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Postnatal Neural Ontogeny :Environment-Dependentand/or Environment-Expectant?

MARC BEKOFFMICHAEL W. FOX

Department ofPsychologyWashington UniversitySt. Lou is, Missouri

Recent advances in the study of postnatal neural development, an adaptiveprocess depen dent on an intimate interplay of bo th genetic and environmental factors,are reviewed in mouse, rat, cat, and man. Since developmental n euroan atomica l studiesprovide a useful and relevant way of approaching the much belabored and controver-sial nature-nurture issue, behaviorally oriented workers should be made aware of t h eheuristic value of the field as bo th an impe tus and a guide for future research, and as ameans for providing explanations for observations unexplainable at the ethological orbehavioral descriptive level. The conclusion reached in this review is that postnatalneural ontogeny is both environment-dependent and env ironment-expectant . To dividethe process into mutually exclusive halves is indefensible.

IntroductionThat the nervous system is capable of undergoing morphological, physiological,

an d biochemical changes postna tally is a well established fact. Postn atal mo dific ationof the central nervous system may be viewed as an adaptive process. At birth, thequali ty and modali t ies of afferent stimuli impinging upon the organism are radicallyaltered to which the nervous system must adapt by appropriate postnatal modifica-tion, as has been suggested by some workers. Arbib and K ahn (196 9) viewed the brainas a comp uter th at develops to survive in an environm ent, and conceptualize this develop-mental process in a neurocybernetic framework. Anokhin (1964) postulated thatpostnatal plasticity should be viewed as an adaptive process, that development followsa path which allows maximum adaptation for the survival of the neonate. This isReceived for pu blication 12 April 197 1Developmen ta l Psychobiology, 5(4) , 323-341 (197 2)0 197 2 by J oh n Wiley & Son s, Inc.

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similar to Carmichaels law of ant icipato ry morphological ma tur atio n (Carmichael,1970) in wh ich is implied an intim ate structure -function relationship or, as emphasizedby Gottlieb (1 970), a struc ture-fiinction-structure relationship.

The pertinent questions that have been given great consideration are: (1) are thedevelopmental changes seen a fter birth genetically de term ined, delayed maturationalgrowth processes? (2) Are these p ostnatal changes influenc ed by th e patterns of inter-action between the developing organism and its environment? The first question in-volves consideration of the environm ental-expectant model and the second, considera-tion of the environmental-dependent model. [See Hebb (1953); Lehrman (1953,1970); and Lorenz (1965) for in depth discussions of this controversial developmentalissue]. The question that should be considered, however, is: How are maturationalprocesses influenced by interaction with the environment? Schneirla (1966) statedthat the developmental contribution of maturation and experience must be viewed asfused at all stages of ontogenesis of any organism. Krushinskii (1962) and Chance andJolly (1970) add further support to the view that the determinants of behavior of allkinds always involve the interaction between hereditary disposition and experience.Nevertheless, the postnatal changes may not be the opportunity for plasticity forexternally c onditio ned and inp ut-c ont ing ent reorganization of the neonates wiringsystem (Altm an, 1967 ) since the precise contr ibu tion of the experiential history ofthe neon ate to postnatal plasticity has no t been established, and the genetic contribu-tion likewise remains unknow n. M oreover, th e plasticity phe no me no n ma y be aninnate or genetic endowment with clear species-phylogenetic differences. [NoteMasons (1968) notion of neoteny in primates capacity for structuro-functionalchange as a conseq uenc e of experience.] The m ajor p art of this review concerns itselfwith presentation of the evidence thus far elucidated for postnatal modification instructure and functio n in bot h the cerebral cortex and the cerebellum.

Postnatal Changes in the Nervous SystemBefore discussing the evidence for postnatal neural modification, we must con-

sider the neural and behavioral criteria that are used as indices of the maturationalstatus of the developing cent ral nervous system. Th ey are as follows:

(1) total number of neurons in a particular area (Eayrs & Goodhead, 1959;Rabinowicz, 1967);

(2) patter ns of connectivity of the neuronal processes (Conel, 1941);(3) size of the perikaryon (Noback & Purpura, 1961; Purpura, Schofer,

Housepian, & Noback, 1964);(4) number of dendrites and branches; size, caliber, and length of the perikaryal

processes; presence of dendritic: spines (pedunculated bulbs, thorns, or gemmules);numbe r a nd length of a xon collateral branches (Conel, 1941; Nobac k & Purpura,1961; Purpura e t al ., 1964);

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(5 ) increased thickness of the cortex; increased brain weight (Conel, 1941;Noback & Purpura, 1961; Purpura et al., 1964);(6) cellular proliferation, migration, and biochemical differentiation (Altman,1967, 1969, 1970; Altman & Das, 1964; Angevine, 1965; Haas, Weiner, & Fliedner,1970 ; Uzman, 1960).

(7) packing density (Haddara, 1 956; Eayrs & Goodhead, 1959);(8) degree of myelination (Langw orthy, 19 33; Conel, 1941; Jacobson, 196 3;

Yakovlev & Lecours, 1967; OBrien, 1970).(9) appearance of certain enzym e systems (Himwich, 1 962 ; Himwich & Dravid,

1967; Richter, 1967; Altman & Das, 1970);(1 0) electrophysiological parameters of the developing brain (Purpura, Schofer &

Scarff, 1967 ; Myslivecek, 1970 ; Rose & Ellingson, 1970);(1 1) electrolytic pattern s (Swaiman, 1970);(12) reflex patterns (Fox, 197 0; Humphrey, 1970);(13) perceptual and mo tor development (Cratty, 1970).Although the greatest part of maturation of most mammalian nervous systems

occurs prior to parturition, ongoing changes are evident in the neonate (as listedabove) and, in certain parts of the central nervous system, even late in adult life.Exceptions include marsupials in which the greatest part of maturation occurs afterparturition. The latter are born in a condition which can be considered only that of arelatively mature fetus (Langworthy, 1928; Carmichael, 1970).

Cerebral Cortex: Neuronal DevelopmentNissl (1898) observed that cells are more closely packed in the cortex of species

lower on the phylogenetic tree than those species occupying higher branches, th at is,that are more evolutionarily advanced. Phylogenetically, the high gray/cell coefficient(volume of Griseum/volume of nerve cells contained in it) which expresses the packingdensity of the neurons-first used by von Eco nom o (Haug, 1956)-is the result of anelaborate development of the dendritic processes of neurons, permitting a higherdegree of functional association among the neurons, and possibly contributing tomans intellectual capacity. Computation of the gray/cell coefficient clarifies the rela-tions between the volumes of the nerve cells and the volumes of other griseal struc-tures comprising glia cells, blood vessels, nerve fibers, and intercellular substanceproper (Haug, 1956). In addition to his previously mentioned observation, Nissl sug-gested that the development of the intercellular gray could be used as an index ofphylogenetic evolution. Haug has pointed out that the volume of cortex increasesduring phylogeny to a greater exte nt than the number of nerve cells, hence a highcoefficient in higher animals. Developmental studies suppo rt the idea tha t the growthof the neuropil is an important aspect of the evolution and morphogenetic develop-me nt of neural capac ity in animals, including man (Altman, 1967).

