Evolution of human brain functions: the functional

structure of human consciousness

C. Robert Cloninger

The functional structure of self-aware consciousness in human beings is described based

on the evolution of human brain functions. Prior work on heritable temperament and
character traits is extended to account for the quantum-like and holographic properties (i.e.
parts elicit wholes) of self-aware consciousness. Cladistic analysis is used to identify the
succession of ancestors leading to human beings. The functional capacities that emerge
along this lineage of ancestors are described. The ecological context in which each clado-
genesis occurred is described to illustrate the shifting balance of evolution as a complex
adaptive system. Comparative neuroanatomy is reviewed to identify the brain structures and
networks that emerged coincident with the emergent brain functions. Individual differences
in human temperament traits were well developed in the common ancestor shared by reptiles
and humans. Neocortical development in mammals proceeded in five major transitions: from
early reptiles to early mammals, early primates, simians, early Homo, and modern Homo
sapiens. These transitions provide the foundation for human self-awareness related to sexu-
ality, materiality, emotionality, intellectuality, and spirituality, respectively. The functional struc-
ture of human self-aware consciousness is concerned with the regulation of five planes of
being: sexuality, materiality, emotionality, intellectuality, and spirituality. Each plane elaborates
neocortical functions organized around one of the five special senses. The interactions
among these five planes gives rise to a 5 × 5 matrix of subplanes, which are functions that
coarsely describe the focus of neocortical regulation. Each of these 25 neocortical functions
regulates each of five basic motives or drives that can be measured as temperaments or
basic emotions related to fear, anger, disgust, surprise, and happiness/sadness. The result-
ing 5 × 5 × 5 matrix of human characteristics provides a general and testable model of the
functional structure of human consciousness that includes personality, physicality, emotion-
ality, cognition, and spirituality in a unified developmental framework.
Key words: cognition, emotionality, human characteristics, personality, thinking.

Australian and New Zealand Journal of Psychiatry 2009; 43:994–1006

Human beings are perennially curious about their inner
nature and seek to understand what motivates their
desires, actions, feelings, thoughts, and values. The
study of human characteristics has led to many insightful
theories and useful approaches, but each suffers from
serious limitations regarding its scope and the qualitative
properties of its form, aetiology, and dynamics.
C. Robert Cloninger, MD, Wallace Renard Professor of Psychiatry, Genetics,
and Psychology
Washington University School of Medicine, 660 South Euclid Avenue,
St Louis, MO 63110, USA. Email clon@wustl.edu
Received 7 August 2009; accepted 7 August 2009.
Regarding scope, there are many different theories that
focus on sexuality, physicality, emotionality, sociality,
character, cognition, or spirituality [1]. Some broad
theories try to serve as a coherent theory of theories
(i.e. meta-theory), as did Freud, Piaget, and Maslow [2].
Each still focused on a particular aspect of being, such
as sexuality, cognition, or spirituality. Separate theories
for personality, cognition, and spirituality can each be
useful, but the divisions are actually artificial and impair
understanding in serious ways. Health is an integrated
state of physical, emotional, social, cognitive, and
spiritual well-being [3,4].

