is any meaningful relationship between rel- particular slope and y-intercept of this line
FIG. 5. Allometric patterns of comparative vertebrate brain size and mammalian brain growth. Graph A,
on the upper left, depicts convex polygons that enclose all points of brain and body size for four major
vertebrate classes (from Jerison, 1973) along with an approximation of the polygon that would have enclosed
the stem mammals. Note the incredible mammalian brain and body size expansion from this precursor group.
Note also the overlap of teleost fishes and lizards and of birds and mammals and the lack of a scala naturae
trend from fish to mammals. Graph B, on the upper right, shows the trend line for carnivores and for the
domestic dog breeds. Arrows indicate measures of encephalization o r somatization for a small dog with respect
to the carnivore trend. This is intended to show that "encephalization" differences do not necessarily imply
selection on brain traits. Graph C, on the bottom left, shows an ontogenetic developmental trajectory for
brain and body growth in two typical mammals of different body size. T h e prenatal phase overlaps completely
for most species. Graph D, on the bottom right, shows ontogenetic curves for different mammalian species
and their relation to interspecific trends. Note that ontogenetic lines overlap for different size species during
the early ontogenetic phase. T h e shift of ontogenetic curves that distinguishes primates, cetaceans and ele-
phants from other mammals is shown in gray.
differs depending on the taxonomic group mechanism common to all mammals, and
under consideration. Proposals for possibly all vertebrates (Deacon, 1990b).
explaining the regularity and slope of these Ultimately no single explanation can
trends include the possibility that brain size account for the substantial differences in
tracks body surface (Snell, 189 1; Dubois, scaling relationship exhibited at different
19 13; Jerison, 1973), that brain size is con- taxonomic levels of analysis. Within a
strained by metabolic capacity which is also species the allometry is strongly negative
negatively allometric (Martin, 198 1; Arm- with slope on the order of 0.1 to 0.2,
strong, 1983),that because brain is derived whereas within a whole order o r whole ver-
from embryonic ectodermal tissue, the tebrate class the allometric slope is often
same growth control mechanisms may con- in the range of 0.6 to 0.8. See Figure 5a
trol mitosis in brain and body surface struc- and b.
tures (Deacon, 1990b), o r that target body T h e brain-body allometries of the dif-
size is controlled by neuron number via a ferent living vertebrate classes appear to
be distributed bimodally. T h e homeo- tational trade-offs involving large litter sizes
thermic classes-birds and mammals— and rapid reproductive rates characteristic
tend to scale together and the poikilother- of small r-selected species. These repro-
mic classes-fish, amphibians and rep- ductive specializations have been corre-
tiles-tend t o scale together, with homeo- lated with gestational constraints that affect
therms exhibiting a much larger brain growth (Martin, 1983; Deacon,
percentage of brain to body a t any given 1990b). Similar factors may also be impor-
body size (see Fig. 5a). In the evolution of tant for understanding marsupial brain size
birds and mammals there has clearly been development. It is possible that low esti-
an increase in encephalization over the mates of "basal" encephalization may be
ancestral reptilian condition as repre- misleading if they incorporate superim-
sented by modern reptiles. But using mod- posed developmental trade-offs that sec-
ern species as exemplars for ancestral rela- ondarily reduce encephalization. We
tionships it cannot be said that there has should expect that progressive removal of
been a steady increase in encephalization these constraints in lineages radiating into
from fish to amphibians t o reptiles t o birds K-selected, larger-body-size niches might
and mammals. In fact, some of the most result in an apparent " rebound" of
"primitive" fishes, the sharks and rays, encephalization. A similar "rebound" effect
comprising the Chondryichthes, exhibit has been suggested by Gould (1975) and
levels of encephalization that exceed all Deacon (1990b) in response to intense
other fishes, amphibians and reptiles, and selection for increasing body size in evo-
overlap the ranges for birds and mammals lution. Breeding experiments demonstrate
(Bauchot et al., 1979) . There is no clear that selection on body size produces body
scala naturae of encephalization. In con- size increase in successive generations with
trast, relative conservatism of the enceph- little correlated increase in brain size
alization relationship is demonstrated by (Atchley, 1984; Riska et al., 1984). Deacon
the extensive overlap of encephalization in (1990b) argues that after an initial rapid
different vertebrate classes. evolution of increased body size effected
Discerning the progressive encephali- by modifications of peripheral hormonal
zation of mammals relative to their reptil- mechanisms, continued stabilizing selec-
ian ancestors involves more subtle distinc- tion would tend to produce complemen-
tions, but the major step across this gap tary brain size increase as a more stable
appears to have already been taken by the central determiner of target body size.
time of the common ancestor of metatheri- T h u s t h e rapid radiations into m o r e
ans and eutherians (Ulinksi, 1986). In com- K-selected, large-body-size niches t h a t
parison with other mammalian lineages the characterized many mammalian lineages in
marsupials and the insectivores appear to the Eocene may have provided a biased
occupy the low end of encephalization, but sample of species for comparison to more
the monotremes appear on a par with the modern lineages.
mean for eutherian mammals. If the small T h e case for an increase in encephali-
brained basal insectivores and marsupials zation in primates, elephants and cetaceans
are characteristic in this regard of most is strengthened by independent evidence.
stem mammalian groups then most other From very early in embryogenesis all these
mammalian lineages have exhibited pro- species exhibit approximately double the
gressive encephalization. Such a trend is ratio of brain to body size found in any
demonstrated in the fossil record and has other mammal group at a comparable
been used as support for the claim that developmental stage (Count, 1947; Sacher
there has been a progressive trend toward and Staffeldt, 1974; Martin, 1983; Deacon,
increased intelligence in all these lineages 1990b). This difference is evident at the
(Jerison, 1973). earliest stages in which brains are discern-
T h e relatively lower encephalization of able in the developing embryo and so rules
many small bodied forms including basal out explaining this encephalization in terms
insectivores and rodents, may reflect ges- of the terminal addition of neural tissue
late in development (see Fig. 5c, d). Curi- Body size is a highly flexible and ecologi-
ously, the trajectory of brain-body growth cally significant variable, whereas brain size
for all three groups closely overlaps for the is a relatively inflexible and as yet poorly
entire fetal period, suggesting a common understood variable that may o r may not
brain growth mechanism. T h e brain-body correlate with differences in behavior. T h e
growth trajectories of the remainder of the search for changes in brain structure that
eutherian mammals also all appear to share correlate with addition or subtraction of
a common fetal trajectory, suggesting that neural tissue in evolution in order to
they all share a different common mech- account for encephalization is for this rea-
anism for determining brain growth. As son probably misguided; we might just as
with t h e encephalization difference well look for addition o r subtraction of the
between homeotherms and poikilotherms, many parts of the rest of the body.
this. embryological encephalization differ-
ence distinguishing primates, dolphins and Disentangling allometry and progression
elephants from the remainder of the When organisms get larger, either dur-
eutherian mammals appears as a distinct ing development o r in the course of evo-
discontinuity without intermediates. lution, all features of the organism are not
As a final comment on the encephaliza- scaled up isometrically. Even more trou-
tion issue it should be pointed out that the blesome for the comparative anatomist is
term itself reflects an underlying bias that the fact that homological relationships can
is part historical and part theoretical. Early appear to change with evolutionary changes
writers often did not clearly distinguish in size. Different structures may radically
absolute brain size from the relation of change size with respect to one another o r
brain size to body size in their discussions alter their relative position, structures may
of brain evolution (Gould, 198 1). T h e ulti- radically change shape due to unequal
mate interest has of course all along been growth rates among their parts o r single
the explanation of human brain size. But structures may divide o r differentiate to
measures of brain size with respect to body become two o r more distinct structures.
size are inherently relational. Increased This is the source of one of the most insid-
encephalization is also decreased somati- ious problems in evolutionary theory: the
zation, and vice versa (see Fig. 5b). One confusion of size related changes with evo-
need not necessarily assume neurological lutionary advancement. T h e secondary
explanations for differences in this rela- effects of change of size can include the
tionship. Although breeds of dogs differ apparent addition of new structures to old
enormously in degree of encephalization or the appearance of increased complexity
(from small highly encephalized dogs to in existing structures. It may be difficult t o
large poorly encephalized dogs) no one tell whether an increase in size has caused
doubts that body size is the selected vari- old structures to differentiate and subdi-
able and brain size the relatively less flex- vide o r whether the addition of new struc-
ible parameter. In fact, breeding experi- tures has caused an increase in size.
ments selecting progeny on the basis of As D'Arcy Thompson pointed out in his
either extremes of brain size o r extremes classic treatise on the effects of growth o n
of body size demonstrate that selecting for form (1917), most mechanical forces,
body size produces a poor correlated material properties and structural relation-
response in brain size whereas selecting for ships do not change isometrically with
brain size produces a highly correlated changes in size. Geometric effects are most
response in body size (Roderick et al., 1976; obvious — e.g., surface area to volume— but
Fuller, 1979; Atchley, 1984; Riska et al., also there are changes in the relative vis-
1984; Kruska, 1987). Given that a large cosity of fluids, diffusion rates of mole-
fraction of the variance in "encephaliza- cules, structural plasticity o r rigidity of
tion" within a species can be a consequence materials, rates of chemical reactions, etc.