Postnatal neural development and its modification has been studied extensively in

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the rat. At bi rth , the rat superficial corte x is largely ma de up of und iffere ntiate d cells,tightly packed in vertical columns. During the first 2 weeks, these cells differentiatein to either neuroblasts or neurons or in to spongioblasts and neuroglia. T he roughendoplasmic reticulum swells during the transition in to neurons during the secon dweek, and the number of ribosomes increases (Caley & Maxwell, 1968). Cellularorganelles increase in bot h num ber an d intensity.

Eayrs an d Good head (19 59) studied the grow th and ramification of cell processesin ra t se nsori-motor cortex using th e Golgi-Cox staining meth od. F or quantitativeevaluation they used the graytcell coefficient, since formation of the neuropil andcorresponding reduction of cell density is an importa nt p arame ter of brain matur ation.They fo und tha t the greatest reduction in cell density occ urs in the first 6 dayspostnatally, in spite of the fact that the cell number increases. The period of mostrapid increase in the density of a xons is 6- 18 days and of den drites, 18-2 4 days. Th efew axons at birth have a predominantly tangential course; radially oriented axons(presumably specific thalam ic affe rents) appear at 12-18 days. The mean num ber ofdendrites arising from the perikaryon reaches the adult level as early as the 12 th day oflife. Subsequent development of the dendritic field is marked by peripheral extensionof the dendrites and an increase in branching. By the 3rd week of life, Nissl-stainedsections of the cerebral cortex resemble the adult brain, but impregnated sectionsshow a continuing growth of neuronal processes and, in add ition, a furthe r reductionin the packing density of the n eurons (Altm an, 19 67).The rat is an altricial animal with a gestation period of only 21 days, and under-goes a good deal of postnatal neural development and modification. Altman and Das(1964), using tritiated thymidine (3HT) autoradiography, found the proportion oflabelled cells in the granular cortex of the rat at 30 days of age to be 45%, confirmingthe extensive duplication of cells subsequent to birth and the injection of the DNAprecursor. In contrast, Do bbing and Sands (1970) state tha t the timing of events in thecentral nervous system development of the guinea pig, a precocial animal, is in accor-dance with th e precocity of central nervous system developm ent in h s pecies. Theguinea pig, with greater neurological endowment at birth, undergoes less rapid post-natal neural changes than the rat.

The major site o f cell proliferation in the rat neona te is in the su bependym al layerof the brain ventricles. Cell proliferation is very low in the caudal neuraxis (spinalcord, fourth ventricle, and aqueduct) and very rapid around the third ventricle andlateral ventricles in the olfac tory lobes (A ltma n, 1970 ). This fact has recently beenconfirmed b y Haas, e t al. (1970). They injected 3H T in to rats intra-peritoneally,during the course of pregnancy and studied the development of the brain in theneon atal period by observing the dim inuitio n of the labelling ind ex and labellingintensity of various cell types. They demonstrated that in the subependymal layer ofthe lateral ventricle, cellular proliferation includes various medullary layers and fibertracts such as the fimbria of Ihe hippocampus, meduallary layer of the cerebellum,gray matter in the h ippocam pal region, and various layers of the cerebral cortex. Thesubependymal layer of the lateral ventricles in the anterior forebrain retains its high

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proliferation even in th e adult stages (Altman, 1962). [Postnatal cell proliferation inthe ca t (Altman, 1967; Smith, 196 9) and in the guinea pig (Altman & Das, 1 964) hasalso been repo rted.] The cell migration in rats surviving for 1-20 days afte r injection isfrom the subependymal layer of the lateral ventricles t o the hippocampal den tategyrus, where the ordering is chronological according to time of arrival: the first cellsreaching the hippo cam pal d entate gyrus go to the superficial layer.

Postnatal neurogenesis tends to be restricted t o microneurons (Altman, 1967,1970). These are the small nerve cells with very short axons, or possibly n o axons atall, as in the amacrine cells of the retina or the sh or t axoned cells which term inatewithin th e structure in which their cell bodies are located, as in granule cells of thehippocampus or cerebellar cortex. Exceptions seem to be large neurons which areformed after birth in the caudate nucleus, the putamen, and the accumbens septalnucleus in the rat (Altman, 1970; Das & Altman, 1970). The postnatally formedneurons in the caudate and putamen originate from the lateral wall of the lateralventricles whereas those in the accumbens septal nucleus arise from the ventral aspectsof the lateral ventricles.

As men tioned above, undifferentiated cells are formed in the subependymal layerof the internal wall of the lateral ventricles and migrate to the granular layer of thehippocampus. The first step in differentiation, the establishment of synaptic contactand the induc tion of axon form ation , begins only after the undifferentiated cells havereached the dendritic fields of the pyramidal cells of Amm ons horn (A ltman, 1970).There they form synaptic c ont acts with the dendrites of the pyramidal cells. The cellsthen continue to the basal zone of the granular layer w here the second step in thedifferentiation takes place: the outgrow th of its dendrites into the molecular layer andthe establishment of dendritic synapses. Altman suggested that the cell bodies of theprecursor cells of the micron eurons must move past the dendritic field to macro-neurons with which they have synaptic contact when matured, and that some in-fluence emanates from the dendritic plexuses of existing macroneurons. What is respon-sible for this macroneuronal induction of maturation is not yet known.

Noback and Purpura (1961) and Purpura et al. (1964) have recently completeddetailed studies of postnatal ontogenesis of neurons in the cat neocortex. They usedthe Golgi-Cox staining technique along with the following indices of ma turation alstate: ( 1) num ber of dend rites and their branches; (2) size, caliber, and length of theseprocesses; (3) presence of dendritic spines (pedunculated bulbs, thorns, or gemmules);and (4) number and length of axon collateral branches. They classified cortical neu-rons into 3 basic cell types: pyramidal cells, stellate cells, and horizontal cells ofRetzius-Ca jal. Their results are as follows.

The cortex increases in thickness from .8 t o 1.5 mm during the first 3 postnatalweeks. The pyramidal neurons, from the time of their initial development until theirmorphological maturation during the first postnatal m ont h, maintain their radial orien-tation with axons directed into the white matter and apical dendrites extending dis-tally toward the molecular layer (layer I of the cortex). Since differentiation of thecollateral branches of axons and of apical dendrites and basilar dendrites to produce

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tangential or lateral extensions is essentially a postnatal event in the ca t, the changingpyramidal neurons constitute the major postnatal maturational event in the develop-ment of the cerebral cortex. During the perinatal period (birth to 3 days), shortunbranched basilar dendrites and unbranched apical dendritic collateral branches arepresent. At 8 days of age, basilar and apical dend rites are bran ched ; a few havedendritic spines. Between 8-14 days, the basilar dendrites show further branching,collateral branches of apical dendrites divide, and dendritic spines are abundant andprominent. By 21 days of age pyramidal cells are almost completely differentiatedmorphologically. The number of basilar dendrites and apical dendritic collateralbranches are essentially the same as seen in the mature cats cortex. Spines are numer-ous and indistinguishable in overt characteristics from those observed in the adultanimal (Noback & Purpura, 1961). The terminal branches of apical dendrites ofpyramidal cells in superficial layers of the cor tex are more numero us and have a widerlateral spread in the molecular layer I than the terminal branches of apical dendrites ofpyramidal cells in deeper layers. In addition, pyramidal neurons of superficial layersdevelop more rapidly than do those of the deeper layers. Pyramidal neuron axonsundergo relatively delayed growth and myelination with respect to differentiation ofdendrites (Purpura et al., 19 64 ) in accord with a three-phase partially overlappingsequence: (1) development of apical dendrites; (2) cell body and basilar cell bodydevelopment in which apical dendritic growth continues to completion; and (3) axongrowth and myelination. After the first month, the major neocortical maturationalevent is related to an increase in conduction velocity of pyramidal neuron axons. Theprocesses of growth and myelination which underlie changes in the physiological prop-erties of pyramidal neuron axom proceed slowly to completion during the fourth tofifth postnatal m onth (Purpura e t al., 1964). Thus in the cat, in addition to postnatalneurogenesis, extensive modification also occurs in neural architecture and neuralphysiology.