© 2009 The Royal Australian and New Zealand College of Psychiatrists

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 C.R. CLONINGER
Regarding qualitative properties and form, most
models of human characteristics fail to recognize the
unique properties of different planes of being. ‘Planes’ are
defined as distinct levels of existence, thought, or develop-
ment [5]. Emotions cannot be fully described or explained
by sexual or material mechanisms. Symbolic communica-
tion cannot be fully explained in terms of emotional proc-
esses. Spirituality cannot be adequately explained by
intellectual judgments or rules of moral conduct.
Even within the cognitive domain, there is often failure to
attend to the qualitatively distinct properties of the multiple
systems of learning and memory that are observed in human
beings [6]. For example, associative conditioning varies quan-
titatively according to the strength of habits (Table 1).
Aesthetic appreciation of beauty, however, is a qualitative
experience. Self-aware consciousness is always subjective and
holographic in form (i.e. self-aware perceptions are holistic
and personal), so information about beauty cannot be specified
by any amount of quantitative or objective detail [7].
No models of neurobiology or personality provide an
adequate explanation of subjectivity (i.e. self-aware con-
sciousness). There are several promising neurobiological
insights for explaining different components of conscious-
ness [8–13]. These individual components of consciousness
need to be integrated in a unified general model recognizing
the holographic nature of self-aware consciousness.
Personality and emotionality have other properties that
must be satisfied by a general model of consciousness.
Personality and emotionality have a universal structure
shared by all human beings, as emphasized by Darwin and
supported by cross-cultural studies of facial expression
by Ekman [14]. Likewise, Chomsky suggested that there
is a universal grammar for the development of language
Table 1. Distinctive properties of three systems
of learning and memory in human beings
Qualitative
System Form of learning properties
Procedural Habits and skills Prelogical
Emotion-laden
Quantitative
(variable strength
Not self-aware
Semantic Facts and Logical
propositions Algorithmic
Hierarchical
Not self-aware
Autonoetic Intuitions and Self-aware
narratives Holistic
Biographical
Creative and freely
willed
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995
as part of the rich innate endowment of human beings
[15]. He argued that without such universal structure we
would not be able to communicate and respect one
another as we do [16]. There may still be substantial dif-
ferences among individuals in the expression of these
universal functions, which provides diversity in adaptive
capacities for possible ecological change [17,18].
Finally, a general model of human consciousness needs to
provide a meta-theory for development, including the matu-
ration and integration of sexual, physical, emotional, intel-
lectual, and spiritual aspects of being [19–21]. Lifespan
psychology is an effort to understand development from the
perspective of multiple disciplines in an integrated fashion
[22]. It recognizes biological and cultural influences on
development, but lacks a coherent model of the functional
structure of human beings. Development is a complex adap-
tive process that cannot be specified by linear stage models,
such as those of Freud, Erikson, Piaget, or Kohlberg. Human
consciousness is holographic, and so its development must
be a quantum-like adaptive process, much like the develop-
ment of fractals [7].
Unfortunately, there is no consensus at present regarding
the functional structure [23] or the developmental paths
[22,24] of basic human characteristics, such as personality,
emotionality, or cognition. Likewise, there is no consensus
regarding the structure of psychopathology and other dysfunc-
tional human characteristics. Most psychiatrists recognize that
current categorical systems of classification are seriously
flawed, but do not know with what to replace them. It is impos-
sible to build an adequate science of health and well-being
without understanding how normal adaptive functions are
organized [7,25]. Hence a general model of the functional
structure of human consciousness is imperative for under-
standing well-functioning and ill-functioning human beings.
Darwin’s anniversary is a propitious time for the develop-
ment of a general model of the functional structure of human
beings. As Darwin recognized, human evolutionary history
provides a solid scientific basis for describing the functional
structure of consciousness. As he asked (C Notebook, p. 166,
around May 1838), ‘Why is thought being a secretion of the
brain, more wonderful than gravity a property of matter? It
is our arrogance…our admiration of ourselves’ [26].
Methods
Several recent scientific advances have now converged to permit the
preliminary description of a general model of human consciousness
that can be tested and refined by subsequent research. First, cladistic
analysis is used to identify the succession of ancestors leading to
human beings based on molecular phylogenetics [27,28]. A clade is a
group of organisms that share a common ancestor. Recent advances in
molecular phylogenetics have clarified the succession of ancestors
leading to human beings from the earliest life forms [29–33].
996 FUNCTIONAL STRUCTURE OF HUMAN CONSCIOUSNESS
The functional capacities that emerge along this line of ancestors
are described. The ecological context in which each cladogenesis
occurred is described to understand the influences on evolution, as
illustrated by the co-evolution of angiosperms and the ancestors of
primates [32,34,35] and the importance of hunting animals for meat
for increasing body and brain size of early Homo [36]. These observa-
tions illustrate the shifting balance of evolution as a complex adaptive
system [37].
Comparative neuroanatomy is reviewed to identify the brain struc-
tures and networks that emerged coincident with the emergent brain
functions. Detailed neuroanatomical studies have been conducted that
were guided by cladistic analysis to focus on the ancestral line leading
to human beings [38,39]. Other studies identify which clades have spe-
cific brain structures and networks, such as mirror neurons [40] or von
Economo neurons [8].
Results
What evolutionary transitions led to humans?
Evolution is a complex adaptive process in which multiple genetic
and environmental events are constantly interacting, shifting the
balance of reproductive fitness from situation to situation and
time to time [37]. As a result, genetic influences on personality and
other human characteristics show extensive gene–gene and gene–
environmental interactions [7,41,42]. Consequently, it is impor-
tant to follow the thread of evolution leading to humans as it
unfolded in response to the unrepeatable ecological complexities
of the past.
The timeline of major transitions in brain system structure and
function in human evolution is summarized in Tables 2–4. The transi-
tions represent the emergence of clades, usually with some living
Table 2. Timeline of major transitions in nervous system structure and function in human evolution:
cells to reptiles
Time period (mya) Animal clade no. Animal group
15 000 – –
4540 – –
4000 – –
900 Vendian 0 Choanoflagellates
505 Cambrian 1 Craniates
480 Ordovician 2 Vertebrates
315 Carboniferous 3 Amniotes
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descendants of the common ancestor shared with human beings. All
life forms share DNA as the mechanism of genetic inheritance, going
back to the emergence of the first life forms on earth 4 billion years
ago. The ancestral lineage leading to humans includes the first eukary-
otes, craniates, and amniotes, thereby leading to the common ancestor
shared by reptiles and mammals. Among mammals, the line continues
from the earliest non-placental mammals to tree shrews and then the
proto-primates called plesiadapiforms. The tree shrews were small,
nocturnal, placental mammals who spent little time in maternal care.
Their young developed quickly and they are free to spend most of their
time having sex and eating. The pen-tailed tree shrew, Ptilocerus iowii,
is found in Indonesia, Malaysia, and Thailand. It is thought to be the
closest living example of the common ancestor of primates [33]. It
consumes fermented nectar regularly with 3.8% alcohol without getting
excessively intoxicated [59].
The primate-like mammals called Plesiadapiforms, such as Car-
polestes simpsoni, are known from the late Palaeocene epoch
of Wyoming. They had a grasping foot like primates, including
an opposable toe and a nail rather than a claw. It could probably grasp
with its hands as well. As a result, it was well-adapted to move in the
terminal branches of fruit-bearing trees that flourished at that time
[32,35].
Among primates, the line continues through ancestors in com-
mon with prosimians, simians, then great apes. Prosimians are
typically nocturnal and solitary foragers, whereas simians (monkeys
and apes) are typically diurnal and active in social groups most of
the time [48,49,60]. The great apes show warm emotional expressions
and affectivity, including ventral hugging, in addition to more com-
plex imitation learning, more flexible dominance hierarchies, and
communication with concrete symbols such as sign language
[49,61].
Among the hominoids, the line continues through ancestors of
Australopiths to early Homo. The details of the lineage are intensively
Functional change
[Reference] Living examples
Origin of universe Big Bang
Formation of Earth Planet Earth
Prokaryotic cellular life with DNA Archaea, Bacteria
Sperm-like unicellular ancestor of Monosiga
eukaryotes, including animals,
plants, fungi [31]
Jawless fish without vertebrae; Hagfish
Bilaterally symmetrical chordates
with heads and neural crests [43]
Vertebrae, taste buds, genome Lampreys, bony fish,
duplicated [44] amphibia
Adapted to reproducing and living Reptiles
on land [45]
 C.R. CLONINGER 997