of selection on body size, why should this Many of these non-geometric scaling allo-
not also hold for cross-taxa comparisons? metries result from the fact that ultimately
some components of organisms are of fixed trends. T h e fossil evidence clearly dem-
sizes (e.g., molecules and cells). In order to onstrates that with the demise of the dino-
maintain isometry of functional properties saurs, small mammal species rapidly
across major changes in size it is nearly adapted to fill niches for large bodied
always necessary for structures to enlarge forms. T h e mammalian radiations can be
at different rates. seen as markedly asymmetric with respect
Allometric analysis can help control for to body size (and correlated brain size). T h e
the influence of size, allowing one to com- lower limit of mammalian body size has
pare quantitative traits with the effects of probably not been significantly altered since
size subtracted. This "criterion of subtrac- the Paleocene but the upper limit has prob-
tion" is most often assumed to indicate that ably been extended about a millionfold
some functional relation has been main- compared to a typical basal insectivore!
tained in the face of the change in size. Brain size necessarily followed this trend,
This does not mean that such changes are although the extension of the upper limit
merely passive effects induced by the mass of'brain size, due to its negative allometry
of t h e organism. T h e y a r e inevitably with respect to body size, has probably not
"internal" facultative or genetic adapta- exceeded ten thousand times that of a typ-
tions to the imbalances or weaknesses ical basal insectivore brain. Parallel
induced by the change in size. Many of enlargement trends characterized numer-
these secondary adaptations may b e ous lineages of mammals.
encoded in the genome of the organism. I will argue that it is this remarkable par-
However, a trait that is somehow expressed allelism, and not some progressive selec-
facultatively, in a size graded manner, tion for increasing intelligence, that is
would have obvious advantages over one responsible for many pseudoprogressive
that is specific to a given range of sizes. In trends in mammalian brain evolution.
these cases size change should be consid- Larger whole animals were being
ered the "primary" adaptation and the selected-not just larger brains—but along
correlated reorganizations of structure can with the correlated brain enlargement in
be considered "secondary." each lineage a multitude of parallel sec-
A genetically encoded, size-correlated ondary internal adaptations followed.
trait that has evolved in response to the
functional demands of size change is a par- Allometry of brain traits any levels
adigmatic example of a derived condition. Mammalian brains range in weight from
But it also represents a conservative fea- around a gram to nearly ten thousand
ture to the extent that it is necessary to grams. Even within a single lineage like the
preserve some ancestral functional rela- anthropoid primates, in which individual
tionship. Functional homology is main- species share many strong similarities in
tained at the expense of structural homol- brain structure, there is more than a hun-
ogy. T h e reverse scenario is also possible— dredfold difference between the smallest
structural homology maintained by virtue and largest adult brains. Yet most micro-
of change in supportive functions to keep structural features change little in size from
pace with the effects of size. Finally, it is brain to brain. T h e maximum sizes of neu-
also possible for size change to be the "sec- ron and glial cell bodies increase slightly
ondary" adaptation. A change in size can from the smallest to the largest brains, but
be secondary to the production of some nowhere near the thousandfold scaling of
correlated effect that has itself become the the brains they comprise (Haug, 1987). T h e
trait of primary adaptive significance. This functional constraints on cell volume no
latter possibility will be suggested in the doubt set an asymptotic upper bound on
case of human brain size enlargement (see cell size that the largest neurons are likely
last section). approaching. T h e apparent tetraploidy of
In cases where size change is primary it the giant Betz cells of the human motor
would be inappropriate to consider the cortex likely indicates that these cells are
many secondary adaptations as progressive already forced to come up with unusual
ways to circumvent certain functional lim- projection neuron rnyelin sheath
smaller brain
variation (Rocket et al., 1980). This may
also be the reason that many larger scale
morphological features like cortical thick- larger brain
ness increase only slightly from the small-
est to the largest brains (Rocket et al., 1980).
As a cdnsequence the disparity between
microstructure organization and macro- rnyelin sheath
structure organization grows incredibly
with increasing size. Since the macro-
morphology of the brain, including
distinct homogeneous structures and their
various functional subdivisions, is derived
by ontogenetic processes that function at local circuit neuron
(e.g. granule cell)
subsequent Triune Brain hypothesis, the orderly addition of cortical areas in evo-
theory of the accretion of new cortical areas lution and the progressive elaboration of
necessitated a hierarchic conception of sensory motor processes in "higher" mam-
brain organization and function; Flechsig mals. T h e associationist assumption at the
(1900) and Campbell (1905) clearly artic- center of this theory was that higher order
ulated this complementarity between the mental associations are built from lower
FIG. 9. A graphic depiction of Campbell/Brodmann/Flechsig, Bonin/Sanides and Lende/Poliakov scenarios
for the addition or differentiation of new cortical areas in mammalian evolution. Although none of the
individual schemes is exactly identical with any other (and may not exactly correspond with those depicted)
they have been grouped into three distinct categories for depiction because of their underlying theoretical
similarities. T h e relative sizes of these brains are depicted in column A and show that the increase in distin-
guishable cortical areas is not independent of size. Column B shows an accretive scheme in which projection
areas a r e primitive and association areas are added derived characteristics in later brains. Column C shows a
progressive differentiation scheme in which association areas are considered most undifferentiated and there-
fore primitive and more specialized sensory and motor areas are assumed to be later derived conditions that
have differentiated in a series of stages out of previous levels of association cortex. Sanides additionally argues
that there is a dual origin of most major sensory/motor fields that determines differentiation at the intersection
of a dorsocaudally originating archicortical and a ventrorostrally originating paleocortical trend. This is not
depicted here. Column D shows a progressive differentiation scheme based on the parcellation and retraction
of initially diffuse overlapping projection fields into eventually discrete non-overlapping fields. T h e boundaries
of the initially overlapping projection fields are depicted by dashed lines. Later parcellation and reduction of
diffuse projections within each projection field is depicted as progressively darker regions of gray. T h e notion
of reduction of diffuse projections within a field is from Poliakov and is not discussed as a possibility by Lende,
whose theory focused only on the earliest stages of cortical evolution in mammals.
order simpler associations, and compli- the previous association area in the hier-
cated and flexible skilled responses are archy and provided an additional layer of
constructed by associations between sim- association processes superimposed upon
pler reflex responses. They argued that an already complete functional brain (see
association areas of cortex only received Fig. 9).
information from sensory projection areas Vestiges of this view are still widespread.
o r other association areas and served as the T h e pinnacle of this conception of the cor-
locus for higher-order associations between tical hierarchy is of course the addition of
sense data and motor programs from pri- language areas in the human brain-
mary areas. Association areas ultimately are inserted into an otherwise complete and
envisioned as an additional higher-order functional ape brain. T h e assumption that
reflex arc superimposed upon and elabo- Broca's area for speech is a new association
rating existing lower level reflex arcs area peculiar to the human brain has been
(Luria, 1980; Sherrington, 1906). There- represented in a number of schemes by the
fore association areas could be added as identification of some region within the
evolutionary after-thoughts with minimal third frontal convolution of the human
rewiring of other brain circuits. Each new brain that is assigned no homologous coun-
association area was one step removed from terpart in the monkey brain. T h e possibil-
ity that Broca's area has no prehuman by Allman (1990) and Kaas (1987, 1989).
homologue and could have been simply They argue that the multiplication of cor-
added on to an otherwise complete brain tical areas in many mammalian lineages
seems to be taken for granted in a number might be explained by the duplication of
of recent discussions of human brain evo- existing areas. They suggest that a new
lution (Passingham, 1981; Tobias, 1981; population of neurons could appear inter-
Falk, 1983) and language evolution (e.g., digitated in position between older popu-
Chomsky, 1972). Galaburda and Pandya lations as a result of some genetic accident
(1982) and Deacon (1984, 1988a, 1990c) that caused redundant production of the
provide architectonic and tracer evidence neurons from one of these regions (it is
that a homologue for Broca's area exists compared by Kaas, 1987 and 1989, to the
in the monkey brain, despite the fact that addition of an extra body segment in the
it plays no apparent role in vocal commu- evolution of lobsters; Gregory, 1935).
nication in monkeys. Recent studies of genetic mutants in fruit
A similar argument was presented by flies has demonstrated that at least in these
Geschwind (1964) and has been reasserted species genetic mutations can cause the
by a number of later writers concerning production of whole duplicate body sec-
the inferior parietal lobule of the human tions or limbs interdigitated between exist-
brain. Following the classic associationist ing structures. Allman (1 990) suggests
model of language processing, Geschwind that similar genetic mutations might
argues that this area plays a fundamental underly areal duplication events in mam-
role as an "association area of association malian cortical evolution. In fact, to account
areas." Its placement at the temporo-pari- for the number of such events that have
eto-occipital juncture seemed to ideally suit occurred this would have to be a somewhat
it for associating the outputs of association common sort of mutation.