Conel (1941) studied the development of the human cerebral cortex during thefirst month of life. Although the cortex vanes considerably in shape and linear mea-surements are of little significance with respect to increase in size, Conel was able toreport th at on the average, at the en d of 1 month of life, the brain is 1 cm higher and 1cm longer than tha t of the ne wbo rn. C onel followed the growth changes and madethese age com parisons: (1) More consistent and noticeable ma turation occurs in layer V(internal pyramidal layer) than in any other layer. The greatest gain in layer V is in theregion of the trunk, shou lder, and arm in the anterio r central gyrus; no gain is seen inlayer V in the region of representation of the lower extremities. (2) The nerve cellsgenerally decrease in number and increase in size although the p yramidal cells in layerV show the greatest increase. (3 ) The dendrites and axons increase in size during thefirst month. The processes of the giant pyramidal cells in layer V (anterior centralgyrus) are largest and longest and those in the region of the hand show the greatestdevelopment. Cells in layer I1 (internal granular layer) and I11 (external pyramidallayer) show the least increase. (4) The num ber of spines (pedunculated bulbs) increasesparticularly on apical dendrites of layer V. (5) Axons of Golgi I1 cells form a mesh of

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fine fibers in all layers throughout the cortex. The mesh is densest in the receptiveareas with the som esthetic area showing the greatest gain. (6) The size and number ofexogenous fibers increase during the first month. (Exogenous fibers are fibers whichinvade any area of the cortex from m ore or less distant centers.) The greatest increaseis in the giant pyramidal cells in the anterior central gyrus.

Cerebral Cortex: MyelinationJacobson (1963) studied the sequence of myelination in the cerebral cortex of the

laboratory rat. He fou nd th at the cerebral cortex m yelinates successively with theprojection fibers myelinating before association fibers: the sensory radiations myelin-ate first; the cortico-fuga l radiations ne xt; and finally, the callosal projection fibers.Myelination of the medulla, pons, and midbrain is started and completed earlier thanth at of the thalamus and cerebral cortex. The ra t cortex myelinates in a similar mannerto the cat and human cortices: the process starts in motor, somesthetic, auditory,limbic and pyriform cortex and spreads to neighboring regions; the visual sensoryregions mye linate last.

Myelination in the hum an fetus and infant has been studied by Flechsig and Kaes[cited by Altman (1970), Langworthy (1933), Conel (1941), and Yakovlev andLecours (1967) and has been recently reviewed by OBrien (1971)]. Only a slightincrease in myelination occurs during the first postnatal month (Conel, 1941).Myelination is great in the area of the trunk, shoulders, and arms in the anteriorcentral gyrus. The greatest increase in the anterior central gyrus is in the region of thehand. Very little increase is seen in the auditory receiving area and only a slightincrease in the visual receptive area. Some general features of t h ~ s yelination processin man, probably also applicable to othe r mam malian species, are as follows. (1) My-elination does not occur at a uniform rate, but in what seems to be pulses or waves(Fox, 1971a; Yakovlev & Lecours, 1967). Myelination, once begun in one system offibers, often does no t continue rapidly and m ay be surpassed by anothe r system inwhich the process began much later. For example, the acoustic pathway is myelinatedto the level of the inferior colliculus in the 8-mo nth human fetus. By contrast, theoptic fibers receive no myelin until the time of birth. Nevertheless, the optic projec-tion fibers to the cortex are myelinated slightly in advance of the tracts from thecochlear nuclei (Langworthy, 1933). Although development is no t uniform w ithin thecentral ne rvous system, the fully mature organism seems to depend on developm entaland functional convergence; it functions as an integrated whole, making specificadaptations to its own environment, and acquiring species-characteristic behavioralpatterns. (2)In general, myelination first occurs close to the cell body and slowlyproceeds to the terminal portion of the nerve (OBrien, 1970). (3)Tracts becomemyelinated in the order of their importance in controlling the fundamental activitiesof the organism (Langworthy, 1933). Myelination occurs in various tracts of the spinalcord prenatally whereas myelination of tracts in the forebrain occurs postnatally dur-ing early or late infancy. The myelination of cortical gray matter continues past

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puberty, possibly into adulthood (Yakovlev & Lecours, 1967). Flechsig (cited byAltman, 1970) postulated a considerable difference in the rate of myelination ofdifferent cortical regions. He constructed a myelogenetic map of the human cerebralcortex, claiming that sensory projection areas and the motor areas myelinate muchearlier than the intercalated, phylogenetically more recent brain regions, i.e., associa-tion areas. Since myelination of axons alters conductile properties, progressive my-elinatiori may reflect the recruitment of more conduc tile eleme nts int o the circuitry ofthe brain. (4) Tracts in the nervous system become myelinated at the time when theybecome functional. The fetus receives tactile, proprioceptive, auditory, and gustatorystimuli in utero and the tracts converying the input from these various systems arepartially myelinated in the fetus at 6 months and are myelinated to the level of thethalamus at birth (Langw orthy, 1933). However, myelination of th e optic and olfac-tory tracts is delayed until birth. They become fully myelinated when light and smellbecome major stimuli to the body. However, function is possible without myelin;absence of myelin does not m ean absence of fun ctio n (Fox, 1971a). For example,simple reflexes develop in the cat prior to myelination (Windle, Fish, & ODonnell,1934). Nevertheless, an increase in the amount of myelin is correlated with an increasein functional capa city (Fox, 1971a). Huttenlocher (19 70) suggests tha t increases inmyelination of the central nervous system (CNS) may increase the ability of centralaxons to fire repetitively. Langworthy (1933) felt that initiation of activity in a groupof neurons stimulated the laying down of myelin. Myelination can be diminished bypreventing the conduction of impulses in a nerve or the opening of an eyelid (Gyllen-stein, Malmfors, & Norrlin-Grettve, 19 67; OB rien, 1970). However, although animpulse is an imp orta nt stimulus to myelination in a nerve, it is not known h ow thenerve impulse conduction stimulates m yelin formation a t the cellular and molecularlevels.

In summary, the rate of development is not uniform throughout the cerebrum.The development and complication of the structure and function of the cortex corre-spond to the perfection in the forms of behavior and to complication, or increasingcomplexity, of the neural systems concerned with analysis and synthesis of stimulireaching the body (Sarsinov, 1964).