Table 3. Timeline of major transitions in nervous system structure and function in human
evolution: mammals to apes
Animal Functional change
Time period (mya) clade no. Ancestral group [Reference] Living examples

220 Permian 4 Non-placental mammals Neocortical control of sexuality, Monotremes, marsupials

warm, milk-feeding [27]
125–65 Cretaceous 5 Placental mammals Live births, minimal maternal care, Pen-tailed tree shrew
pleasure-moderating [33]
65–55 Palaeocene 6 Plesiadapiforms Primate-like with more maternal (fossil only)
care and varied diet [32,35,46,47]
47 Eocene 7 Prosimian primates Solitary nocturnal foragers, agile Lemurs, lorises, tarsiers
with forward-facing eyes [48]
40 Oligocene 8 Simian primates Diurnal and social with neocortical Monkeys, gibbons
control of emotions [40,49,50,51]
15 Miocene 9 Great apes Neocortical control of sociality and Orangutans, gorillas,
imitative learning [51] chimps

Table 4. Timeline of major transitions in nervous system structure and function in human evolution:
early Homo to modern Homo sapiens
Time period (mya) Animal clade no. Animal group Functional change [Reference] Living examples

2.5–1.6 9/10? Homo habilis ‘Handy’ tool-maker, australopith-like (Fossil only)

Pliocene–Pleistocene size and proportions, brain
approx. 650 cm3 [52–54]
1.8–0.3 10 Homo erectus Larger body and brain, prominent (Fossil only)
Pleistocene (Ice Age) parietal area for language,
migrated to Eurasia, brain
approx. 880 cm3 [55–57]
0.35–0.04 11 Neanderthals, ancient Larger brain volume than modern (Fossil only)
Palaeolithic Homo sapiens Homo, possibly interbred with
other Homo [53]
0.2–present 12 Homo sapiens sapiens Self-aware with art, science, spiritu- Modern Homo
ality [55,58]

debated, but the functional and structural changes are fairly clear even
when the precise transitional form remains uncertain. Australop-
ithecines had well-developed erect bipedal walking, as was shown in
the fossilized footprints preserved at Laetoli in Africa,. The footprints
preserve evidence of one holding hands with a younger child while a
second adult followed, stepping precisely in the tracks of the first adult
[55]. Homo habilis is classified as the earliest human species on the
basis of an average brain volume of >600 cm3 and development of
brain regions that support language functions in modern humans.
Some argue, however, that it should be grouped with Australopiths,
not Homo, because its body was similar to that of an Australopith
[52]. It is clear that between Australopiths and Homo erectus there
was a revolutionary increase in the size of the brain and body of
human beings [62]. This increase required a new way of obtaining
nutrients to support the greater energy consumption of a larger body
and brain.
What were the circumstances of adaptive
change?
Every transition in the ancestral lineage leading to modern humans
involved adapting to a novel ecological challenge. Some of the major
adaptive forces playing out in human evolution are summarized in
Table 5. Every transition was associated with different challenges that
the extant species had to adapt to or face extinction. Mass extinctions
occurred often, shifting the balance of dominance from one life form to
another [63,75,76]. Animals co-evolved with plants, just as both plants
and animals had to adapt to the changing climate and tectonic shifts.
The adaptive challenge helps to recognize the functional shifts that
occurred at each transition leading to modern human beings. Both
mammals and dinosaurs emerged around the same time during the
Jurassic period. The earliest mammals were small nocturnal animals
that ate insects and avoided the large plant-eating dinosaurs. Then

