J of Comparative Neurology - 2016 - Bayer - Joseph Altman 1925 2016 A Life in Neurodevelopment

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E D ITO R IAL
Joseph Altman (1925–2016): A Life in

Neurodevelopment
Shirley A. Bayer*
Laboratory of Developmental Neurobiology, Inc., Ocala, Florida 34481
INDEXING TERMS: rat brain development; human brain development; olfactory bulb; hippocampus; cerebellum;
neocortex
became a librarian in the School of Education in New

York University. All this time he was continuing to read
about human behavior, animal behavior, and brain
structure and was looking for an opportunity to study
brain and behavior on his own. Altman had the opportu-
nity to become a neuroscientist while he was working
as a tenured librarian in New York. He gave up that
position and became a graduate student in psychology
in the laboratory of Hans-Lukas Teuber, earning a PhD,
in 1959 from New York University. That degree
launched a successful career, first as a postdoctoral fel-
low at Columbia University, next at the Massachusetts
Institute of Technology, and finally at Purdue University.
From the early 1960s to 2016, he published many
articles in peer-reviewed journals, books, monographs,
and online free books that emphasized developmental
processes in brain anatomy and function. The notes he
took on animal behavior during his years as a librarian
appeared in his first book (Altman, 1966). His many
contributions from his own experiments are a legacy
Joseph Altman at age 75. that sheds new light on the mechanisms of develop-
ment at the tissue and cell level in both the central and
the peripheral nervous systems.
Joseph Altman was born in Budapest on October 7, His first major discovery was that neurons are gener-
1925, and died in his home in Ocala, Florida, on April ated in adult rat and cat brains (Altman, 1962, 1963),
19, 2016, 6 months into his 91st year. It is my privilege especially in the dentate gyrus of the hippocampus
to be asked by Patrick R. Hof to write a retrospective (Fig. 1). This finding was nearly universally rejected by
of his contributions to developmental neurobiology. most of his colleagues, but Altman and his coworkers
As a teenager in prewar Budapest, Altman spent continued onward, adding more data to substantiate
many hours in the public library reading books about the claim (Altman and Das, 1965a; Bayer et al., 1982;
psychology, human behavior, psychoanalysis, and
human brain structure. After World War II, he spent
Grant sponsor: Atomic Energy Commission; Grant sponsor: National
some time at the University of Heidelberg. Then his Institutes of Health; Grant sponsor: National Science Foundation.
entire family immigrated to Australia, and he became a *CORRESPONDENCE TO: Shirley A. Bayer, Laboratory of Developmental
Neurobiology, Inc., 8518 SW 86th Terrace, Ocala, FL 34481. E-mail:
librarian at the University of New South Wales in bayeraltman@earthlink.net
Sydney Australia. He moved to New York with his first
Received June 8, 2016; Revised June 9, 2016;
wife, Elizabeth Altman (an American citizen), and Accepted June 10, 2016.
DOI 10.1002/cne.24058
Published online June 30, 2016 in Wiley Online Library
C 2016 Wiley Periodicals, Inc.
V (wileyonlinelibrary.com)
The Journal of Comparative Neurology | Research in Systems Neuroscience 524:2933–2943 (2016) 2933
10969861, 2016, 15, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/cne.24058 by CAPES, Wiley Online Library on [30/11/2022]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
S.A. Bayer
Figure 1. The first published photomicrographs showing labeled dentate granule cells in the hippocampus of an adult rat that had been
injected with 3H-thymidine on postnatal day 60 and killed 2 weeks later. During that 2-week survival period, several dentate granule cell
progenitors absorbed the label and differentiated into mature granule cells, mainly positioned at the base of the granular layer (at the top
of each of the photographs; Figs. 12–17 in Plate 4 from Altman, 1963).
2934 The Journal of Comparative Neurology | Research in Systems Neuroscience