CerebellumThe cerebellum effects smootlxng error correcting, feedback regulation of pos-

tural adjustmen ts, locom otion, and performance of skilled acts (Altman, 1969). Byfollowing the development of these suggested functions, we recognize in the cerebel-lum a good system in which to correlate developmental changes in anatomy w ith bothenvironmental feedback and the behavior of the neonate.In the rat, the area of the cerebellum increases 20-fold over the first 21 days oflife. This is primarily due to growth of the cerebellar cortex (Altman, 1969). Del Cerroand Snider (1 96 8) c onducted electron microscopic studies on the developing cerebel-lum, studying particularly the grow th of axons and dendrites between the 1st and 45th

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postnatal day. The growth process starts under the cell membrane as a local accumula-tion of vesicles w ithou t any visible con tents. This is followed by an outw ard bulging ofthe membrane which then becomes filled with vesicles and is known as the primarygrowth cone, described as early as 1 89 0 by Cajal (Del Cerro & Snider, 1968). In axons,the synaptic and growth cone vesciles cc-exist until the third week or longer. Indendrites, secondary growth cones exist at the tip of the branching dendrites andspines. Variations in the shape of the growth cone vesicles are related to th e age of theanimal.

Growth cones change in appearance as other structures evolve. The biologicalsignificance of growth cones is still unknow n, n or is it known ho w they disappear withmaturation. There are 3 periods of accelerated maturation: at 1-3, 9-1 2, and 1 6-1 9days of age, which appear as waves of cell migration and mitotic activity separated byintervals of less intensive activity. The period from 9-12 days is further characterizedby a trem endous b urst of protein synthesis (Del Cerro & Snider, 1968).

Altman (1966, 1969, 1970) and co-workers (Altman & Das, 1 970 ) have studiedcell proliferation, migration, and differentiation in the cerebellum of the rat, and haveconcluded that cellular proliferation takes place in the germinal layer of the cerebellarcortex, that is, the external granular layer. The migration of precursor cells lasts forabout 3 weeks. The differentiating cells move laterally over the dendritic field of thematuring Purkinje cells. As the cell moves horizontally, the lateral arms of the parallelfiber axons are formed. The cell body the n dips down and, moving through themolecular layer and past the bodies of the Purkinje cells, forms the vertical branch ofthe parallel fiber axon. With the arrival of the granule cell in the interna l granule layer,the form ation of the axon is completed. The formation of the sho rt dendrites andsynaptic con tact w ith mossy fibers subsequently takes place.

As cells migrate from the external granular layer into the molecular and internalgranular layers, the external granular layer becomes depleted of cells. Basket cells inthe lower half of the molecular layer are formed before stellate cells in the upper half.Most of the granule cells are formed during the 2nd and 3rd week of life. Purkinje cellshave not been labelled with 3HT: apparently, the short-axoned, small neurons (micro-neurons) of the cerebellar cortex are of postnatal origin (microneurons), whereas thePurkinje cells (macroneurons), large with long axons, are formed prenatally. Altmanand Das (1970) have also confirmed the chronology of the maturation in the cerebel-lum by studying the con centration and distribution of cholinesterase in the rat.

The dura tion of cerebellar neurogenesis is judged by the time of dissolution of theexternal granular layer (Altman & Das, 1967). In the rat, the cerebellar externalgranular layer disappears at the end of the 3rd week, in the cat at the end of the 2ndmo nth, and in man between the 12t h and 2 0th mon th of life (Altman, 1970). Theduration seems to be correlated with the period necessary for the maturation of theanimals locomotor and related skills and also with the species differences in com-plexity of these skills.

The most recent and intensive studies on postnatal cerebellar development in thecat has been conducted by Purpura et al. (1964). They studied postnatal ontogenesis

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of Purkinje cells at different time periods. By the first week, the Purkinje cells have awell developed main stem w ith a small, highly branched axon distributing collaterals inrelation to adjacent Purkinje cells and other neurons. The main dendritic trun k is notvery prominen t. The tips of the den drites terminate at the lower border of the ex ternalgranular layer, which is about 10-12 layers thick in the immediate neonatal period.Granule cells are more superficially located: Furkinje cell dendrites expand greatlyduring the 2nd week (8-12 days). The external granular layer is less densely packedand ab ou t 8 -1 2 layers ~ c k . etween 3-6 weeks Purkinje cell dendrites elaboratefurther with elongation of the main stem den dritic trunks. The ex ternal granular layerprogressively attenuates by inward migration of cells leading to increased cellularity ofthe molecular layer. At the end of 6 weeks, the external granular layer is about 1-2layers thick. The dissolution of the germinal layer therefore takes abo ut twice as longin the cat as in the rat. At the end of 2 months, the external granular layer hasvirtually disappeared and the Furkinje cells are fully elaborated. In man, developmentof the cerebellum continues beyond the first year (Altman, 197 0).

In the kitte n (birth to 8 weeks postnatal), Sm ith (19 69 ) observed postnatal devel-opment in Clarkes column (the area in the spinal cord from which the posteriorspinocerebellar trac t arises) in the L2 -3 segments. At b irth there is a lack of stainablesynapses, with great changes by 3 weeks when there are 2 types of synaptic endings.There is centripetal orientation of the dendritic tree in relation to the center ofClarkes column.Altman (1967) and Dobbing, Hopewell, Lynch, and Sands (1970) demonstratedthe high susceptibility of the developing rat cerebellum (in contrast to other brainregions) to X-irradiation leading to eventual impairment in motor tasks. Recently,Altman, Anderson, and Strop (1971) have shown that focal X-irradiation duringinfancy can lead to a decrease in the mature weight of the rats cerebellum due tointerference with acquisition of microneurons. Further, animals given numerous ex-posures persisted longer in displaying infantile m otor patterns.

Tasks in which locomotor and manipulatory appendages of the body are used forcomplex m oto r performances require ce ntral nervous mechanisms in which the con-nections among the neural elernents are not determined totally by morphogeneticmechanisms but are influenced environmentally (Altman, 1966). The postnatal genesisand m aturation of the mod ulatory comp onents of the cerebellar cortex can be relatedto the circumstance that the connections established by these elements are condi-tioned by environmental feedbacks or by input-contingencies which connotes a com-parator or matching mechanism. (See, for example, Altman, 1967, and Sokolov,1960). Held and Bossom (1961) demo nstrated tha t self-produced movements, (sensoryfeedback) are necessary for adult hu mans to ad apt to re-arrangement of their environ-ment and tha t passive m otio n is no t sufficient. They questioned whether developmentand compensation reflect the same process. If these processes do, then the need forself-produced movement and contingent reafferent stimulation in compensation-environmental feedback-are equally applicable to development. Held and Hein (1963)demonstrated that self-produced movement with concurrent visual feedback is neces-

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sary for the development of visually guided behavior in the cat. (See, also, Held,1968). Hein, H eld, and Gower (1970) have very recently demonstrated th at if one eyeis covered during self-produced movement then the visually guided behavior acquiredby the open eye is not transferred to the unused eye, even with the corpus callosumand other commissures intact. They demonstrate that environmental feedback is im-portant in the development of a behavioral repetoire although the relative contribu-tions of the built-in factors and of the environmental feedback system remain difficultt o assess.