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Table 5. Geologic timeline of coincident events in human evolution
Time period Emerging Climatic and
(mya) ancestral group tectonic events
650–543 0 Choanoflagellates Before Vendian, methane and other
Vendian gases fill atmosphere, complex
chemicals form in oceans.
543–490 1 Craniates Oxygen accumulated enough by end
Cambrian of Vendian and early Cambrian to
form ozone layer blocking ultraviolet
radiation and permitting land to be
colonized. Mass extinctions may
have been related to glacial cooling
or oxygen depletion in the oceans.
490–354 2 Vertebrate Climate is variable. Most land was in
Ordovician– southern supercontinent Gondwana.
Devonian When it shifted to South Pole,
massive glaciers formed and
sealevel dropped, possibly leading
to mass extinctions in Late
Ordovician.
354–290 3 Amniotes Climate was mostly warm, humid and
Carboniferous tropical initially. It then cooled with
glaciations in south in Gondwana.
Sealevels fell all over the world due
to southern glaciation. Oxygen
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levels in atmosphere around 35%
(compared to 21% today). The large
continent Pangaea begins to form.
290–144 4 Non-placental Initially there was an ice age followed
Permian– mammals by warming. Much of land was com-
Jurassic bined in one large continent of Pan-
gaea, much of which was arid. There
were alternating warming and cool-
ing periods.
Bacterial and
plant events
Cyanobacteria produce oxygen as
waste product, creating an
oxidizing atmosphere. Plants form
by symbiosis of cyanobacteria to
form chloroblasts excreting
oxygen, and animals cells by
symbiosis with mitochondria
consuming oxygen.
Primitive algae and seaweeds
present. Primitive plants evolve
from green algae and move onto
land. Fungi also may have aided
colonization of land by symbiosis.
True plants emerge in water and on
land, and dense forests emerge
during the Devonian period. There
were arid periods during the early
Devonian, followed by more
temperate conditions allowing
more plant growth.
Great forests of fern-like seeding
plants flourish and dominate land,
herbivores grow large to accom-
modate large guts needed to
digest nutrient-poor food.
Extensive plant life does not
decay and forms future coal
deposits.
Gymnosperm plants flourish, replac-
ing fern forests. Conifers appear and
spread inland and up mountains,
and later diversify. Southern hemi-
sphere dominated by large seeding
ferns
998
Animal competition/extinction events
[References]
RNA and DNA formed in chemical soup of
oceans. Increasing oxygen level retards
anaerobic life and stimulates aerobic life.
Bacteria, archaea, and simple soft-bodied
organisms live entirely in ocean. First fossil
animals appear [31,63]. Mass extinction of
soft-bodied biota at end of Vendian allowed
diversification of fauna with shells.
Cambrian explosion of multicellular life forms.
Most major groups of animals appear in fossil
records. Trilobites are the dominant animals
initially, but were reduced by mass extinctions
[63].
Rapid evolution of fish in water and wingless
insects on land. Ordovician and Devonian
extinctions eliminate most species, leaving
sharks as the top predators in oceans.
Sharks are top predators in ocean, tetrapods
move to land, and first amniotes emerge. The
amniote egg protects the developing fetus from
desiccation on land, and reptiles thrive.
FUNCTIONAL STRUCTURE OF HUMAN CONSCIOUSNESS
95% of species go extinct at end of Permian,
especially marine invertebrates. This allows
survivors to diversify. Reptiles take over from
amphibians on land. Mammal-like reptiles lose
dominance, and large plant-eating dinosaurs
dominate Jurassic. Mammals emerge approx.
same time as dinosaurs and survive as small,
prolific nocturnal animals feeding on insects
and avoiding reptiles.
 144–65 5 Placental Pangaea is now split up in separate
Cretaceous mammals continents. Generally a warm climate
with high sealevels. Meteorite impact
in Yucatan occluded sunlight for long
period at 65.5 mya, leading to
extinction of dinosaurs except for
ancestors of birds.
65–55 6 Primate-like Initially climate was temperate, cooler
Palaeocene mammals and drier than the Cretaceous. Then
epoch it began to warm as Eocene
approached.
55–34 7 Prosimians Global warm and moist climate
Eocene develops from pole to pole. Hot-
house effect on plants and animals.
Australia separates from Antarctica
and current changes led to global
cooling in later Eocene.
34–24 8 Simians Climate gets colder for 7 million years,
Oligocene making daytime activity desirable and
competition for food greater.
24–5.3 9 Great apes Climate is initially warmer than
Miocene Oligocene and then becomes cooler
and drier, facilitating the expansion of
grasslands in continental interiors.
Asia and Africa have contact and
animals migrate.
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5.3–1.8 9 Australopiths Climates continue to get cooler and
Pliocene drier, similar to modern seasonally
variable climates. Glaciation begins
toward end of period.
Initially angiosperm flowering plants
are abundant, with pollen spread by
insects. Then lack of sunlight killed
much plant life and large herbivores.
Angiosperms flourish producing fruit in
terminal branches of trees,
stimulating agility and varied diet.
Tropical rainforests spread from pole
to pole, displacing other plants.
Primates appear in Asia and
America.
Grasses evolve among the
angiosperms, grasslands begin to
dominate, tropical broad-leaf forests
regress to equatorial belt. Primates
appear in Africa for first time [63].
Wetland forests decline, temperate
grasses using C4 photosynthesis
expand that assimilate CO2
efficiently but are richer in silica
Cooling and drying spurs spread of
temperate climate grasslands and
open savannas with further regression
of wetland forests. Australopiths but
not most other primates adapt to
eating grasses or opportunistic
scavenging meat of grazing animals.
Extinction event eradicates more than half of all
animals, including nearly all dinosaurs [64].
Archaic mammals rapidly diversify and
become dominant vertebrates.
Primate-like nocturnal mammals become agile in
grasping and feeding on fruits and insects in
trees [34,35,46].
Hothouse effect favoured smaller mammals like
prosimians with relatively large surface areas
[65].
Monkeys have higher metabolic rates than
prosimians, allowing for larger bodies and
brains, stimulating shift to diurnal and so cial
activities [66]. Diurnal elephants with trunks
and raptors such as hawks also appear.
C.R. CLONINGER
Silica-rich grasses cause worldwide extinction of
most large herbivores so grasslands safer for
apes [67,68].
Distribution of primates restricted by forests
retreating. Wide expanses of open grassland
provide advantage for emergent bipedal
walking and opportunistically consuming
grasses or meat of grazing animals [69–71].
(Continued)
999
1000 FUNCTIONAL STRUCTURE OF HUMAN CONSCIOUSNESS