cortices from different sensory modalities. It is unquestionable that new cortical
Since Geschwind conceived of word mean- areas have evolved in some of the larger
ings as complex associations between word mammal brains and that different lineages
sounds and a multitude of other sensory (e.g., cats and monkeys) exhibit different
associations abstracted from sensory expe- spatial arrangements and functional spe-
rience, an association area of association cializations of the cortical areas that have
areas would have to be the necessary sub- been added (Kaas, 1989). But is it reason-
strate for semantic processes. Posterior able to imagine that these areas have been
temporal-parietal-occipital damage often literally inserted between existing cortical
results in disturbances of semantic lan- areas by the addition of new neural tissue
guage comprehension. Geschwind argued in that position? This claim depends on the
that no homologue to this highest order possibility that functional areas of cortex
association area was evident in monkey are modular in their construction. T h e
cortices. According to this logic the addi- neurons that comprise a new cortical area
tion of this area during human evolution would need to be added along with speci-
was a necessary condition for language fications regarding intrinsic circuitry and
evolution. Language evolution becomes the afferent and efferent connections with
natural end point of a progressive process neighboring areas and subcortical sites.
of adding association areas on top of asso- This requirement is contradicted by
ciation areas in the course of mammalian developmental evidence that the afferent
brain evolution. This non-homology claim and efferent connections of a cortical area
has also been contradicted by subsequent are not specified by the information that
tracer experiments (e.g., Mesulam et al., is intrinsic to the cells in that area, but
1977; Seltzer and Pandya, 1980) and ani- rather by competitive interactions among
mal behavioral studies (e.g., Jarvis and competing axons from many areas. Even
Ettlinger, 1977). the transplantation of a section of cortex
Recently, a more sophisticated version into a novel position within a fetal brain
of an accretion theory has been suggested prior to the development of cortical con-
nections will not bring with it the functions less driven by reflex and habit. T h e newer
and connections appropriate to its site of the area then, the more indirect its link
origin (O'Leary and Stanfield, 1989; Stan- with the input and the more complex its
field and O'Leary, 1985; see discussion in functional properties. In this way the dif-
the next section). T h e transplanted area ferentiation of association areas from asso-
will develop functions and connections ciation areas could be correlated with an
appropriate to its new position. Thus, even additive functional hierarchy as well.
if some new area of cortex miraculously It turns out that many of the assumptions
appeared interdigitated between older cor- that initially supported this hierarchic
tical areas'in a developing brain it would scenario have been subsequently under-
not bring with it any new connectional or mined. T h e first difficulty to crop u p was
functional information. the discovery that association cortex did
not lack extensive subcortical connections
Is there an evolutionary sequence of (Diamond, 1982; LeGros Clark and North-
new cortical areas? field, 1939; Rose and Woolsey, 1949).
An alternative approach is to conceive Association areas cannot be conceived as
of new cortical areas as differentiating out added on top of a complete working sys-
of old areas rather than being created inde- tem, sending and receiving information
pendently adjacent to them. This has the only from adjacent lower level cortical
attractive property that new areas should areas. They have independent inputs and
continue to bear some functional and con- outputs and are thereby completely inte-
nectional interrelationship with their par- grated into the whole brain at every level
ent areas. Because there is a parent-descen- every bit as much as are "projection" areas.
dent relationship between areas there will More problematic still is the nature of these
also be an implicit sequential order of connections. T h e "highest" association
regional .evolution, depending on assump- areas exhibit extensive connections with
tions about the "initial brain." Correlated limbic cortical areas (Pandya and Yeterian,
with t h e order of the proposed evolution- 1985), whose evolution is presumed to pre-
ary sequence may also be an implied hier- date the evolution of primary projection
archy of increasing functional differentia- areas in all theories of cortical evolution.
tion and complexity. Recent tracer studies have also suggested
T h e comparative cytoarchitectonic stud- that association areas project to core mid-
ies of Brodmann (1909) and others brain and tectal areas and receive indirect
appeared t o corroborate associationist projections from these areas relayed
assumptions that association cortex was through the thalamus. They may even
newer than projection cortex and that some exhibit connectional topography that cor-
association areas could only be identified responds more to midbrain maps than to
in the most "advanced" brains. T h e order cortical sensory o r motor maps (Deacon et
of regional evolution of the cerebral cortex al., 1987). These features are also incom-
thus appeared to begin with primary sen- patible with the assumption that the "high-
sory receptive areas and motor output areas est" association areas are only connected
and involve the progressive differentiation with areas at the next hierarchic level down.
of ever higher association areas. In the ini- In many ways their principal links are to
tial state sensory and motor areas were some of the most primitive brain struc-
thought to be directly connected to one tures.
another to form direct reflex arcs. With Finally, there is the problem of archi-
the differentiation of new areas inserted tectonic a n d functional specialization.
between these primary areas the reflex arc Probably the most extreme architectonic
becomes more indirect and reflex action and functional specializations anywhere in
gives way to more complex and variable cortex can be found in the primary visual
associations between sensation and action. and motor areas of anthropoid brains. T h e
T h e more intermediate stages, the more primate striate cortex, for example,
complex the analytic capabilities and the exhibits highly derived cytoarchitecture
with distinct sublamination of layer IV, further specialized core areas developing
complex mosaic distribution of different within these specialized areas, and so on.
visual submodalities into a microscopic T h e ancient status claimed for association
matrix of architectonically distinct patches areas could account for their extensive
o r "tufts" (Livingstone and Hubel, 1988), connections with limbic structures and their
and approximately double the number of prominent links to midbrain systems. T h e
cells per cortical column of any other cor- progressive stages of differentiation also
tical area in any other mammal (Rockel et appear to correlate with connectional rela-
al., 1980). T h e s e a r e clearly recently tionships between cortical areas (Pandya
derived conditions that indicate a high and Yeterian, 1985). If it is assumed that
degree of functional and architectonic spe- cortical areas only retain connections with
cialization. T h e architecture of association their immediate precursors but not second
areas is generally less variable from area to generation precursors, this model could
area and species to species than is the explain the links between association areas
cytoarchitecture of specialized primary and limbic cortex as well as the lack of
areas (Sanides, 1970). This indicates that connections between limbic areas a n d
structural and functional specialization is either primary sensory-motor areas or their
not limited to and probably is less often adjacent belt areas.
exemplified in "higher order" association As noted earlier in this discussion, the
areas. most serious argument against Sanides'
Some of these arguments against the evolutionary sequence is the apparent exis-
classic view have also served as support for tence of specialized visual, auditory and
an almost exactly inverted view of regional somatic projection areas in all mammal
cortical evolution. Roughly inverted sce- brains, even in marsupials and mono-
narios have been proposed by Bishop tremes (Kaas, 1987). Even the primitive
(1959), von Bonin and Bailey (1961) and cortex of turtles exhibits representation of
Sanides (1969, 1970, 1975). Probably the visual and somatic responses in distinguish-
most ambitious and most widely adopted able regions crudely appropriate to their
of these is Sanides' theory of progressive topological position in mammalian cortex.
waves of cortical differentiation o r "Ur- An ancient status for these specialized sen-
trends." Sanides infers the sequential evo- sory areas contradicts Sanides' model.
lution of cortical areas from a trend toward One possible counter-response is to argue
increasing architectonic specialization that that the apparent homology between the
culminates in the evolution of specialized specialized primary sensory areas of
primary projection areas (see Fig. 9). Fol- advanced brains and the primary sensory
lowing the lead of Abbie (1942) and Dart areas of ancestral and conservative brains
(1934), Sanides argued that isocortical areas is incorrect. For example, von Bonin and
evolved from undifferentiated periallo- Bailey (1961) argue that the presumed
cortical zones along the borders of primi- homology between the hedgehog visual
tive hippocampal and olfactory cortex in a cortex and monkey primary visual cortex
series of stages of increasing differentia- is not supported by the cytoarchitectonic
tion. T h e trend is envisioned as a series of criteria Brodmann (1909) originally sug-
"growth rings" (Sanides, 1970) constituted gested. They conclude that it is far more
by progressively more specialized cortical similar to the more generalized areas of
areas differentiating out of relatively less visual association cortex. This interpreta-
differentiated areas. Areas that correspond tion is supported by the fact that in the
to the highest level association cortices in visual systems of the opossum and hedge-
the classic view comprise some of the most hog the thalamocortical projections of the
primitive ancestral areas in this view. T h e lateral geniculate nucleus (corresponding
most highly specialized areas in advanced to primary visual cortex projections) and
brains are envisioned to be the result of pulvinar nuclei (corresponding to extra-
specialized core areas developing within striate association cortex projections)
more generalized areas, and subsequently, extensively overlap (Diamond et al., 1985;
Kaas et al., 1970). Although the so-called of areas should be highest at its terminal
projection areas are specialized for receiv- end. If areas are capable of differentiatin g
ing relatively more direct information from out of other areas in the course of evolu-
peripheral sensors, all adjacent areas com- tion there should be an increasing number
prising a single modality receive indepen- of bifurcations as the process continues.