Environmental Influences on the Developingand Mature Nervous SystemsIn a series of studies, Hubel and Wiesel investigated both the effect of visual

deprivation on the development of the striate cortex in kittens and recovery from thedeprivation over a period of time. They made recordings at 3 months from the visualcortex of kittens raised from birth with one eye sutured closed and showed that fewcells could be driven from the deprived eye (Wiesel & Hubel, 1963). By producingartificial squints in kittens, Hubel and Wiesel (1965) demonstrated that binocularinteraction in the developing striate corte x is imp orta nt. They severed the right medialrectus muscle at about the time of normal eye opening and produced thereby adivergent squint. The animals were then raised for periods of 3 months t o 1 year in anormal environment. When the 2 eyes were tested, no behavioral visual deficits wereevident. E lectrophysiological recordings from the striate corte x were normal; however,the proportion of binocularly driven cells was markedly decreased from a bou t 80 % to20%. The cortex appeared microscopically normal. T he investigators concluded th at ashift in ocular dominance ha d occurred due t o the squ int, with a cell coming to favormore and more the eye tha t dominated it at birth and ultimately losing all connectionwith the nondominant eye. The lack of synergy in the input from the 2 eyes wassufficient to cause a profound disruption in the co nnections that subserve binocularinteraction (Hubel & Wiesel, 1965). Furthermore, recovery from the effects of earlymonocular or binocular visual deprivation, whether measured behaviorally, morpholog-ically, o r in terms of single-cell cortical activity, was severely limited even fo r recoveryperiods of a year or more (Wiesel & Hubel, 1965).

That the fine structure of the nervous system can be altered by changes in theenvironment has been demonstrated by a number of workers. Holloway (1966) pre-sents evidence th at supports the suggestion that dendritic branching is increased in thevisual cortex of animals raised in a complex, enriched environment. Cragg (1969),studying rod-bipolar junctions in the rabbit, demonstrated microscopic (electron)changes within the first few min utes of exposure to daylight in dark-raised animals.Schapiro and Vukovich (1970), studying the rat cortical pyramidal cell, showed thatearly stimulation (handling, stroking, shaking, placing in h ot and cold wa ter) leads t oan increase in the number of dendritic spines and the number of neurons staining at

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8-16 days of life. They postulated tha t the neurons stained are those t hat are func tion-ally involved at the time of staining. These authors concluded that the effect ofafferent input on development of the dendritic spine may represent the neuroanatom-ical basis for the influence of early experience on subsequent behavior. Hirsch andSpinelli (1970) raised cats from birth with one eye viewing horizontal lines, and theother eye viewing vertical lines. They fou nd t hat units in the visual cort ex withhorizontal fields were activated only by the eye exposed to horizontal lines, and unitswith vertical fields were activated only by the eye exposed to vertical lines. Unitrecordings yielded n o oblique visual fields. The investigators conc luded tha t func tiona lneural connections can be selectively and predictably modified by environmentalstimulation. Fifkova (1970a, b, c) has recently demonstrated anatomical changes inthe visual cortex of rats unilaterally deprived of visual stimulation. Changes weredetectable 1 0 days after lid suture ; the changes were independent of previous visualexperience (Fifkova, 1970a). In rats monocularly deprived at 14 days of age, the meandensity of synapses in pre-visual corte x supplied by the deprived eye was 20% less thanthe controls (Fifkova, 1970b), and the size of axo-somatic syna ptic conta cts weresmaller throu ghou t all the layers s tudied (Fifkova, 19 70 ~ ).

Sugita (191 8) experimentally starved young rats, by separation from the nursingmother for a stated period each day, by entrusting one mother with an excessivenumber of young (greater than 17) and thereby reducing the milk for each youngster,and by starving the nursing mother producing a decrease in milk secreted. He foundthat myelination was somewhat retarded in the underfed rats and that, although celldivision was normal, the underfed rats were smaller and weighed less. He reported nodecrease in cell number, but rather decreases in the growth or development of theconstit utent n eurons. However, Dobbing, Hopewell and Lynch (197 1) have recentlydemonstrated that moderate undernutrition during the first 21 days of life produces adeficit of neurons in the rat cerebral cortex and a reduction of weight and cell num berin the cerebellum (granular layer).

Gyllenstein et al. (1967), workmg with rats, compared the effect of bilateralremoval of b ot h eyes at birth with tha t of rearing animals in complete darkness. Theystudied the developing visual cortex, lateral geniculate nucleus, and superior colliculusand n oted tha t the effe ct of bilateral enucleation was greater than dark-rearing on thedeveloping visual system. They concluded that impulses along the optic nerve, origi-nating from the retinae of the dark-reared animals, were important in the develop-me ntal process.

Motor neu rons in th e developing spinal cord are greatly influenced by the develop-ing limb , as revealed in ex perim ents consisting of grafting of add itiona l limbs or ofamputating a limb at different developmental stages. Hamburger (1934) found thatremoval of the wing bud of the chick embryo at 255-3 days of incubation resulted in areduction of the number of motor neurons in the ventrolateral column of the spinalcord. Within 3 days after removal of the hindlimb bud in the chick embryo, approxi-mately 20,000 motor neurons died in the lumbosacral region of the spinal cord(Hamburger, 1958). (See Hughes [196 8, Chapter 31 and Jacobson [1970, pp .240 246 3 for reviews of t h s l it era tu re) .

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Altman and Das (1967); Altman, Wallace, Anderson, and Das (1968); Diamond,Krech, and Rosenzweig (1964); and Diamond, Law, Rhodes, Linder, Rosenzweig,Krech, and Bennett (1966) studied the effects of enriched versus impoverished envi-ronments on the structure and function of the rat cortex. The brains of animalsexposed t o en riched environm ents were fou nd t o have the following characteristics incomparison with the brains of the animals exposed t o impoverished conditions: in-creased weight of the cerebral cortex, increased total activity of acetylcholinesterasethroug hou t the brain, increased cortical de pth , some indications of increased vascu-larity in the cortex (Bennett, Diamond, Krech, & Rosenzweig, 1964; Diamond e t al.,1964; Rosenzweig, Krech, Bennett, & Diamond, 1968), and an increased number ofnewly formed glia cells (Diamond et al., 1966; Altman & Das, 1967). Some of theseinduced cerebral changes may regress after animals are removed from the enrichedconditions (Zolman & Morimoto, 19 62; Valverde, 197 1) bu t how these changes inbrain struc ture affect the organism is no t ye t understood.

CommentFuture research in the study of postnatal neural ontogeny should concern itself

with investigating the in terplay of gen ic-environment influences on the developingnervous system. Efforts m ust be made t o correlate behavioral and anatomical findings.At the molecular level, the conditions necessary for the initiation of the myelinationprocess should be investigated and the relationship between stimulation (i.e., function)and myelination should be m ore carefully defined.

Better definition and control of stimulus conditions must be undertaken (Fox,1971b). Enriched and deprived are relative terms and have different meanings indifferent laboratories. In themselves, they do not reveal very much about the truelaboratory environment. Control of temperature, visual, auditory, tactile, and olfac-tory cues is mandatory as is precise control of handling of the animals. [See Morton(1968) for a review of the effects of handling in laboratory animals.] Cage size (Bell,Miller & Ordy, 1971), litter size (LaBarba & White, 1 971 ; Poole, 1 966), time ofweaning, and the existence of possible endogenous rhythms must also be controlledfor. L ittle is gained by knowing the genetic strain of the animal under st ud y if theexpe riential life-history is only partially accou nted for (see Denenberg , 19 69 ). Brain(1971) suggested that critical periods may be the source of nongenetic variation some-times encountered in pure strains of rats and mice; Henderson (1968 , 1 97 0) hasdemonstrated that laboratory rearing and treatment effects in early experience canobscure genetic influences on behavior. Furthermore, Henderson (1970) concludedthat investigators must be aware of the possibilities that early environmental inter-actions with geno type may limit the validity of their findings t o their own laboratorysituations. Genetic and environmental (experiential) control must complement oneanother in order to produce meaningful and valid results.