65.5 million years ago a large asteroid struck the Yucatan and the

[36,72,73]. Extinction of most large mammals,

abundant. Human diet required meat protein,

fishing to support larger body and brain size

fat, and essential nutrients from hunting and

northward out of Africa if capable. By end of

resulting dust is thought to have occluded sunlight for so long that the

non-domesticated species are threatened by

Pleistocene, humans have spread through
Animal competition/extinction events

Agriculture and husbandry permitted human

herbivorous dinosaurs were extinguished, except for the ancestors of

domesticated food sources [72,74]. Many

sabre-toothed cats, bison, and birds are
Large land mammals such as mammoths,

allowed humans and others to spread

population expansion with more stable

birds [63,64].
The extinction of the dinosaurs allowed mammals to diversify and
they rapidly became the dominant land animals. The emergence of
[References]

fruit-bearing trees provided the circumstance in which sexually prolific

mammals were selected for greater agility, taste discrimination, and
maternal care [34,35]. Extant prosimians are like living fossils of

most of the world.

these Palaeocene ancestors of human beings except that they are true

human impact.
primates with forward-directed eyes. The prosimians thrived as noc-
turnal solitary foragers during most of the hothouse period of the
Eocene, in which the earth was covered with tropical forest between
55 and 45 million years ago.
The global climate began to cool during the late Eocene. Vegetation
changed in response to climate. As competition for resources increased,
diurnal animals emerged, including elephants with trunks, diurnal raptors
source for large body and brains of

structures adapted for omnivorous

during this relatively stable period

areas for food supply. Wild plants

such as eagles and hawks, and also the first simians. Simians are typically
did not provide adequate energy

Plant life has not changed much

diet with substantial reliance on
Glaciation caused retreat of most
plant and animal life to warmer

shifting available foods for diet.

Homo. Homo teeth and cranial

Agriculture is introduced, sharply

diurnal and social, which gave them advantages in energy consumption.

Simians have a higher rate of oxygen consumption than prosimians [66],
Bacterial and
plant events

so being active during the day and foraging in social groups confers an
energy advantage that supported larger bodies and brains. Some prosimi-
ans did later adapt to diurnal living, but only one group of simians, the
(Continued)

until recently.

owl monkey, reverted to nocturnal existence.

When grasslands become widespread, replacing forest, most large
herbivores became extinct. In contrast, Australopiths adapted well to
meat.

the grasslands. They walked upright and also consumed grass or the
meat of grass-grazers, giving them an advantage over apes that did not
Table 5.

adapt for grass consumption [69–71].

30% of world at its peak. Temperate

Ice age ended, warm habitable zones

Great Ice Age, recurrent glaciation, in

Early humans developed larger bodies and brains, which required a

open grasslands remain in some

extend with fairly stable climates

means of richer nutrition. Hunting, fishing, tool-making, and use of fire

all contributed to the supplementation of their high-fibre diets by early
tectonic events

humans with meat for adequate nutrition during the Palaeolithic Ice
Climatic and

Age [36,72]. They had the intelligence to migrate out of Africa and
colonize areas throughout most of the world during the Pleistocene
epoch. The end of the Ice Age made the development of agriculture
feasible, providing a more reliable source of nutrition for modern
regions.

Homo sapiens.

What brain structures emerged coincident with

the functional changes?
habilis to ancient
ancestral group

10/11 Early Homo

12 Modern Homo
Homo sapiens
Emerging

The transitions described in Tables 2–5 can be summarized as the

sapiens

emergence of specific aspects of consciousness, as detailed in Table 6.