dent sensory afferents from the thalamus Each sense modality contains multiple asso-
and all share some thalamic connections in ciation areas at the same level of the cor-
common (Caviness and Frost, 1980; Dia- tical hierarchy but only one primary sen-
mond, 1982). sory area. This would not be likely if these
Hierarchic scenarios of cortical evolu- specialized areas represented a terminal
tion are appealing both because of their end in the evolutionary differentiation pro-
agreement with tacit assumptions about cess. And yet the extreme other end of the
mental progress and mental processes, and spectrum-paralimbic association areas—
because of the way they simplify the is not the level of the highest multiplicity
assumptions about connectional and func- of cortical areas either. In the visual modal-
tionaI integration associated with the addi- ity it appears that the most diversity and
tion of new parts to a complex brain. Add- multiplicity of cortical areas is found at
ing the new parts to the terminal end of a middle levels in the processing hierarchy.
growing hierarchy limits the presumed This is likely true of other modalities as
problems of integration with all lower well. This pattern is implausible in either
levels. It also provides an explanation for of the two general terminal addition sce-
the evolution of complex structures by narios.
demonstrating plausible intermediate steps Strict hierarchical terminal addition is
in complexity, differentiation and special- not the only possibility, nor is it necessarily
ization. One serious problem with both less complex than are non-hierarchic sce-
hierarchic schemes for explaining regional narios. Given that most cortical areas are
evolution of cortex is the constraint of the connected to more than one other area and
linear sequence itself. Ultimately, both the- that all are connected with distinct sub-
ories'are terminal addition theories. T h e cortical structures, there is no obvious sense
arguments in support of both are analo- in which a new cortical area can be thought
gous to those for terminal addition in gen- of as superimposed on an already complete
eral: addition of new structures to systems and functioning system-it must inevitably
that were complete in an adult of the pre- emerge in the middle of a complex inte-
ceding evolutionary stage; avoiding the grated network. Terminal addition con-
complication of inserting structural tributes no additional explanatory power
changes in the middle of a complex pro- toward solving the problem of the pre-
cess; and the assumption that additional established integration of new areas.
structures augment the function of the pre- Models of cortical evolution that make
ceding structures. As a result they are prone no assumptions about the order of appear-
to similar criticisms. It is not at all clear ance of cortical areas have been outlined
that cortical areas within any one brain are by Allman (1982,1990) and by Kaas (1987,
organized according to simple linear hier- 1989). They each argue that the multipli-
archies, nor is it obvious how cortical areas cation of cortical sensory areas of the visual
in different lineages can be homologized system can be explained by duplication of
with respect to a strict number of steps in existing cortical areas followed by subse-
the evolutionary sequence. For example, quent differentiation of function in the new
the primate visual system exhibits at least area. Presumably the new area will initially
two, and probably three or four, distinct share the same connections and cell types
processing pathways for different aspects as its older twin and gradually will come to
of visual perception that diverge from gain o r lose connections and exhibit mod-
striate cortex into distinct groups of asso- ifications in cellular architecture associated
ciation areas. Like a branching tree struc- with its changes in function. It is often the
ture, one would assume that multiplication case that adjacent cortical areas serving the
same sensory modality also exhibit con- might be too complex to be handled effi-
nections with similar structures elsewhere ciently by a single large visual area, do
in the brain-sometimes to separate divi- appear to be handled by only a few visual
sions of these structures, at other times areas in small brains. T h e r e is n o evidence
overlapping in connectivity, and it is not that "new" functions have evolved, only
unusual that neurons in common afferent that existing functions have become seg-
sources will send collateral branches of the regated and distributed to parallel visual
same axon t o adjacent cortical areas. processors. If processing all these modali-
Duplication of this sort would also account ties together in a single area is merely an
for the many striking homologies between efficiency problem, we should expect that
all isocortical areas. at least some very small brains would also
T h e duplication of an existing area is segregate visual functions into the almost
presumed to be a relatively innocuous acci- two dozen visual areas that endow large
dental mutation. However, the availability primate brains and that at least some large
of redundant areas frees one of the two brains would collapse visual processing into
from the constraints of the primary adap- only one o r two visual areas, but this is not
tation so that it is able to develop some seen. There are clearly size factors involved.
additional, complementary visual function. Accretion assumptions are not essential
In the primate visual system it is clearly the to explain the appearance of new cortical
case that distinct visual areas seem to be areas in mammalian evolution. A scenario
specialized for different submodality func- for the early stages of mammalian cortical
tions in vision, such as color, form and evolution was presented by Lende (1963,
movement perception. Thus, by duplica- 1969) that does not make any assumptions
tion and subsequent differentiation of about evolutionary precedence of cortical
function the entire collection of interde- areas. He argues that the pattern exhibited
pendent visual areas could have been pro- in the common ancestor to all mammals
duced. T h e apparently hierarchic arrange- (including marsupials and monotremes)
ment of these areas is not explicitly included cortical projection fields that were
explained in either model, but probably it extensively overlapping a n d t h e r e f o r e
could be argued that the one area that poorly differentiated from one another. By
retains the ancestral function becomes the a gradual process of differentiation over
more primary area and the differentiated the course of evolution each projection field
one becomes more secondary. Progression retracted with respect to the other until in
from one to the next in sequence could most modern species each projection field
then be explained simply on the basis of is exclusive of all others. In Lende's view
the influence of adjacent areas. the marsupial and basal insectivore cortices
Allman (1990) and Kaas (1987, 1989) represent a state where the retraction into
assume that new areas are added to an oth- separate territories is nearly complete, with
erwise complete visual system, inserted only somatic and motor areas still overlap-
between existing cortical areas. This is con- ping. Because it is purely a differentiation
sistent with their focus on advancement and model there is no addition of areas and no
augmentation of function as the prime distinction between old and new cortical
mover in the evolution of new cortical fields, just old and new patterns. A closely
areas-duplicated areas become recruited related theory of the evolution of connec-
to some new adaptive function that aug- tional differentiation has been proposed by
ments o r complements existing functions. Ebbesson (1980, 1984) and will be dis-
This argument is used to explain how dis- cussed in the next section.
tinct cortical visual areas have become spe- Lende's model was only intended to
cialized for distinct visual submodalities, explain the earliest stages of mammalian
such as color, movement, or form percep- cortical evolution (better resolution phys-
tion. A major criticism is that the separate iological recording techniques have largely
functional specializations of the different contradicted his claims about the lack of
visual areas, which Kaas (1989) suggests differentiation in primitive brains; Kaas,
isocortical evolution
by areal differentiation
FIG. 10. Depiction of a scheme of progressive differentiation of cortical areas from one another that does
not assume an evolutionary sequence in which some coexisting areas are older than o r ancestral to others.
T h e figures are meant to represent flattened cortical hemispheres with limbic cortical areas representing the
white perimeter of each and isocortical subareas represented by the gray areas contained within. Below each
of the three brains of increasing size is a block diagram of the ancestor-descendent relationship for the
progressive generation of new cortical subdivisions. T h e use of diverging shades of gray is intended to represent
the differentiation of both descendents of a subdivided ancestral area from the architectonic and functional
characteristics of this ancestor.
before duplication-addition after duplication-addition before axonal invasion after axonal invasion
/','
. . parcellation hypothesis equivalent cell population hypothesis
FIG. 11. Four commonly cited o r assumed rewiring hypotheses are depicted with source nuclei indicated by
shaded ellipses, cortical (or other nuclear) targets indicated by shaded boxes, and connections indicated by
black arrows connecting them. Antecedent and consequent conditions a r e shown in neighboring boxes. 'The
simple accretion hypothesis is depicted at the top left, in which a new structure is added t o the brain including
its own new connections. T h e invasion hypothesis is depictedat the top right, in which a new set of connections,
or connections originally targeting some other area, invade and establish synapses in a novel brain structure.
The parcellation hypothesis is depicted at the bottom left, in which previously diffusely interconnected
structures lose some of their diffuse connections in a complementary fashion so as to produce subdivisions of
each that are connectionally distinct. T h e "equivalent cell" hypothesis is depicted at the bottom right, in
which cells from one region migrate into another structure and attract their afferents t o this new structural
position.
ancestral condition
axonal connectivity
before allometric
reorganization
FIG. 14 . T h e displacement hypothesis is depicted with four possible interpretations of invasion-like effects.