Further understanding of the premature and of the birth process might also shedlight on CNS development. Changes in stimulus parameters between late fetal and

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early neonatal life should be considered as might the effects of various modes of birth(cesarean vs. vaginal parturition) (Meier, 196 4; Meier & Garcia-Rodriguez, 1966;Grota, Dennenberg, & Zarrow, 1966). Careful control of the prentatal environmentmay be as important in some species as is control of the postnatal environment.

It should be stressed that the developmental method provides a key to under-standing the workmgs of the mature, integrated nervous system. The study of individ-ual components during their maturation must lead to further consideration of howthese parts fit together to form a whole, a whole that is far greater than the sum of itsparts. A gestalt of CNS interaction is the end-product of the developmental method.Just as the nature-nurture issue is no longer separable into mutually exclusive halves,neither is the nervous system divisible in to isolated discrete parts.

ConclusionPostnatal neurogenesis and/or neuronal plasticity has been repeatedly confirmed

in mouse, rat, cat, and man. It takes place at different rates in different parts of thebrain, the heterochronicity of which may have adaptive value for the neonate(Anokhin, 1964). This level of neurogenesis appears to be restricted to microneuronswhich modulate interaction among macroneurons. The microneurons function tochannel neural information and to increase the number of synaptic connections, andtherefore the presumed computing power and storage capacity of the brain. Theincrease in the neuropil is greatest in the higher species and reflects the importanceof growing connectivity. Microneurons situated near the juncture of the first- andsecond-order afferents are found to be recipients of centrifugal efferents descendingfrom the higher levels of the nervous system, such as centrifugal efferents of theolivo-cochlear bundle that terminate on granule cells (microneurons) in the ventralcochlear nucleus and centrifugal efferents of the optic tract that terminate onamacrine cells in the r etina .

Neuroanatomical, chemical, and physiological studies suggest that environmentalstimulation may be necessary for normal postnatal growth but the unique contribu-tions of environmental influences on p ostnatal neurogenesis are difficult to assess.

To view the nature-nurture in an either/or, mutually exclusive framework is un-real. Normal developm ent mo st certainly requires bo th the proper genetic endow men tof the developing structure and the proper env ironmental stimulation for dev elopmentafter birth. Postnatal development relies solely neither on the evolutionarily built-indirective forces (environmental expectancy model) nor on the immediate postnatalenvironment (environmental dependency model) but rather on the intimate interplayof the two.

NotesMarc Bekoff was supported by a pre-doctoral fellowship under PHS Grant GM-1900,from the National Institutes o f Health.

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Many thanks to Alice Bronsdon for her patience and careful typing of theSend reprint request to : Marc Bekoff; Department of Psychology, Washington

manuscript.University, St. Louis, Missouri 63 130 U.S.A.

ReferencesAltman, J. (1962). Are new neurons formed in the brains of adult mammals? Science,Altman, J. ( 1966). Autoradiographic and histological studies of postnatal neuro-

genesis. 11: A longitudinal investigation of the kinetics, migration and transforma-tion of cells incorporating tritiated thymidine in infant rats, with special referenceto postnatal neurogenesis in some regions. J. Comp. Neurol., 128: 431-474.

Altman, J. (1967). Postnatal growth and differentiation of the mammalian brain, withimplications for a morphological theory of memory. In G. Quarton, T.Melnechuk, and F. 0. Schmitt (Eds.), Neurosciences: A Study Program. NewYork: Rockefeller University Press. Pp. 723-743.

Altman, J. ( 1969). Autoradiographic and histological studies of postnatal neuro-genesis: 111: Dating the time of production and onset of differentiation of cerebel-lar microneurons in rats. J. C o m p . Neurol., 136: 269-294.

Altman, J. (1970). Postnatal neurogenesis and the problem of neural plasticity. InW. A. Himwich (Ed.), Developmental Neurobiology. Springfield: Thomas. Pp.

Altman, J., Anderson, W. J., and Strop, M. (1971). Retardation of cerebellar andmotor development by focal X-irradiation during infancy. Physiol. Behavior, 7:

Altman, J., and Das, G. D. (1964). Autoradiographic examination of the effects ofenriched environment on the rate of glial multiplication in the adult rat brain.Nature (London), 204: 1161-1 163.

Altman, J . , and Das, G. D. (1967). Postnatal neurogenesis in the guinea pig. Nature(London), 214: 1098-1 101.Altman, J . , and Das, G. D. (1970). Postnatal changes in the concentration and distribu-tion of cholinesterase in the cerebellar cortex of rat. E x p . Neurol., 28: 11-34.

Altman, J. , Wallace, R. B., Anderson, W. J., and Das, G. D. (1968). Behaviorally in-duced changes in length of cerebrum in rats. Develop. Psychobiol., 1: 112-1 17.Angevine, J. B., Jr. (1965). Time of neuron origin in the hippocampal region: An

autoradiographic study in the mouse. E x p . Neurol., Supplement 2 : 1-70.Anokhin, P. K. (1964). Systemogenesis as a general regulator of brain development. InW. A. Himwich and H. E. Himwich (Eds.), The Developing Bruin, Progress in Bruin

Research, Vol. 9. Amsterdam: Elsevier, Pp. 54-86.Arbib, M., and Kahn, B. (1969). A developmental model of information processing in

child. Perspectives Biol. Med. Pp. 3-28.Bell, R. W., Miller, C. E., and Ordy, J. M. (1971). Effects of population density and

living space upon neuroanatomy, neurochemistry, and behavior in the C57 B1/10mouse. J. Comp. Physiol. Psychol, 75: 258-263.Bennett, E. L., Diamond, M. C., Krech, D., and Rosenzweig, M. R. (1964). Chemicaland anatomical plasticity of the brain. Science, 146: 6 10-6 19.

Brain, P. F. (1971). Some physiological and behavioral consequences of hormonalmodifications in the early life of rodents-A review. Comm. Behav. Biol., 6: 7-18.

Caley, D. W., and Maxwell, D. (1968). An electron microscopic study of the neurons

135: 1127-1 128.

197-237.

143-150.

8/3/2019 Bekoff & Fox 1972

16/19

338 BEKOFF A N D FO X

during pos tnata l developm ent of the ra t cerebra l cor tex. J . Comp. Neurol.. 133:17-44.Carmichael, L. K. (19 70) . Th e onset and early developmen t of behavior. In P. A.Mussen (Ed .), Carmichaels Manual of Child Psychology, Vol. 1. New Y ork : Wiley.Chance, M . R. A., and Jolly , C. J . (1970) . Social Groups ofili lonkeys, Apes, and Men.New York: Dut ton.Conel, J. L. (1941). Development of the human cerebral cortex during the firs t month