The five major transitions are described more briefly in Table 7
because they are the crux of each functional development. In reptiles
central regulation of brain functions is organized in the hypothalamus.
0.10–Holocene

Sensory information is first processed in the basal forebrain of before

Pleistocene
Time period

being relayed to the thalamus and dorsal cortex of reptiles. The dorsal
1.8 –0.10

epoch

cortex and thalamus of reptiles receive sensory input, but do not recip-
(mya)

rocate with output that could modulate the hypothalamus [83].

A multi-layered neocortex first emerges in early mammals, and there is

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 Table 6. Evolution of major brain functions in human evolution
Clade Emergent functions
1 Craniates Animals with skulls, all associated with emergence of the neural crest Neural crest derivatives: skull, brain with five components and cranial nerves
for development of central nervous system. Also all have
ectodermal placodes for development of paired organs for smell,
hearing, and vision in the head.
2 Vertebrates Fish and amphibia show well-developed associative conditioning.
Whole genome duplicated. Amphibia still reproduce in water.
3 Amniotes Adaptations for tetrapods to live and reproduce on land, breathing
oxygen, and amnion to protect developing fetus.
4 Non-placental All mammals are warm-blooded, have skin with hair and glands,
mammals including milk-producing glands to feed young. Early mammals are
typically sexually prolific, a trait shared with rabbits and others.
5 Tree shrews Specialized genital openings and bear live young that require little
maternal care. Can show restraint in sexual activity and eating, e.g.
no excess leading to intoxication when consuming fermented fruits.
6 Protoprimates Enhanced physical agility to grasp food and maternal care of young.
Eyes still laterally directed.
7 Prosimians Nocturnal solitary foragers with skill in finding and selecting food.
Brain size varies with foraging complexity, flexibility of diet and
activity patterns, not social variables. Extensive maternal care
provided to young. Teeth are distinctive for highly variable diets of
primates.
8 Monkeys Diurnal and social with increased metabolic rate able to support larger PFC (mainly orbital and medial PFC) expands and projects directly to
body and brain. Enduring social relationships, much time in social
activities of large groups.
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9 Great apes Highly social, warm emotional expression and affectivity, flexible
dominance hierarchies, imitation learning. Australopiths developed
skilled bipedal walking.
Emergent structures
1–10 (except for eye muscle nerves 3,4,6, which may have been
secondarily lost by hagfish). All have peripheral nervous systems, endocrine
tissues, in addition to paired organs for smell, hearing and vision in head.
Cranial nerves for eyes (3,4,6) are present typically [43].
Reptile brain is centrally regulated by hypothalamus without thalamocortical
feedback to or control of hypothalamus. Dorsal cortex is single layer of
pyramidal neurons.
Neocortex emerges with six layers and allows cortical control of sexual
copulation. All special senses represented neocortically, but most of
neocortex processes touch with no separate motor areas.
Somatosensory, motor, and premotor areas differentiated in neocortex.
Approx. 20 distinct cortical regions compared to >200 in human beings [38].
(Fossils only: functions suggest similar to prosimians except eyes not
forward-directed)
Taste is processed in primary gustatory cortex prior to hypothalamus and
amygdala (frontal operculum and insula) [77]. Eye–hand coordination facilitated
by greater topical ordering of inputs to nuclei for hand and foot and expansion
of parietal association cortex. Ventromedial hypothalamus has many oxytocin
C.R. CLONINGER
receptors, allowing regulation of feeding behaviour in favour of reproductive role.
Differentiation of DPIC supports awareness of the affective aspects of
sensation [78].
hypothalamus, thalamus, septum, basal amygdala, and striatum.
Mirror neuron system appears in monkeys, allowing mirroring of observed
behaviours by neurons in speech motor area (BA 44 posterior inferior
frontal gyrus), VPC, and IPL (BA 40) [40]. The VPC supports both action
understanding and imitation, a precursor to language. In monkeys, affective
information is also relayed to the middle insular cortex, which has extensive
reciprocal connections with the amygdala and hypothalamus, so it is
well-positioned for the regulation of sensuality.
Somatosensory processing becomes serial and less parallel for greater depth
of processing. Differentiation of parietal association cortex for integration of
visual, auditory, and somatosensory information. Great apes and humans,
and not other primates, have von Economo neurons that allow reciprocal
connections of AIC and ACC.
Mirror neurons are also present in great apes in Broca’s area (BA 44) and IPL. Also
in great apes there is differentiation of the AIC for enhanced emotional awareness,
which supports the communication of social emotions in great apes [8].
1001
(Continued)
 1002 FUNCTIONAL STRUCTURE OF HUMAN CONSCIOUSNESS

ticularly around the lateral sulcus in regions related to language [55,79]. a progression of five transitions whereby the neocortex takes control
Hemispheric asymmetry is observed in Homo and some Australopiths, par-

Fossils only but enlarged frontal opercular area and IPL, suggesting emer-

Fossils only but findings indicate language ability with prominent development
of IPL (BA 39/40) and emergence of brain default network that supports
daydreaming, holistic attention, and subconscious problem-solving. Default
brain network includes subsystems in the ventral medial PFC, dorsal medial
PFC, IPL, posterior cingulate/retrosplenial cortex, and hippocampal forma-