In each case either the effective enlargement or reduction of targets or afferents (depicted by the size of the
structure) is invoked to explain the source of bias driving the displacement of connections from one target
to another. An analogous pattern could be produced by relative increases o r decreases of axon-target affinities
or by heterochronic advantages of some afferents over others that mature at different times. These could
also be depicted in this manner by assuming that the relative size of the structures depicted represents afferent-
target biases in general. Although displacement can also explain parcellation processes, these are not depicted
here. They would roughly follow Ebbesson's schema with the added provision that parcellation is not spon-
taneous, but must be induced by a change in the relative numbers of target synapses with respect to competing
axons o r changes in axon-target affinities. Even if enlargement of both afferent and target populations during
generalized size increase is isometric, there may be limited collateral extent of correlated axon activity such
that diffuse overlap of connectivity could not be maintained and axons from the same source would have a
better chance of eliminating interdigitate axons from more diverse origins.
hood of synapse formation with respect to hypothesis it assumes that the basic molec-
axons arriving out of synch with cell mat- ular affinities between initial connections
uration. As a result heterochronous and their targets a r e essentially conserva-
changes in developmental time schedules tive, and if anything, only change in
for different systems may be a source of response t o prior displacement events,
developmental bias analogous to differ- under selection to stabilize a newly adap-
ences in size of competing projections. T h e tive circuit against the regressive influ-
increased affinity for synchronously arriv- ences of competing biases. What is missing
ing axons should have the same effect as from both invasion and parcellation the-
relative enlargement of one source or tar- ories is a cause. Displacement theories
get area with respect to another. introduce cause in the form of regressive
Both invasion-like and parcellation-like processes (e.g., cell death or reduction of a
processes are explainable in this way. What peripheral sensory o r motor system) o r dif-
is different about displacement hypotheses ferential growth processes (e.g., unequal o r
is that they propose that all such events are hyperplasic neuron production, expansion
driven by competitive biases between dif- of some peripheral organ, o r hetero-
ferent axon populations and their pro- chronic change in maturation schedules for
spective targets and not by instructional different structures).
processes such as might be encoded in Finlay et al. (1987) suggest that regres-
molecular affinities. T h e strong form of sive events during development, such as
the displacement hypothesis denies both cell death and axon retraction, may account
the possibility of spontaneous axon inva- for total brain size variation, the elabora-
sion and also the possibility of spontaneous tion of specialized sensory, motor or cog-
parcellation. But like the parcellation nitive adaptations, and allometric dispro-
portions of specific systems during brain tor in major allometric changes. First, in
evolution. Widespread cell death appears order to play a significant role it must be
to be a normal developmental mechanism able to account for at least a major part of
for sculpting cell populations of intercon- the many thousandfold differences in brain
nected structures. T o a limited extent cell size. Small brains are simply not analogous
death may be exaggerated or eliminated to large brains that have experienced 99%
by variations in afferent populations o r cell death. T h e role of cell death is clearly
efferent associations. These effects are, limited to secondary "fine tuning" of inde-
however, buffered in systems with multiple pendently developed functionally inter-
afferent sources and efferent targets, and dependent systems (although it may reach
so can be expected to be most significant 80% in peripheral receptors). Second, as
in systems with highly limited connectional compared t o peripheral systems, the evi-
relationships. Neural populations of dence suggests that the total amount of cell
peripheral sensory and motor projections death is relatively small in most forebrain
a r e generally entirely dependent o n structures, even if peripheral structures
peripheral structures as afferent sources or relaying information to them are signifi-
efferent targets, respectively, and provide cantly reduced (Rakic, 1988). This prob-
the most notable examples of variation in ably correlates with the fact that forebrain
cell death. structures receive afferents from and send
A number of the changes in CNS orga- efferents to diverse cortical and subcortical
nization in response to the evolution of structures rather than just one, as in
novel sensory organs o r motor systems may peripheral structures. T h e cell d e a t h
thus be the result of such a sculpting pro- reported in areas like cortex appears t o be
cess. Wilczynski (1984) reviews evidence associated with cells maintaining transient
for the neural reorganization of CNS cell synapses during early phases of develop-
populations and connections in response to ment that may serve a preliminary organ-
some major vertebrate sensory and motor izing role for later stages. If there was sig-
specializations (e.g., auditory, electrical and nificant cell death in t h e normal
infrared reception) that show relatively development of cerebral cortex it would
subtle differences centrally in response to have to be relatively uniform because of
major changes of the periphery. Despite the remarkable uniformity of cell numbers
homoplaseous peripheral changes, central per area in all areas and all species. T h e
reorganization often recruits homologous initial production of neurons (or the initial
systems for similar perceptual processes. production of "ontogenetic units" with
H e argues that the interlocking of periph- fixed neuron production patterns) is prob-
eral and central reorganization in these ably much more important in determining
cases arises out of competitive develop- populations in most structures.
mental processes that match peripheral Finlay et al. (1987) also point out the pos-
functional requirements to central func- sible significance of heterochronous mat-
tional predispositions and match cell pop- urational processes for both cell death and
ulations to one another. Although there connectivity patterns. They argue that ear-
may be major changes in cell number in lier maturation or delayed maturation of
peripherally specialized nuclei as a conse- areas may introduce competitive biases in
quence of cell death there appear to be no normal axonal competition. Since some
"cascading" effects on cell death through- competitive processes may extend for only
out the remainder of their functional con- a few days, significantly delayed o r pre-
nections within the CNS. mature connections may be left out of the
T h e main point of the cell death hypoth- competition, with cell death o r connec-
esis proposed by Finlay et al. (1987) is to tional replacement resulting. Although
account for quantitative allometric changes Gould (1977) argues for the widespread
in the brain and brain structures. How- presence of heterochrony in other systems
ever, there are a number of reasons why (e.g., somatic growth and puberty) there is
cell death is unlikely to be a significant fac- little evidence concerning variance of mat-
uration schedules in the mammalian ner- Armstrong, 1985; Campos and Welker,
vous system at this time. However, time 1976; Deacon, 1988b; Gould, 1975; Pas-
scale effects may be significant in mam- singham, 1975; Sacher, 1970; Stephan,
malian brain evolution. T h e maturation of 1969). T h e systematic differentials in neu-
a small mammal brain may b e completed ronal production in different structures in
within the space of weeks whereas that of brains of different sizes should determine
a large brain may take many years. This correlated differences in structural parcel-
means that the absolute time scale of com- lation throughout. For example, the reg-
petitive-regressive events during matura- ular increase in proportion of visual asso-
tion can differ enormously despite the like- ciation cortex with respect to visual
lihood thqt, at the synaptic and cellular scale koniocortex in brains of increasing size may
the trophic processes that underly these reflect a growing competitive disadvantage
effects are the same for all mammal brains. for primary projections in the recruitment
T h e prolongation of these events in larger of cortical space determined by a growing
species might affect variability, degree of disproportion between the retina and its
differentiation o r sensitivity to extrinsic potential thalamic and cortical targets.
influences. In non-mammalian vertebrates As we examine species differences in
where neurogenesis may persist through- neural organization we should expect to
out the lifespan heterochrony may be a see certain necessary correlations between
more significant factor. changed connection patterns and the allo-
In previous papers I have also proposed metries of the various structures involved.
that axonal competition and other regres- For example, in cases where an invasion
sive processes play crucial roles in brain event is suspected to have taken place one
evolution (Deacon, 1984, 1988b, 1990c), would expect to find some corresponding
but I have focused largely on the possible deafferentation of the new target by a for-
influences of size relationships. If the mer projection source that has regressed
determination of initial cell number in most in size with respect to its target, o r some
structures takes place prior to major axonal unusual size increase in the new source
invasions, the major role of competitive and structure relative to its normal target, o r
regressive processes must be the subdivi- significant regression of its normal target.
sion of these neurogenetic fields with In cases where loss of connection is sus-
respect to each other. Even though no cell pected either cell death in the source or
death nor substantial cell saving may result target or, alternatively, displacement by a
from increases o r decreases of specific projection from a disproportionate com-
afferents o r efferent targets of a multiply peting afferent source would be expected.
connected structure within the CNS, such Failure to find these correlates either in
changes can substantially alter local axonal adult brains o r during development would
competition processes. Rather than axonal falsify a displacement interpretation.
competition determining the size of brain Displacement hypotheses are falsifiable
structures via cell death (probably only sig- in ways that parcellation o r invasion
nificant for peripheral structures), the rel- hypotheses are not because a displacement
ative sizes of interconnected brain struc- explanation is an account of a mechanism
tures should be a major determinant of not merely of a change in structure. T h e
patterns of axonal connection. displacement hypothesis is essentially an
Allometric effects are probably the most extension of well studied mechanisms of
common sources of bias, given the enor- developmental axonal plasticity. T h e pro-
mous range of brain sizes and the great duction of topographic functional and con-
ranges in the relationships between central nectional organization within a developing
and peripheral systems. These effects are area induced by reduction o r over-exag-
not limited t o unusual reorganization geration of input from some outside source
events. Deviations from isometry with phy- is the limiting case for developmental dis-
letic size increase is the rule among brain placement. T h e extension of this concept
structures as in peripheral organs (e.g., to incorporate allometric influences as a
major source of bias on major projection both its normal target and nearby low affin-
patterns completes the synthesis of allo- ity targets.