of life. Arch. Neurol, Psychiat., 45: 387-389.Cragg, B. G . (1 969). Stru ctur al changes in naive retinal synapses detectable withinmin utes of the firs t expo sure to daylight. Brain Aes., 15: 79-96.Crat ty , B. J . (1970) . Perceptual and Motor Development in Infants and Children. NewYork: MacMiUan.Das, G., and Altman, J. ( I 970). Postnatal neurogenesis in the caudate nucleus andnucleus accumbens sept i in the rat. Brain Res., 21: 122-127.Del Cerro, M. P., and Snide r, R. S. (1968). Studies on th e developing cerebellum:Ultras t ruc ture of the growth cones . J. Comp. Neurol., 133: 341-362.Denenberg, V. H. ( 1 969). Expe rimen tal program ming of l ife his tories in the rat . I n A.Ambrose (Ed.), Stimulation in Early Infancy. N ew York: Academic Press. Pp.Diamond, M. C., Krech, D., and Rosenzweig, M. R. (196 4) . The effec ts of an enrichedenvironment on the histology of the rat cerebral cortex. J. Comp. Neurol., 123:1 11-120 .Diamond, M. C., Law, F. , Rhodes , H., Linder , B., Rosenzweig, M. R. Krech, D., andBennett , E. L. (1966). Increases in cortical depth and glia numbers in rats sub-jec ted t o enriched environments . J. Comp. Neurol., 128: 117-125.Dobbing, J . , and Sands, J. (1970) . Growth and development of the bra in and spinalcord of the gu inea pig. Brairf Res., 17: 1 15-123.Dobbing, J. , Hopewell , J. W., Lyn ch, A., an d S ands, J . (19 70) . Vulnerabili ty of devel-oping brain: I . So me lasting ef fects of X-irradiation. Exp. Neurol., 28: 442-449.Dobbing, J. , Hopew ell , J . W., and Lynch , A . (1 97 1). Vulnerabili ty of d eveloping brain:Permanent def ic i t of neurons in cerebral and cerebellar cortex following earlymild undernutrit ion. Exp. Neurol., 32: 439-447.Eayrs, J. T., and Goodhead, B. (19 59) . Postna tal developm ent of the cerebral cortex inthe rat ..I.na t . , 92: 385-402.Fifkova, E. (19 70a ). The effect of unilateral deprivation on visual centers in rats. J.

Coinp. Neurol., 4: 43 1 -438 .Fifkova, E. (1 970b) . The effec t of monocu lar depriva t ion o n the synapt ic contac ts ofthe visual cortex. J. Neurobiol., 1: 285-294.Fifkova, E. ( 1 9 7 0 ~ ) .Changes of axosom atic synapses in the visual cortex of m onoc -ularly deprived rats. J . Neuro biol., 2: 6 1-7 1 .F o x , M. W. ( 1 970). Reflex develop men t and behavioral organization. In W. A.Himwich (Ed.) , Developmental Neurobiology. Springfield: Thomas, pp. 553-580.F o x , M. W. (1971a) . Integrative Development of the Brain and Behavior of the Dog.Chicago: University of Chicago Press.F o x , M. W. (1971b). Effects of rearing conditions on the behavior of laboratory ani-mals. In Defining the Laborutory Animal. Washington, D.C. : National Academy ofSciences. Pp . 294-3 12.Got t l ieb , G. (19 70) . Concep tions of prenatal behavior. In L. R. Aronso n, E. Toba ch,D. S. Lehrman, and J. S. Rosenblatt (Eds.), Development and Evolution of Be-havior. San Francisco: Freeman. Pp. l l 1-137.

Pp. 447-563.

21-43.

8/3/2019 Bekoff & Fox 1972

17/19


Grota, L. J., Denenberg, V., and Zarrow, M. X. (1966). Normal versus Cesarean de-livery: Effects on survival probability, weaning weight, and open field activity. J.Comp. Physiol. Psychol., 61: 159-160.

Gyllenstein, L., Malmfors, T., and Norrlin-Grettve, M . (1967). Visual and non-visualfactors in the centripetal stimulation of postnatal growth of the visual centers inmice. J. Comp. Neurol., 131 : 549-558.

Haas, R. J., Weiner, J., and Fliedner, T. M. (1970). Cytokinetics of neonatal brain celldevelopment in rats as studied by the complete 3H thymidine labelling method.J. Anat., 107: 421-437.

Haddara, M. (1956). A quantitative study of the postnatal changes in the packingdensity of the neurons in the visual cortex of the mouse. J . Anat., 90: 404-501.

Hamburger, V. H. (1934). The effects of wing bud extirpation on the development ofthe central nervous system in chick embryos. J. Exp. Zool., 68: 449-494.

Hamburger, V. H . ( 1958). Regression versus peripheral control of differentiation inm-motor hypoplasia. Am. J . Anat., 102: 365-410.

Haug, H. (1956). Remarks on the determination and significance of the gray cellcoefficient. J. Comp. Neurol., 104: 473-492.

Hebb, D. 0. (1953). Heredity and environment in animal behaviour. Brit. J. Anim.Behav., 1: 43-47.

Held, R. (1968). Action contingent development of vision in neonatal animals. In D. P.Kimble (Ed.), Experience & Capacity, Vol. 4. New York: New York Academy ofScience. Pp. 31-1 11.

Held, R., and Bossom, 3. (1961). Neonatal deprivation and adult rearrangement: Com-plimentary techniques for analyzing plastic-sensory-motor coordinations. J.Comp. Physiol. Psychol., 54: 33-37.

Held, R., and Hein, A. (1963). Movement-produced stimulation in the development ofvisually guided behavior. J . Comp. Physiol. Psychol., 56: 872-876.

Hein, A., Held, R., and Gower, C. (1970). Development and segmentation of visuallycontrolled movement by selective exposure during rearing. J. Comp. Physiol.

Henderson, N. D. (1968). The confounding effects of genetic variables in early experi-ence research: Can we ignore them? Develop. Psychobiol., 1: 146-152.

Henderson, N. D. (1 970). Genetic influences on the behavior of mice can be obscuredby laboratory rearing. J. Comp. Physiol. Psychol., 72: 505-5 11.

Himwich, W. A. (1962). Biochemical and neurophysiological development of the brainin the neonatal period. International Review of Neurobiology, Vol. 4. New York:Academic Press. Pp. 117- 158.

Himwich, W. A., and Dravid, A. R. (1967). Amino acid content of various brain partsas related to neurophysiological and behavioral maturation. In A. Minkowski(Ed.), Regional Development of the Brain in Early Life. Oxford: Blackwell. Pp.

Hirsch, V., and Spinelli, P. (1970). Visual experience modifies distribution of horizon-Holloway, R. L., Jr. (1966). Dendritic branching: Some preliminary results of trainingHubel, D. H., and Wiesel, T. N. (1965). Binocular interaction in striate cortex ofHughes, A. F. W. (1968). Aspects of Neural Ontogeny. New York: Academic Press.Humphrey, T. (1 970). Postnatal repetition of human prenatal activity sequences with

some suggestions of their neuroanatomical basis. In R. Robinson, (Ed.), Brain andEarly Behavior. New York: Academic Press. Pp. 43-84.

Psychol., 73: 181-187.

257-271.tally and vertically oriented receptive fields in cats. Science, 168: 869-871.and complexity in rat visual cortex. Brain Res., 2: 393-396.kittens reared with artificial squint. J . Neurophysiol., 28: 1041-1059.