Altman and Neurodevelopment
Bayer, 1982). By the 1990s, other neuroscientists had campus had been lesioned (Bayer et al., 1973; Brunner
confirmed that, all along, Altman and his coworkers et al., 1974; Haggbloom et al., 1974; Gazzara and
were correct: adult neurogenesis did exist. Laboratories Altman, 1981). The irradiated animals also showed
all over the world intensively study the phenomenon abnormalities in brain electrophysiology (Whishaw et al.,
today. Altman recently received recognition for this 1978) and monoamine innervation (Moore et al., 1978).
discovery, The Prince of Asturias Award from the One of Altman’s most complete contributions was a
Crown Prince of Spain (now King Felipe) in 2011 and comprehensive analysis of the development of the cere-
the International Prize for Biology from the Emperor of bellum and the precerebellar nuclei in the brainstem.
Japan and the Japan Society for the Promotion of These classic articles were published between 1967
Science in 2012. and 1987. There was a series on the normal postnatal
However, the discovery of adult neurogenesis was development of the cerebellar cortex (Altman, 1969a,
only the beginning. He was an enthusiastic and creative 1971, 1972a–c). Interspersed with these articles were
powerhouse of keen observation, well-designed experi- many on the effects of low-level X-irradiation to elimi-
ments, and insightful interpretations. Many of his major nate all or some of the postnatal microneurons in the
contributions (the majority published in the Journal of cerebellar cortex (Altman, 1973a,b, 1976a–c; Altman
Comparative Neurology) centered around an extensive and Anderson, 1969, 1972, 1973; Altman et al., 1967,
study of postnatal neurogenesis in three areas of the 1968, 1969). Altman analyzed all of the findings and
brain, the olfactory bulb, the dentate gyrus in the hippo- came up with one of the best explanations—backed up
campus, and the cerebellar cortex (Altman and Das, with experimental evidence—of cytoarchitecture in the
1965b, 1966). cerebellar cortex and the planar orientation of Purkinje
Altman was the first to describe a rostral migratory cell dendrites (Fig. 3; for review see Altman, 1982).
stream of stem cells and young olfactory neurons that Finally, there were many articles on embryonic develop-
extends from the anterior lateral ventricle all the way ment of the cerebellum (Altman and Bayer, 1977,
into the internal granular layer of the main olfactory 1978a, 1985a–c) and the precerebellar nuclei in the
bulb (Fig. 2; Altman, 1969b). Ten years later Rosselli- brainstem (Altman and Bayer, 1978b, 1987a–d). During
Austin and Altman (1979) showed that new microneur- all this time, Altman also published some seminal
ons are routinely generated in the adult olfactory bulb. articles on the maturation of motor behavior and the
Today, many laboratories are studying the rostral migra- effects of interfering with cerebellar development
tory stream and the stem cells inside it. (Wallace and Altman, 1970a,b; Altman et al., 1971;
Altman and his coworkers extensively studied the Altman and Sudarshan, 1975; Altman and Bulut, 1976;
development of the hippocampus and its contributions Pellegrino and Altman, 1979; Gruner et al., 1980; Gruner
to behavior. Today, these articles are often referenced and Altman, 1980), the effects of hypo- and hyperthyroid-
and are considered classic contributions. Postnatal neu- ism (Nicholson and Altman, 1972a–c), and the effects of
rogenesis of the granule cells in the dentate gyrus was alcohol exposure (Bauer-Moffett and Altman, 1975), and
established in some overview articles (Altman and Das, he pioneered transplantation studies with G.D. Das (Das
1965b, 1966, 1967) and was later quantified with pro- and Altman, 1972). Altman summarized all his findings on
gressively delayed cumulative 3H-thymidine labeling and the cerebellum in a major book published in 1997 that is
low-level irradiation (Bayer and Altman, 1974, 1975). now out of print: Development of the cerebellar system in
The Altman laboratory then sponsored an extensive relation to its evolution, structure, and function.
analysis of neurogenesis in the entire hippocampal Throughout all of the prolific work on the olfactory
region (Bayer, 1980a) and its prenatal development bulb, hippocampus, and cerebellum, Altman continued
(Bayer, 1980b). Altman revisited the hippocampus in to publish seminal articles on other topics. An extensive
1990, analyzing the mosaic organization of the hippo- series appeared on the diencephalon (Wallace et al.,
campal neuroepithelium (Altman and Bayer, 1990a), the 1969; Altman and Bayer, 1978c–e, 1979a–c, 1986,
migration of pyramidal cells in Ammon’s horn (Altman 1988a–c, 1989a–c; Bayer and Altman, 1987), the mid-
and Bayer 1990b), and the migration of dentate granule brain tectum (Teuber, 1960; Altman, 1961; Altman and
cell precursors (Altman and Bayer, 1990c). His final Carpenter, 1961; Altman and Malis, 1962; Altman and
contribution appeared in Altman and Bayer (2014), doc- Altman, 1962; Altman and Bayer, 1981b,c), the brain-
umenting a large subgranular zone in the human hippo- stem (Altman and Bayer, 1980a–d, 1981a), the spinal
campus from age 1 month to 6 years. Several articles cord (Altman and Bayer, 1984, 2001), and the sensory
showed that, when the hippocampus was irradiated ganglia (Altman and Bayer, 1982).
with schedules that eliminated 85% of the dentate gran- In the late 1980s, Altman and Bayer launched a com-
ule cells, the animals behaved as if the entire hippo- prehensive study of neocortical development in the rat
The Journal of Comparative Neurology | Research in Systems Neuroscience 2935