metric effects, neogenetic processes and An experimental example demonstrates
developmental processes. this possibility. Frost and Metin (1 985) and
Displacement interactions can also con- Sur et al. (1988) have demonstrated the
ceivably account for true invasions of axons possibility of inducing optic afferents to
into targets that even exuberant projec- project to inappropriate thalamic nuclei
tions would not otherwise contact. It is not and thus relay inappropriate sensory infor-
necessary to assume any changes in the mation to their cortical target areas. T o
actual affinities of axons for their targets, accomplish this in a developing rat they
only t h e reduction of t h e specificity destroyed all the normal targets of the optic
requirements for target affinity. This may projections (including lateral geniculate,
occur under some extreme conditions. In superior colliculus and visual cortex) and
an earlier section it was noted that the ini- additionally deafferented another tha-
tial target specificity of many neural con- lamic nucleus (e.g., either the ventrobasal
nections is significantly underdetermined. o r the medial geniculate nucleus) by cut-
This has been best documented for cortical ting ascending (spinothalamic o r tecto-
afferents and efferents but has also been thalamic) fibers. One of these procedures
noted widely in the developing nervous sys- is diagrammed in Figure 15. Despite the
tem. As a result, initial axonal projections fact that the misrouted connections inner-
invade a multitude of diffuse targets and vate anomalous thalamic targets which
may establish numerous transient synapses project t o non-visual cortical areas, cells in
that will later be eliminated. There prob- these areas exhibited response properties
ably are some predetermined affinity gra- appropriate t o visual cortex. This dem-
dients involved because these initial pro- onstrates that fundamental rewiring is
jections are far from entirely random. achievable by displacement and that the
Edelman (1987) has argued that this initial new connections thereby established can
affinity between axons and potential target differentiate their targets appropriate to
cells is the result of specific cell surface their new functions. However, it may be
molecules that exhibit a range of interac- significant in these cases that the alternate
tion o r "recognition" strengths (analogous thalamic and cortical targets are homolo-
to immunological binding relationships). gous with the normal targets at some level.
In order to produce distinct connections Similar natural experiments appear to be
these affinities need not be highly specific exhibited by different breeds of Siamese
so long as there is either a significant cats. These cats all have abnormal routing
threshold difference between nearby of ipsilateral projections to the contralat-
potentially competing projections or a era1 lateral geniculate with the result that
means for dynamic parcellation of rela- the visual field maps are misaligned. When
tively nonspecific projections, as is found the lateral geniculate projections reach the
in cortex. Extremely weak axon-target cortex they are dealt with in one of two
affinities can likely only exhibit themselves ways depending on the breed: 'they are
when all competing affinities are essentially either inactivated so as not to interfere with
eliminated o r when extremely strong com- the remainder of the map o r form an iso-
petitive biases are introduced. Elimination lated independent map that' is inserted
of alternative stronger affinity competitors adjacent to the otherwise normal map (Kaas
can occur if the majority of normally and Guillery, 1973; Guillery, 1974). What
occurring transient and permanent affer- factors bias the axonal competition toward
ents to an area are eliminated, o r if a nor- one o r the other option are not known.
mal target is essentially eliminated, forcing Analogous competitive processes may
axons to compete for alternative low affin- underly the evolution of new cortical areas.
ity targets. Strong biasing may also occur Simple invasion is astronomically unlikely
if a weak affinity afferent source becomes because it can only occur when there is a
disproportionately large with respect to significant loss of target affinity in one set
of axons and simultaneously a significant
increase in affinity for that same target area
by other axons that have also simulta-
neously lost affinity for their own target.
Each of these conditions involves an inde-
pendent mutational event that alters the
respective cell surface molecules or causes
certain whole classes of cells to die. In con-
trast, invasion by displacement need not
involve any changes in affinity o r signifi-
cant cell death. T h e only conditions
required are either significant allometric
disproportions between areas or the elim-
ination of some target area o r the elimi-
nation of some projection as a result of
some. degenerative event in evolution.
These conditions are probably not at all
uncommon in the course of evolution. Sig-
nificant allometric changes in proportions
between different structures and projec-
tion systems is the rule in all mammalian
and nonmammalian lineages where brain
size has changed by many orders of mag-
nitude. Such a principle may account for Normal connections
the parcellation trends in neocortical areas
seen in larger mammalian brains.
FIG. 17. Laminar segregation of corticocortical connections due to functional parcellation of cortical areas
is depicted on the assumption that both the ancestral and developmentally prior state are an undifferentiated
laminar termination pattern. The hypothesized undifferentiated state is depicted in the upper figure as a
single cortical area with intrinsic connections. The subsequent loss of selected classes of connections with area
parcellation is depicted in the lower figure. Note that the culled connections are asymmetric with respect to
their directional orientation. Possible sources of competitive bias that might drive this asymmetric parcellation
during development are discussed in the text.
to explain this correlation between archi- This suggests that we should look for cor-
tectonic gradients, asymmetrically pat- responding biases, either in terms of het-
/
terned reciprocal connections, inverse erochronic, allometric o r functional dif-
maturational gradients, and the apparent ferences, that distinguish association areas
functional hierarchy of cortical areas in from specialized sensory/motor areas. In
terms of competitive biases and displace- fact, all three possible sources of bias can
ment processes in cortical development. be identified and are probably not inde-
At the present time there is no devel- pendent.
opmental information concerning corti- Another important clue concerning the
cocortical laminar differentiation pro- particular cortical lamina that distinguish
cesses. Nonetheless, speculation concerning these different cortico-cortical projections
the possible mechanisms involved can be comes from the finding that different
concentrated on a few plausible factors. For classes of thalamo-cortical projections also
corticocortical connections within a corti- appear to segregate according to termi-
cal area there does not seem to be this level nations in these same lamina. Multiple tha-
of laminar specification (Rockland and lamic nuclei project to each cortical area
Pandya, 1979). T h e differentiation of a new but tend to terminate in different lamina
cortical subdivision out of a single ancestral within the same area. It appears that prin-
area must therefore correlate with a loss cipal thalamic projection nuclei, whose
of projections to certain cortical lamina. projections are generally limited to a single
Furthermore the loss is different depend- architectonic area, tend to terminate in
ing upon whether the projection is in the columnar fashion within layers III and IV,
centrifugal o r centripetal direction. Since usually coinciding with the distribution of
the appearance of a new cortical division granule cells in those layers (Diamond,
must be a consequence of the competitive 1982; Frost and Caviness, 1980). Intralam-
parcellation-displacement processes, these inar thalamic nuclei, which exhibit rela-
systematic connectional losses likely cor- tively non-specific projections to many cor-
relate with competitive asymmetries tical areas, tend to terminate in layer VI
between different afferent populations. (Frost and Caviness, 1980; Herkenham,
1980; Rausell and Avendano, 1985). Other
nonspecific nuclei that project to many
areas within the same modality and midline
"limbic" nuclei, which also exhibit wide-
spread paralimbic cortex and association
cortex projections, tend to terminate in
layer I (Diamond, 1982; Friedman et al.,
1987; Frost and Caviness, 1980; Rausell
and Avendano, 1985). T h e non-specific and
limbic nature of thalamic projections t o
layers I and VI and the specific projections
to layers III and IV can be interpreted as
functionally analogous to their counter-
parts among cortico-cortical projections in
a number of ways. Middle layer projections
appear always to introduce information
associated with a source that is more
centripetal directly connected with the peripheral ner-
vous system than are their target, whereas
deep and superficial layer connections
appear to convey information that ulti-
mately derives from systems involved more
with the regulation of internal state, as well
as attentional and emotional arousal (Dea-
con, 1989).
Two important heterochronic matura-
tional factors differentiate cells and axons
in these cortical lamina. These correlated
heterochronic differences may account for
which lamina tend to be associated with
which afferents by virtue of their biasing
influence on axonal competition. Neurons
occupying positions that would be super-
ficial to layer II and deep to layer VI in the
adult brain mature before the cells of the
cortical plate and form a single primordial
centrifugal cortical layer. Cells in the outer layer called
FIG. 18. Centrifugal and centripetal corticocortical Cajal-Retzius cells exhibit two large
projections are depicted on idealized flattened maps "extraverted" dendrites that extend up
of the cerebral cortex of one hemisphere. Areas toward t h e pial surface a n d laterally,
depicted in darkest gray are koniocortical areas o r
specialized motor cortex, those in lightest gray are whereas cells in the deep layer called Mar-
association cortex, and the white perimeter repre- tinotti cells are of a distinct bi p olar shape
sents limbic cortex. T h e arrows represent multisy- with dendrites extending more superfi-
naptic pathways from area to area extending either cially a n d deeper. Cortical plate cells
from koniocortex (or motor cortex) to intermediate
association cortex to paralimbic association cortex to migrate into position in an inside-out pat-
limbic cortex (centripetal) or from limbic cortex to tern between these two cell layers. T h e ear-
paralimbic association cortex to intermediate associ- liest cortical plate cells to mature are the
ation cortex to koniocortex (or motor cortex). T h e deep layer V and VI pyramidal cells and
terms centripetal and centrifugal are chosen not the very last cortical plate cells to mature
because of their spatial connotations (which may be
somewhat confusing in this depiction) but because of are the most superficial pyramidal cells of
the orientation of these projections with respect to layers II and III and the granule cells of
the gradient between areas specialized for peripheral layer IV. Prior to the appearance of the
systems and those representing regulation of internal cortical plate neurons both primordial cell
state.
types appear to establish transient synapses
with early afferent projections (Marin-Pa- tition for synapses in the middle cortical
dilla, 1978). Although there is some dis- lamina may be biased by earlier myelina-
agreement on the ultimate fate of these tion of ai-eas that are more peripherally
early maturing cells most argue that they specialized.