8/3/2019 Bekoff & Fox 1972

18/19

340 BEKOFF AND FOX

Huttenlocher , P. R. (1970). Myelination and the development of function in immaturepyramidal tract. 1:xp. Neurol., 29: 405-41 5 .Jacobson, M. (1970) . Developmental Neurobiology. New York: Hol t , Rinehart &Winston.Jacobson, S. ( 1 963). Sequ ence of m yelinization in the brain of the albino rat . A.Cerebral corte x, thalamu s and related structures. J. Comp. Neurol., 121: 5-29.Krushinskii, L. V. (1962) . Animal Behavior, Its Normal and Abnormal Development.New York: Consultants Bureau.LaBarba, R. C., and White, J. I,. (1971 ). L itter s ize variations and emo tional reactivityin BALB /c mice. J. Comp. .Physiol. Psychol., 75: 254-257.Langworthy, 0. R. ( I 928). The behavior of pouch-young opossums correlated withthe myelinization of tracts in the nervous system. J. Comp. Neurol., 4 5 : 201-247.Langworthy, 0. R. (1 933). Developm ent of behavior patte rns and m yelinization of th enervous system in the human fetus and infant. Contrib. Embryol., Carnegie Insti-t u t e , XXI V: 3-57.Lehrman, D. S. (1953) . A critique of Ko nra d Lorenzs theo ry of instinctive behavior.Quart. Rev. Biol,, 28: 337-363.Lehrman, D. S. (1970 ) . Semant ic and conceptual i s sues in the na ture-nuture problem.In L. R. Aronson, E. Tobach, D. S. Lehrman, and J. S. Rosenblatt , (Eds.), Devel-opment und Evolution of Behavior. San Francisco: Fre ema n. Pp. 17-52.Lorenz, K. 2. (1965) . Evolution and Modification o f Behavior. Chic ago: U niversity ofChicago Press.Mason, W. A. (1968) . Scope and potent ia l of primate research. In J . H. Masserman(Ed.) , Animal and Human. New York: G rune & Stra t ton. Pp. 101-11 1.Meier, G. W. (1 964). Behavior #of nfant m onke ys: Differences attributable t o mod e ofbirth. Science. 143: 968-970.Meier, G . W., and Garcia-Rodn.guez, C. (1 966 ). Co ntin uin g behavioral differe nces ininfant mo nke ys as related t o mod e of delivery. Psychol. Rep., 19: 1219-1225.Morton, J . R. C. (19 68). E ffects of early experien ce handling and gentling onlaboratory animals . In M. W. Fox (Ed.) , Abnormal Behavior in Animals. NewYork: Wiley. Pp. 261-292.Myslivecek, J . (1970). E lectrophysiology o f the developing brain-Central and EasternEuropean contr ibut ions . I n W. A. Himwich (Ed.), Developmental Neurobiology.Springfie ld: Thomas . Pp. 475-527.Nissl, F. (1898). Nervenjcllen und grave substanz. Munch. Med. Wschr., 45: 988-992.Noback, C. R., and Purpura, D . P. ( 1 96 1). Postna tal ontogenesis of neurons in the cat

OBrien, J . S. (1970). Lipids and myelination. In W. Himwich (Ed.) , DevelopmentalPoole, T. B. (1966). Aggressive play in polecats. Symp. 2001.SOC.Lond. , N o. 1 8 :Purpura , D. P., Schofer, R. J., Housepian, E. M., and Noback, C. R. (1964) . Compara-tive ontogenesis of s tructuro-f unction al relationships in cerebral and cerebellarcortex. In D. P. Purpura and J . P. Schade (Eds.), Growth and Maturation of the

Brain, Progress in Brain Research, Vol. 4. Am sterdam : Elsevier. Pp. 187-22 1.Purpu ra, D. P., Schofer, R. J. , and Scarff, T. (1967 ). Intracellular s tud y of spike poten-tials and synaptic activit ies of neurons in immature neocortex. In A. Minowski(Ed.) , Regional Development of the Brain in Early Life. Oxford: Blackwell . Pp.

neocortex. J. Comp. Neuro.!., 117: 291-307.Neurobiology. Springfield: Thomas. Pp. 262-28 6.23-44.

2 9 7- 3 25.

8/3/2019 Bekoff & Fox 1972

19/19


Rabinowicz, T. (1967). Techniques for the establishment of an atlas of the cerebralcortex of the premature. In A. Minowski (Ed.), Regional Development of theBrain in Early Life. Oxford: Blackwell. Pp. 7 1-89.

Richter, D. (1967). Enzymic activity in the nervous system in early life. In A .Minowski (Ed.), Regional Development of the Brain in Early Life. Oxford: Black-well.

Rose, G. H., and Ellingson, R. J. (1970). Ontogenesis of evoked potentials. In W. A.Himwich (Ed.), Developmental Neurobiology. Springfield: Thomas. Pp. 393-440.

Rosenzweig, M. R., Krech, D., Bennett, E. L., and Diamond, M. C. (1968). Modifyingbrain chemistry and anatomy by enrichment or impoverishment of experience. InG.Newton & S. Levine (Eds.), Early Experience and Behavior: The Psychobiologyo f Development. Springfield: Thomas. Pp. 258-298.

Sarsinov, S, (1964). The evolutionary aspect of the integrative function of the cortexand subcortex of the brain. In D . P. Purpura and J. P. Schade (Eds.), Growth andMaturation of the Brain, Progress in Brain Research, Vol. 4. Amsterdam: Elsevier.

Schapiro, S., and Vukovich, K . R. (1970). Early experience effects upon corticaldendrites. Science, 167: 292-294.

Schneirla, T. C. ( 1966). Behavioral development and comparative psychology. Quart.Rev. B i d , 41: 283-302.

Smith, D. E. (1969). Observations on the postnatal development of Clarkes column inthe kitten. J. Comp. Neurol., 135: 263-274.

Sokolov, E. N. (1960). Neuronal models and the orienting reflex. In M. A. B. Brazier(Ed.), CNS and Behavior, 3rd Conference. New York: Josiah Macy Jr.Foundation. Pp. 187-276.

Sugita, N. (19 18). Comparative studies on the growth of the cerebral cortex. VII: Onthe influence of starvation at an early age upon the development of the cerebralcortex-albino rat. J. Comp. Neurol., 29: 177-240.

Swaiman, K. F. (1970). Energy and electrolyte changes during maturation. In W. A.Himwich (Ed.), Developmental Neurobiology. Springfield: Thomas. Pp. 3 1 1-330.

Uzman, L. L. (1960). The histogenesis of the mouse cerebellum as studied by H3tritiated thymidine uptake. J. Comp. Neurol., 114: 137-159.

Valverde, F. (197 1). Rate and extent of recovery from dark rearing in the visual cortexof the mouse. Brain Res., 33: 1-1 1.

Wiesel, T. N ., and Hubel, D. H. ( 1963). Single-cell responses in striate cortex of kittensdeprived of vision in one eye. J. Neurophysiol., 26: 978-993.

Wiesel, T. N., and Hubel, D. H. (1965). Extent of recovery from the effects of visualdeprivation in kittens. J . NeurophysioL, 28: 1060-1072.

Windle, W. F., Fish, M. W., and ODonnell, J. E. (1934). Myelogeny of the cat asrelated to development of fiber tracts and prenatal behavior patterns. J. Comp.Neurol., 59: 139-155.

Yakovlev, P. I., and Lecours, A . R. (1967). The myelinogenetic cycles of regionalmaturation of the brain. In A . Minowski (Ed.), Regional Development o f theBrain in Early Life. Oxford: Blackwell. Pp. 3-70.

Zolman, J. F., and Morimoto, H. (1962). Effects of age on training on cholinesteraseactivity in the brains of maze-bright rats. J. Comp. Physiol. Psychol., 55: 794-800.

Pp. 30-38.

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Bekoff & Fox 1972