S.A. Bayer
Figure 2. The first photomicrographs of the rostral migratory stream in Figure 3 from Altman (1969). A: Low-magnification overview in a
sagittal section of a 21-day-old rat (arrowhead indicates the stream; CO cerebral cortex; OB olfactory bulb; LV, lateral ventricle). B: The
rostral migratory stream at higher magnification. NA, nucleus accumbens. C: The neuroepithelium (NE) and subventricular zone lining the
inferior horn of the lateral ventricle (LV) in a coronal section near the caudate/putamen (CP). The arrowhead points to a blood vessel. D:
Terminal part of the migratory stream (MS) lining the olfactory recess of the lateral ventricle. Note the many spindle-shaped cells above
the internal granular layer (IG).

Figure 3. Color-coded revision of Figure 31 of Altman (1982) that diagrams the hypothesis that microneuron axons in the cerebellar cortex
are responsible for shaping the Purkinje cell dendrite; each of these assertions is based on evidence from specifically timed X-irradiation
schedules of the developing cerebellum. This diagram is of the midline cerebellum or vermis. First, basket cell axons (red/orange) in the
lower molecular layer form a “tunnel” around the upward-growing Purkinje cell dendrite and allow only one primary branch to extend
toward the external germinal layer. Second, stellate cell axons (blue) induce secondary branching of the primary dendrite. Third, the Pur-
kinje spiny branchlets synapse (purple dots) with as many different parallel fibers (green dots and lines) as possible. The increased sam-
pling configuration causes the dendrite to stretch out its spiny branchlets perpendicular to the stack of parallel fibers so that the entire
dendrite is pulled into a planar “fan” in the sagittal plane and narrow vertical shafts in the coronal plane (for more illustrations of Altman’s
findings go to http://neurondevelopment.org/cerebellar-development/).
brain. The Altman laboratory was able to publish novel study into a book in which all the findings could be eas-
articles that documented the existence of specific ily related to each other (Bayer and Altman, 1991a).
layers in the intermediate zone visualized with 3H-thymi- Later, the Laboratory of Developmental Neurobiology,
dine autoradiography—Altman now called it the Inc., set up with personal finances, launched an exten-
“stratified transitional field”—that are staging areas sive analysis of the developing human neocortex.
where migrating neurons pause to interact with incom- Layers in the stratified transitional field are grossly visi-
ing axons before continuing their migration to the corti- ble in humans, and prominent regional differences
cal plate (Fig. 4; Altman and Bayer, 1990e; Bayer and exist between sensory and motor parts of the cortex
Altman, 1991a, Chapter 7) and lateral migration in the (Figs. 5, 6; Altman and Bayer, 2002, 2015). On the
embryonic neocortex (Bayer et al., 1991b). A few other whole though, stratification in the developing cortical
articles were published (Bayer and Altman, 1990; Alt- intermediate zone and its importance in the mature
man and Bayer, 1990d; Bayer, 1990a,b; Bayer et al., connections of the cortex are still controversial. As with
1991b), but the Altman lab decided to put the entire the studies on adult neurogenesis, Altman’s discovery