are eliminated by programmed cell death An allometric bias is reflected in the
in most isocortical areas (although they expansion of association areas relative to
appear to pqrsist in entorhinal cortex and sensory/motor specialized areas in larger
in paralimbic isocortex in small species, and brains. As noted above, this suggests that
in all cortical areas in cetaceans; see next primary projection areas, which are more
section). directly linked to peripheral systems, are
Although it is not known what structures competitively constrained by the size of
give rise to the afferent projections that their afferent projections, whereas affer-
synapse on the transient cells above and ents to association areas have no such
below the developing cortical plate, it is extrinsic constraints. This may also be the
reasonable to assume that they arise from reason these areas appear to exhibit less
the same structures that will later inner- clearcut cytoarchitectonic divisions. T h e
vate' the corresponding deep and superfi- gradient in architectonic specialization is
cial lamina in the adult. T h e fact that the one of the primary bases for Sanides' argu-
thalamic afferents terminating in layers I ment.
and VI are nonspecific projections and do Functional differences are also consis-
not appear to respect cortical boundaries tently correlated with this gradient. For
(Caviness and Frost, 1980; Diamond, 1982) example, neurons in striate cortex appear
may reflect their arrival prior to cortical to be precisely "tuned" to specific, highly
plate afferents that subdivide the cortex localized stimulus attributes and are orga-
into-:discrete functional regions. If the nized according t o precise retinotopy
transient 'cells to which these early axons whereas neurons in inferotemporal visual
/
contact are later eliminated, these axons association areas, at the extreme opposite
may be displaced onto adjacent pyramidal end of the hierarchy, seem tuned to global
cell dendrites in the deepest and most stimulus attributes and exhibit very large
superficial lamina of cortex (see Fig. 19). receptive fields with no obvious topo-
Since different target cells within the cor- graphic organization. This is undoubtedly
tex mature at different times and different also a correlate of the relative directness
projections arrive at different times, tem- or indirectness of their respective retino-
poral correlation may play an important cortical afferent circuits (Kaas, 1989). At
role in biasing laminar connection patterns the sensory end of the spectrum of areas
from both thalamic and cortical sites. Early input from the periphery is highly variable
maturing cells located deep and superficial and functional correlation is only exhib-
to the cortical plate may correlate with the ited over very short distances, whereas at
early maturing projections and late matur- the association end input is primarily lim-
ing small cortical plate cells in layers III bic and likely highly intercorrelated over
and IV may correlate with relatively late relatively larger distances. Since functional
maturing projections. Differences in the specialization of cortical areas can be sig-
relative maturation times of cells and axons nificantly affected by sensory experience
from one cortical area to another might during early development it is almost cer-
additionally contribute to areal differences tain that differences in the correlation of
in laminar organization. afferent signals among adjacent axons play
Another possible heterochronic bias that a major role in determining which con-
may influence the asymmetric direction- nections persist into adulthood.
ality of these projections can be discerned Finally, the issue of network allometry
in the differential myelination of thala- should be considered. Given the fact that
mocortical fibers from principal thalamic break-up of previously integrated func-
nuclei projecting to these areas. Since my- tional areas effectively distributes process-
elination appears to precede from special- ing across a number of areas, functioning
ized areas to association areas the compe- to some extent in parallel, cortico-cortical
Pattem of isocortical neurogenesis
and probable programmed cell death
this degenerative process left because cial to the persistence of this trait. Consider
immature dolphin brains do exhibit a tran- the significance of the regression of many
sient but thin layer IV that disappears by specific sensory and motor systems in these
maturity (Garey and Leuba, 1986). It seems species associated with their aquatic adap-
unlikely that this loss can be rationalized tation. They are anosmic, they have sig-
as an adaptation. Given the total break- nificantly reduced visual requirements (and
down of cortical differentiation processes in this regard are comparable to fossorial
that resulted one would presume that this species and echolocating bats with second-
is a costly mutation, although even in the arily reduced visual systems), and they
mutant Reeler mouse, with its totally dis- exhibit significant reduction of the distal
rupted cortical architecture (but not lack- limbs, shoulder girdle and pelvis (which in
ing granule cells), the cortex still functions terrestrial vertebrates comprise the pre-
and allows for adequate perceptual and dominant afferent and efferent represen-
motor functions. T h e fixation and survival tation of the primary somatdsensory and
of this trait in cetaceans as opposed to any motor fields). Although many species have
other terrestrial lineage may be related to highly developed echolocation systems, this
their unusual and relatively complete adap- appears far more substantially represented
tation to the aquatic habitat. T h e lack of by collicular specialization (evidenced by
"granularized" competitors (e.g. , pin- the immensely expanded and highly dif-
nipeds) in this niche until much later in ferentiated inferior colliculus) than by cor-
mammalian evolution may have been cru- tical specialization. All these regressive fea-
tures appear to coincidentally correlate monkeys in one case and capuchin mon-
with the inability of the dolphin cortex to keys in the other) and one Old World mon-
architectonically differentiate. key's brain (Cercopithecus talapoin), than to
In summary, this exception appears t o the brains of any other Old World mon-
prove the rule in a rather striking and keys and apes. It is probably not coinci-
unambiguous way. T h e problems of deter- dental that those primates most closely
mining whether the dolphin brain is con- linked with Homo by these studies also rep-
servative or advanced o r conservative- resent relatively encephalized primates.
advanced are irrelevant. T h e dolphin brain When a structure by structure allometric
is none of these. It is highly derived. These analysis is performed it appears that the
problems that arose in the analysis at the human brain diverges from primate trends
level of comparative morphology and com- in a number of striking ways. Based on pre-
parative cytoarchitecture dissolve once we dictions from primate trends, the cerebral
approach the question from the perspec- cortex and cerebellar cortex of the human
tive of developmental homologies. brain are disproportionately large relative
to the diencephalon, corpus striaturn, brain
Human brain evolution stem and spinal cord (Deacon, 1984,
Assumptions about human brain evolu- 1988b). This is depicted in Figure 22.
tion are the ultimate source for many of T h e production of neurons that consti-
the misleading ideas that have haunted the tute cortical structures takes place well
study of brain evolution, so it is fitting that before any axonal parcellation processes
the exorcism of these ideas in this paper begin, and therefore, as noted earlier, the
should conclude with a discussion of the increase in cerebral cortex cannot be spe-
uniqueness of human brain evolution. Two cific to any particular region of cortex. T h e
unique characteristics of the human brain increase in radial dimensions of the cortical
stand out as central. T h e human brain is germinal field and in the number of onto-
roughly three times larger than would be genetic columns that will differentiate out
predicted for an anthropoid primate of of it must take place in the human brain
human body size, and human brains are prior to neural production within the cor-
capable of acquiring an unprecedentedly tex. T h e size disproportions between the
complex and flexible communication sys- expanded neocortical target field, the rel-
tem- language. T h e s e two facts a r e atively unexpanded population of thala-
undoubtedly linked. mofugal axons, and the relatively unex-
Beginning with the issue of human brain panded efferent subcortical targets of
size, it is important t o find out if this cortical neurons must significantly bias
increased cell production follows trends parcellation processes in all these areas
that are typical in other members of the during subsequent stages of differentia-
primate order. This can be ascertained by tion. One effect of this is apparent in devia-
comparing the relative sizes of the various tions of relative cortical area dimensions
major structural divisions of the human with respect to predictions based on the
brain with predictions based on trends for allometry of these structures in other pri-
primates in general. Initial evidence that mates. Some cortical areas appear signifi-
there is a deviation from predicted allo- cantly smaller than expected for a primate
metries comes from an examination of brain this size and others significantly
studies that have used brain structure vol- larger. For example, the visual cortex
umes to construct possible phylogenetic appears to scale appropriate to the size of
trees for primate ancestry. Two studies, its peripheral input (the retina) and its
using largely similar data but different principal thalamic nucleus, but does not
methods that control for the effects of brain occupy the proportion of cortex predicted
size (Douglas a n d Marcellus, 1975; for a primate brain of this size. Its periph-
Bauchot, 1982), have concluded that the eral sources are constrained by the small
human brain is more similar to either one human body size with respect to the large
of two New World monkeys' brains (woolly brain size. As a result they d o not scale to
thalamocortical parcellation thalamocortical parcellation
process in a brain with typical process in the human brain with
primate cortical nuclear proportions disproportionately enlarged cortex
FIG. 22. Schematic diagram of large-scale human
brain structure disproportions and their effects on
axonal competition processes during human devel-
opment as compared to development in the absence
of these human disproportions. With respect to the
predictions based on other primate brains, human
cortical structures (including the entire cerebral and FIG. 23. A diagram of some of the relative propor-
cerebellar cortices) are larger than expected with tions ofcortical fields in the human brain as compared
respect to brainstem, cerebellar, diencephalic and to predictions based on typical anthropoid primate
telencephalic nuclear structures. Since the cell pro- trends. T h e percentages represent absolute devia-
duction processes which determine the gross size of tions from the predictions for a primate brain of human
these major morphogenetic fields are completed prior size. Temporal, parietal, and motor area predictions
to their parcellation into functional subdivisions it is are based on too few data points to be significant, but
predicted that these disproportions will result in biased demonstrate a pattern that is consistent with the find-
displacement processes. T h e typical condition is ings for other areas and with the displacement
depicted by the three brains on the left. Brains A and hypothesis. T h e depiction of peripheral structures
B represent the normal developmental stages of cor- associated with different cortical areas is intended to
tical axonal parcellation of visual (gray cortex with indicate that cortical areas with relatively direct rep-
gray dashed arrows as afferents), somato-motor (black resentation of peripheral sensory o r motor systems
with black arrows) and prefrontal (gray with solid gray are constrained by these afferents or efferents in their
arrows) cortical fields in a large primate. T h e human competition for cortical representation. Figure taken
deviation from this is depicted by the three brains on from Deacon (1990b).