Autonoetic awareness depends on a distributed frontotemporoparietal network

with encoding via hippocampus [12]. The same brain regions are most
recently differentiated in evolution and are late in myelinating. The whole
neocortex becomes a functional whole by linking all associative areas

ACC, anterior cingulate cortex; AIC, anterior insular cortex; BA, Brodmann area; DPIC, dorsal posterior insular cortex; IPL, inferior parietal lobule; PFC, prefrontal cortex; VPC,
of central regulatory functions from the hypothalamus. In early mam-
mals and tree shrews, the major neocortical function is voluntary
control of copulation, which is reflexive in reptiles [84]. Early mam-
mals noted for their prolific sexuality, such as rodents and rabbits, are

tion and related entorhinal and parahippocampal cortex [9,10].

a sister clade of tree shrews [28]. Primary somatosensory cortex is
clearly developed in early mammals and tree shrews (clades 6/7), but
there is little or no differentiation of sensory neocortex from motor
neocortex [38,39].
Emergent structures

In proto-primates and prosimians there is functional development

gence of language and default brain network.

of motor agility, better discrimination of the taste of a varied diet,

more maternal care of young, and more time spent in grooming and
related form of assuagement. These functions involve regulation of
through projections of visual system

material things such as food and activities of daily living. Unlike

rodents, in primates there is no direct path from the brainstem taste
areas such as the nucleus of the solitary tract to the hypothalamus and
amygdala. Information about taste in primates, in contrast, reaches
the amygdala and orbitofrontal cortex from the primary taste cortex,
which is in the frontal operculum and insula [77].
Prosimians have well-differentiated sensory and motor neocortical
areas, in contrast to tree shrews. Detailed studies of galagos indicated
several changes in brain structure that support enhanced motor agility
with advanced grasping and leaping adaptations [38,39]. The findings
Table 6. (Continued)

include greater topographical ordering of sensory input for the hands

and feet, premotor and supplementary motor areas, at least two motor
Precision grip for making stone tools, reduced size of post-canine
teeth, fishing, and hunting in groups for meat. Enlarged brain size

Creation of aesthetically refined tools, language, and culture with

areas in the cingulate cortex, and feedback circuits between prefrontal

cortex, premotor cortex, and primary motor cortex. In addition, prosim-
ians have an enlarged posterior parietal cortex for processing visual,
Self-aware consciousness with art, science, and spirituality

auditory, and somatosensory information to form and relay instructions

about hand and eye movements to premotor areas.
In simians there is emergence of affectivity with patterns of emotional
expression, attachment, and friendship that are similar to human affectiv-
Emergent functions

ity as noted by Darwin [14] and Bowlby [49,61,85]. Related brain

widespread migration in social groups.

changes include the development of prefrontal cortex for regulation of

emotional functions [80], a distinctive system for interoceptive process-
but body similar to australopiths.

ing of sensual aspects of touch [8,78,86,87], and the emergence of the

mirror neuron system on frontal and parietal cortical areas [40].
In early Homo there is emergence of symbolism, including capaci-
ties for taboo, allegory, language, empathy, and discernment [79].
Symbolism builds on the abilities needed for cooperative group forag-
ing in simians [79]. Homo erectus showed aesthetic appreciation in the
making of refined tools in their Acheulian culture [81,82]. These sym-
bolic functions depend on processing in the inferior parietal cortex,
which is a convergence area for touch, hearing, and vision, allowing
cross-modal transformations important for language and other forms
ventral premotor cortex.

of symbolism [55,79,88]. The angular gyrus in particular has an

important role in the comprehension of metaphor and allegory [89].
sapiens sapiens
12 Modern Homo
11 Ancient Homo
10 Homo habilis

Symbolic activity enhances the capacity of the brain default network,

which allows first-person perspective taking and daydreaming, as when
sapiens

a person is letting his or her mind freely wander about inner thoughts
Clade

and feelings [9,10].

Finally, in modern human beings there is self-aware perception
of a sense of unity, manifest by emergent capacities for harmony,

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 C.R. CLONINGER 1003

Table 7. Cladistic staging of evolution of the functional components of self-aware consciousness in human
beings: five basic stages
Clades Emergent brain network Major function Component functions†
(Voluntary)

4/5 Early mammals Somatosensory neocortex regulating Copulation Sex drive

sexuality Longing
(Pleasure)
(Eroticism)
(Tenderness)
6/7 Early primates Differentiation of sensory and motor Materiality Rhythmicity
neocortex; neocortex regulating taste Agility
Sensation
(Movement)
(Transformation)
8/9 Simians Prefrontal cortex regulating limbic system Affectivity Fulfilment
[80]; von Economo neurons in AIC/ Friendship
ACC; mirror neuron system Emotional
awareness
Romanticism
(Devotion)
10/11 Early Homo Auditory association cortex regulates Symbolism Taboo
cross-modal symbolism; brain default Allegory
network regulates attention and Empathy
daydreaming; frontoparietal percep- Discernment
tual–motor praxis system permits Aesthetics
refined tool-making [81,82]
12 Modern Homo sapiens Autonoetic system unifying frontopari- Unity Harmony
etotemporal association areas (linked Sublimation
by visual projection system) [6,12] Adoration
Contemplation
Universal awareness

ACC, anterior cingulate cortex; AIC, anterior insular cortex.