S.A. Bayer
Figure 4. Autoradiogram of the embryonic cerebral cortex on embryonic day (E) 18, 24 hours after a single exposure to 3H-thymidine on
E17 (based on illustrations from Chapter 7 of Bayer and Altman, 1991a; this is slice 21 in the 24-hour-survival E18 coronal specimen in
braindevelopmentmaps.org) The alternating bands of heavily labeled and unlabeled/lightly labeled cells in the stratified transitional field
(also called the intermediate zone) are shown as one example of their existence. These bands are visible only with 3H-thymidine autoradiog-
raphy in rats. The appearance and disappearance of these bands in various 24-hour-survival groups correlates exactly with peak days of
neurogenesis in various layers of the cerebral cortex. The relationship is as follows: superior band 1 appears on peak days of neurogenesis
in layer 6 (best seen 24 hours after injections on E15 and E16, not seen after E17 injections); superior band 2 appears on peak days of
neurogenesis in layer 5 (best seen 24 hours after E16 and E17 injections); inferior band 1 correlates with peak neurogenesis in layers 4,
3, and 2 and is first seen after an E17 injection and also after injections on E18–20. There are other bands (superior band 3 and inferior
band 2 that correlate with glial production in the deep white matter and in the layer of axons that will cross the midline in the corpus cal-
losum). For a full discussion of their importance, read Chapter 7 of Bayer and Altman (1991b). These bands are evidence that the strati-
fied transitional field is an important staging area for the development of anatomical connections of the cerebral cortex. Arrows indicate
the continuity between cortical and ganglionic neuroepithelia and subventricular zones and have been shown by others to have migratory
streams from the basal ganglia to the cortex. Scale bar 5 0.25 mm.
of stratification in the intermediate zone is awaiting culture. This free e-book summarizes his thoughts and
“rediscovery” by researchers who will be more recep- scholarly readings of the last 70 years (download each
tive in the future. chapter from brainmindevolution.org). He died as he
Altman retired in 1995, and, because he remained was finishing the last chapter. After all, he grew up in
as much a psychologist as a neuroscientist, he never a turbulent time and had first-hand experience of the
lost interest in the relationships between mind, brain, dangers of discrimination, religious intolerance, and
and human behavior. Most of his time in retirement persecution. Adding to that rich personal history are
was spent writing Neural and mental evolution. origins his many years as a neuroscientist. Joseph Altman
of the human body, brain, behavior, consciousness, and offers a unique and new perspective on the

Figure 5. Regional differences between frontal (A) and occipital (B) cortices in the stratified transitional field (STF) in specimen Y27-60
from the Yakovlev Collection, a 5-month-old human fetus (from Fig. 21 of Altman and Bayer, 2015). Layers in the human STF are directly
visible as alternating cell-dense or cell-sparse (fibrous) layers—much more prominent than in the rat STF. The regional differences are as fol-
lows. STF1, the formative white matter, is less prominent in the frontal cortex, but that difference may be due to cutting angle. STF2 is
dense in frontal cortex, difficult to discern in occipital cortex. STF3 is not present in frontal cortex but is the most prominent layer in occi-
pital cortex, having three subdivisions (a–c). STF5 and 6 show little difference between frontal and occipital cortices. Scale bar 5 2 mm.