the right. Brains C and D represent the human devel-
opmental stages with constraint of visual and somatic
fields by their unexpanded peripheral afferents and motor areas as well as for visual areas (Dea-
displacement by prefrontal afferents producing a much con, 1984, 1988b; see Fig. 23).
enlarged adult prefrontal area. T h e competitive limitation of these pro-
jection systems translates into a competi-
tive advantage for other areas not con-
the level that would otherwise be predicted strained by peripheral afferents, which
on the basis of brain size (a brain this big must inherit the cortical surface area that
would be expected only in a very very large is left unrecruited as a result. T h e pre-
ape-the "King Kong" null hypothesis of frontal zone appears to be one major ben-
human brain evolution). T h e competitive eficiary of this competitive imbalance. It is
limits for these afferent systems are con- estimated to be approximately twice the
strained by the size of the peripheral input. size expected for a primate brain of human
Preliminary data suggest that this is prob- proportion (and this translates to six times
ably also the case for auditory, somatic and the size predicted for a primate of human
FIG. 24. Some predicted connectional consequences of prefrontal enlargement are represented by brain A
(typical primate brain structure allometry) as compared to B (human cortical-nuclear disproportion). Dis-
placement theory suggests that the enlargement of the number of prefrontal efferents competing for midbrain
targets as compared to diencephalic efferents will bias competition in favor of prefrontal projections which
will displace both some diencephalic, limbic and intrinsic midbrain axons from their normal targets. This may
lead to the relative dominance of prefrontal outputs over limbic and diencephalic outputs in control of midbrain
and brainstem vocalization centers and motor circuits. This may be linked to adaptations associated with
language skills and the loss of many stereotypic vocalizations in human evolution.
body size; Deacon, 1 984, 1 988b). Prefron- projections from the central gray and retic-
tal cortex is not a recipient of peripheral ular formation. Many of these prefrontal
inputs, but of inputs from other nonspe- and limbic cortical targets turn out to play
cific and polymodal systems of the mid- major roles in vocal call production in pri-
brain and cerebral cortex. It is thus buff- mates. T h e displacement of "normal"
ered by being synaptically removed from afferents of these areas and replacement
the cascading effects of peripheral bias that by a larger fraction of prefrontal axons may
affect other systems. It is probably not inci- have significantly altered their function.
dental that Broca's area for speech is con- Deacon (1990c) argues t h a t this may
tained within this enormously expanded account for the significantly reduced rep-
field. ertoire of stereotypic call types in humans,
This disproportionate prefrontal corti- as well as for the recruitment of some of
cal surface area is a secondary consequence these systems by cortical areas capable of
of the initial disproportion of the entire supporting complex skilled motor pro-
embryonic cortex with respect to its sub- gramming. T h e disproportions among
cortical-peripheral connections. These ini- cortical areas and the relative reduction of
tial disproportions biased axonal compe- thalamocortical as opposed to corticocorti-
tition for cortical representation in favor cal axons undoubtedly also played a role
of cortical areas whose afferents were not in altering cortical functions, some of which
constrained by peripheral systems. But this are related to the human language capac-
secondary disproportion of prefrontal areas ity.
itself must have other tertiary biasing con- Human brain evolution cannot be con-
sequences. Deacon (1990c) notes that effer- ceived in the terms of a conservative-pro-
ent projections of this system target limbic gressive scheme of mammalian brain evo-
cortical structures and a range of midbrain lution. Our brains are not at the pinnacle
structures. We can expect prefrontal pro- of any evolutionary trend. Rather the
jections to have a significant competitive human brain is an unusual divergent case.
advantage over other afferents to these T h e extreme disproportion of human brain
areas during development (see Fig. 24). T h e size with respect t o the human body size
midbrain targets of prefrontal projections with respect to other primates and mam-
also receive descending limbic cortical and mals is only a surface manifestation of a
hypothalamic projections and intrinsic complex allometric reorganization within
the brain, and is unlikely itself to be the and developmental strategies can lead us
crucial trait under selection in human evo- beyond a merely superficial understanding
lution. It is not just the increase in cortical of function to appreciate some of the
complexity nor the increased relative size deeper fundamental organizing principles
of the whole brain but the correlated reor- shared by all features of the brain.
ganization of underlying neural circuitry Neither the study of mammalian brain
that is probably most significant to human evolution nor even the study of human
uniqueness (see also Holloway, 1979). brain evolution is limited to merely theo-
Because the data that we possess con- retical exploration. We currently have
cerning the human brain are still neces- access to experimental tools that are ade-
sarily limited to morphological informa- quate to the task of analyzing the neural
tion and notably do not include detailed developmental processes that underly, can-
connectional data (due to the invasive alize and constrain brain evolution, and are
nature of present tracer techniques) direct capable of gathering the sorts of compar-
verification of these hypothetical reorgani- ative anatomical evidence that can eluci-
zations will have to wait. However, our date the variety of ways these processes
understanding of the processes that must have been expressed in evolution. This is
underly development of a brain with the an invaluable complement to other areas
allometric characteristics of the human of the neurosciences that are rapidly build-
brain can be further augmented by con- ing a database of comparative physiologi-
tinuing investigations of the relationships cal and behavioral information. O u r fail-
between allometric and developmental ure to immediately grasp the significance
processes shared by all mammals. T h e of these data for brain evolution has largely
details of human brain evolution are still been the fault of the unrecognized influ-
largely obscure. T h e hypotheses presented ence of some very old notions about evo-
here are based on a massively incomplete lution, the nature of mental processes;.and
set of data. And yet the basic underlying the place of humans in some cognitive scala
logic of allometric change and axonal dis- naturae.
placement processes during development T h e displacement hypothesis has led me
has provided an important new window to propose four highly speculative. expla-
through which to view these data and an nations of some major problems in mam-
indispensable guide to the gathering of malian brain evolution. But displacement
subsequent information about human brain theory does not depend on the correctness
structures and human development. of these particular interpretations. In fact,
it provides means to falsify them if they re
Conclusions incorrect. T h e theory clearly requires t a t
Understanding the evolutionary ances- patterns of brain evolution be ex p lained in
try of the brain's organization is not merely terms of the biasing of competitive devel-
an academic exercise. It is crucial to the opmental mechanisms a n d suggests
study of its basic functional processes as numerous possible candidates for' biasing
well. Few if any brain structures initially influences that are likely involved: includ-
evolved their present form precisely for ing (in order of likely importance) allo-
the purposes they now serve, and many metric relationships, cell death, hetero-
current brain systems may be the result of chronous changes in maturational events
lucky syntheses of previously separated cir- and changes in molecular affinities between
cuits o r else the result of fortuitous degen- cells and axons. T h e correlate's of displace-
erative events. Because the brain was not ment processes that are postulated t o
predesigned for its current adaptations the account for an evolutionary change must
strategies employed in its operation will not be physically exhibited by the develop-
likely yield to a purely functional physio- mental processes that construct living
logical analysis. More importantly, a n brains. If they are not observed then a dis-
understanding of the predispositions and placement explanation must be rejected o r
constraints inherited from past adaptations modified. T h e examples presented in this
paper have been chosen not as test cases the hominoid thalamus. I: Specific sensory relay
for the theory, but rather as exemplars of nuclei. Am. J. Phys. Anthrop. 51:365-382.
Armstrong, E. 1983. Relative brain size and metab-
the range of possible displacement effects olism in mammals. Science 220: 1302-1 304.
and their consequences. Whatever the ulti- Armstrong, E. 1985. Allometric considerations of
mate applicability of these individual the adult mammalian brain, with special emphasis
accounts, the general approach should at on primates. In W. Jungers (ed.), Size and scaling
in primate biology, pp. 115-146. Plenum Press,
least serve to focus attention on a number New York.
of previously unappreciated correlations Atchley, W. R. 1984. T h e effect of selection on brain
between biasing influences in neural devel- and body size association in rats. Genet. Res. 43:
opment and phylogenetic differences in 289-298.
adult brain structure. T o the extent that Baldwin, J. M. 1985. Mental development in the child
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vertebrates. Vie Milieu Biol. Mar. Oceanogr. 197:
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preparing this manuscript. size and sensory modality: Phylogenetic impli-
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