†Functions in parenthesis are found in human beings but not in original ancestor in which major function came under neocortical regulation.

sublimation, spiritual adoration, and contemplation [7]. These abilities
give modern human beings their potential in art, science, and spiritual-
ity, sometimes leading to transcendent joy, oceanic feelings or even
cosmic consciousness [7,58]. Such integrated awareness is supported
by autonoetic system of learning and memory [6]. Such self-aware
consciousness allows a person to travel in space and time in their recol-
lection of episodic events. Such autobiographical thinking involves a
distributed frontoparietotemporal network [12]. Essentially the visual
projection system connects all tertiary association cortices so that the
brain can function as a coherent whole.
Discussion
I have sketched the ancestral lineage of human beings
and identified five major transitions in functional capac-
ity: copulation, materiality, affectivity, symbolism, and
self-awareness of unity. These five functions are core
abilities for the regulation of what I have elsewhere
called the five planes of being: sexuality, materiality,
emotionality, intellectuality, and spirituality [7]. A plane
can refer to a level of existence, thought, or development.
The term ‘plane’ is particularly appropriate for describ-
ing these components of self-aware consciousness. It
is appropriate because a plane refers to a particular level
of existence, perhaps sexual, material, emotional, and
so on. It also refers to particular kinds of thoughts in
self-aware consciousness. Finally, it refers to components
of consciousness that are inseparably connected and
dynamically developing, even when its manifestation
is latent.
My last statement about latent development is impor-
tant, even though it may seem obscure at first. It is obscure
because throughout this brief sketch of evolutionary devel-
opment I have traced a specific manifest line of develop-
ment. I have talked only about emergent functions, but
latent processes are expected to be already under develop-
ment before they are overtly manifested. Remember that

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1004 FUNCTIONAL STRUCTURE OF HUMAN CONSCIOUSNESS

Table 8. Matrix of functional components of consciousness and the animal clade in

which they are first manifest†
Subplane Sexual plane Material plane Emotional plane Intellectual plane Spiritual plane
Spiritual Union 7 Giving of yourself 7 Exaltation 7 Philosophy 7 Unity 7
Intellect Communion 5 Expression 5 Exhortation 5 Symbolism 5 Teaching 7
Emotional Sensuality 4 Sensitivity 4 Affectivity 4 Symbiosis 5 Humanism 7
Material Satisfaction 3 Materiality 3 Resurgence 4 Artistic creation 5 Incarnation 7
Sexual Copulation 2 Reproduction 3 Intimacy 4 Suggestivity 5 Temperance 7
†Animal groups in which functional component is first manifest: 1, reptiles; 2, early mammals and tree shrews; 3, protoprimates and
prosimians; 4, simians and Australopiths; 5, early Homo; 6, neanderthals and archaic Homo sapiens; 7, modern Homo sapiens
sapiens.
Bolded text designates the crucial functions upon which the other functions are dependent.

evolution and development are complex adaptive systems
within a whole in which everything is interconnected and
interdependent. Language did not develop wholly in one
abrupt step [55,79,90]. Functional precursors that are
developed in response to one challenge are often co-opted
for another use in different situations.
Each plane of being involves neocortical functions
organized around one of the five special senses. The
interactions among these five planes gives rise to a 5 ×
matrix of subplanes, which are functions that coarsely
describe the focus of neocortical regulation (Table 8).
I have deliberately focused only on the five functions in
bold along the diagonal of Table 7. These diagonal com-
ponents are the core functions upon which the others are
built. For example, the material subplane of sexuality
(satisfaction, such as assuagement by grooming) depends
on the differentiation of sensory and motor functions
underlying materiality. Satisfaction and enhanced mater-
nal care (a facet of reproduction) emerge together with
materiality in protoprimates and prosimians. Likewise,
the emotional subplane of sexuality (sensuality) depends
on emotional awareness (affectivity), and they emerge
together in simians.
Within each of the five planes of being, there are
components of each plane that emerge in succession in
the ancestral lineage leading to human beings. For exam-
ple, in the sexual plane, copulation emerges in early
mammals, satisfaction in protoprimates, sensuality in
simians, and soon.
Each of these 25 neocortical functions regulates each
of five basic motives or drives that can be measured as
temperaments (harm avoidance, novelty seeking, reward
dependence, persistence, plus coherence-seeking) or
basic emotions like those described by Darwin and
Ekman (fear, anger, disgust, surprise, and happiness/
sadness) [14]. The resulting 5 × 5 × 5 matrix of human
characteristics provides a general testable model of the
functional structure of human consciousness that includes
personality, physicality, emotionality, cognition, and
spirituality in a unified developmental framework. Each
of the components of this functional matrix can function
either well or poorly, thereby providing the foundation
for a positive science of well-being. I am pleased to
introduce the evolutionary foundation of the science of
well-being on the anniversary of Darwin’s birth and his
publication of The origin of species [91].
Acknowledgements
This work was supported by non-government funds from
the Washington University Center for Psychobiology and
the Anthropedia Foundation.
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