S.A. Bayer
Figure 6. Organization and hypothetical function of STF3 (yellow) in the developing visual cortex (Fig. 23 of Altman and Bayer, 2015). The
two horizontal cell-dense bands (STF3a and STF3c) form an upper plate and a lower plate parallel to the cortical surface, with vertical min-
icolumns of cells and fibers (purple) between them (STF3b). We speculate that fiber bundles from the lateral geniculate nucleus (in STF4)
carry specific information, such as, location of retinal orgin, on-center or off-center excitability, etc., and that these fibers interact with the
nonspecified neurons (light gray ellipses) moving out of STF5, through STF4, and into STF3. As the neurons migrate from STF3c to STF3a,
they intermingle with the thalamic fibers and become specified (dark to very dark gray ellipses). They migrate toward the cortical plate
through STF2 and STF1 as specified neurons, possibly migrating to specific regions in the cortical plate with their associated fibers.
neurobiology of human nature that furthers our scien- LITERATURE CITED

tific perspective on human cultural history. Over the Altman J. 1961. Some fiber projections in the superior collicu-
next few months, the last chapter of his book will be lus in the cat. J Comp Neurol 119:77–95.
packaged and put online along with an enormous bibli- Altman J. 1962. Are new neurons formed in the brains of
adult mammals? Science 135:1127–1128.
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up his insights. tion in the brains of rats and cats. Anat Rec 145:573–583.

Altman J. 1966. Organic foundations of animal behavior. New Altman J, Anderson WJ. 1972. Experimental reorganization of
York: Holt, Rinehart, and Winston. the cerebellar cortex. I. Morphological effects of elimina-
Altman J. 1969a. Autoradiographic and histological studies of tion of all microneurons with prolonged X-irradiation
postnatal neurogenesis. III. Dating the time of production started at birth. J Comp Neurol 146:355–408.
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cortex. III. Regeneration of the external germinal layer of the hypothalamus with the time of origin of its neu-
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Altman J. 1973b. Experimental reorganization of the cerebellar Altman J, Bayer SA. 1978e. Development of the diencephalon
cortex. IV. Parallel fiber reorientation following regenera- in the rat. III. Ontogeny of the specialized ventricular lin-
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cortex. V. Effects of early X-irradiation schedules that in the rat. IV. Quantitative study of the time of origin of
allow or prevent the acquisition of basket cells. J Comp neurons and the internuclear chronological gradients in
Neurol 165:31–48. the thalamus. J Comp Neurol 188:455–472.
Altman J. 1976b. Experimental reorganization of the cerebellar Altman J, Bayer SA. 1979b. Development of the diencephalon
cortex. VI. Effects of early X-irradiation schedules that in the rat. V. Thymidine-radiographic observations on
allow or prevent cell acquisition after basket cells are internuclear and intranuclear gradients in the thalamus.
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cortex. VII. Effects of late X-irradiation schedules that in the rat. VI. Re-evaluation of the embryonic develop-
interfere with cell acquisition after stellate cells are ment of the thalamus on the basis of thymidine radio-
formed. J Comp Neurol 165:65–76. graphic datings. J Comp Neurol 188:501–524.
Altman J. 1982. Morphological development of the rat cere- Altman J, Bayer SA. 1980a. Development of the brain stem in
bellum and some of its mechanisms. Exp Brain Res the rat. I. Thymidine-radiographic study of the time of
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481–497. Altman J, Bayer SA. 1980d. Development of the brain stem in
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S.A. Bayer
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10969861, 2016, 15, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/cne.24058 by CAPES, Wiley Online Library on [30/11/2022].

Joseph Altman (1925–2016): A Life in

became a librarian in the School of Education in New

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neurobiology of human nature that furthers our scien- LITERATURE CITED

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