AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 52405-419 (1980)

A Quantitative Comparison of the Hominoid Thalamus:

Ill. A Motor S u b s t r a t e t h e Ventrolateral Complex
ESTE ARMSTRONG Department of Anthropology, Colurnb~ciUniwrsit.y, New York, N e w York, cind Department o f Ancitomy, Louisiana State Uniuerssty, New Orleons, Louiaicina 701 19

K E Y WORDS Thalamus, Ventrolateral complex, Evolution

ABSTRACT Nuclear volumes, nerve cell densities, numbers of neurons, and volumes of nerve cell perikarya of the thalamic ventrolateral complex tVL), a neural substrate for movement, were measured in specimens from two gibbons, one gorilla, one chimpanzee, and three humans, and t h e values were compared. The human VL had about one-and-a-half times as many neurons as did those of the great apes. The relative frequencies of the sizes of nerve cell perikarya differed slightly i n the ventrolateral segment of VL; no differences were noted in the rest of VL. Compared with findings from other parts of the thalamus, the differences in the volumes of VL were greater than those found in the thalamic sensory nuclei, similar to those of the rest of the thalamus, and less than those found in the whole brain. The increased number of neurons in human VL was similar to that of the somatosensory relay complex, but greater than those of the auditory and visual nuclei and less than those ofthe limbic and association nuclei. In human evolution, the numbers of neurons in the VL appeared to increase at a faster rate than did neurons of the pyramidal tract, whereas the motor cortex apparently increased at a rate greater than VL
During hominid evolution, bipedalism and the oral and manual dexterity necessary for language, facial expression, and tool-making must have been accompanied by alteration in parts of the neural substrates for movement, (Holloway,'75, '70, '68; Phillips and Porter, '77; 'I'uttle et al., '79). Some of the motor regions' of the brain among hominoids have been compared. The motor cortex and the cerebellum are relatively prominent in humans t Passingham, '75; Stephan e t al., '70).Another motor region, the striatum, shows a small overall differential enhancement (Stephan,et al.,'70; Stephan, '79) but possible species-specific shifts between its components tBonin and Shariff, '51; Frahm et al., '79; Harmon and Carpenter, '50; Holloway, '68 1. The ventrolateral complex t VL), the specific motor relay nucleus of the thalamus, is interposed between the pyramidal system of the motor cortex and three other motor centers of the brain. the cerebellum, the globus pallidus, a n d t h e s u b s t a n t i a nigra ( C a r p e n t e r , '76; Strick, '76). The cerebellum and motor cortex project to all parts of VL, whereas the globus pallidus and substantia nigra have more limitedconnections (Mehler et al.,'58; Mehler, '71, Rinvik, '75; Kunzle, '76; Catsman-Berrevoets and Kuypers, ' 7 8 ) .Nonmotor cortical inputs as well as i n t e r n a l ( e . g . , cortico-cerebellothalamic-cortical) and external motor feedback systems pass through VL (Phillips and Porter, '77). Part of the reticular activating system that desynchronizes the cortical electroencephalogram is relayed through VL (Purpura, '72, Ohmoto et al., '78). Integration among the incoming systems uses populations of interneurons (Desiraju and Purpura, '70; Purpura, '72)as well as differing synaptic patterns on relay neurons tDeniau e t al., '78).
'The term "motor region.;" 01 the 1)r:iin doe5 not rnciin t h a t these iiie invol\ed only in m u v r m e n t 01' t h x t other :ire:ih have no involvement T h p motor ;ireas i i i e more directlytied i n with movement t h a n are other iireiih, hut they d m participate i n other functirmal syhtem.;
dieas

Received J u n e 23, 1979, accepted Septemher 13, 1979

0002-9483/8015203-04~5$0~ 90 (1 1980 ALAN R LISS, INC

405

406

ES'I'E ARMSTRONG

The major output of VL is to the motor cortex, on which i t can exert a direct and powerful influence (Yoshida et al., '66; Strick and Sterling, '74; Phillips and Porter, '77). Activation of VL before voluntary movement may represent a general adjustment of posture to accommodate the movement (Evarts, '71; Joffrey and Lamarre, '74; Jasper and Bertrand, '66). VL also helps to control muscle tone and speed of movements t Hassler, '72; Jasper and Bertrand, '66). Activities of cells in VL are not restricted to a particular phase of movement such as flexion, b u t a p p e a r correlated w i t h complex movements i Massion and Smith, '73; Massion, '76-'77). That many of the postural and phasic functions of VL have been found in different mammals (Evarts,'71; Amassian et al., '72) does not preclude species-specific adaptations. Postural a d j u s t m e n t s a r e likely to differ a m o n g brachiators, knuckle-walkers, and bipeds. Adaptations within VL to support a human behavior pattern is suggested. Studies of natural lesions from hemorrhages and tumors and from stereotaxically placed lesions made to abolish tremor and rigidity in patients with Parkinson's disease indicate that VL is involved in speech (Fazio et al., '73; Ojemann, '76; Bell, '68; Riklan and Levita, '69). Much of the involvement is with purely motor aspects of language such as voice volume, rate of speaking, and articylation t Riklan and Levita, '69). Whether the parts of VL involved with the motor aspects of language a r e also involved with nonspeech oral motor activities t,Mateer, '78) is not yet known. One of the requisite mechanisms for the control for speech, t h a t of controlling respiration, may be located in VL tOjemann, '76). Alterations in VL do not preclude changes in other parts of the brain that support the same function. Changes in the termination of the pyramidal tract neurons may also be a necessary respiratory substrate for speech production (Phillips and Porter, '77). In addition to these motor activities, VL in humans appears to be involved in more complex cognitive tasks in a n asymmetric fashion. Lesions in the right VL increase errors in visual perceptual performance leg., face matching), whereas lesions in the left VL impair verbally mediated cognition tOjemann, '76; Vilkki, '78).
MATERIALS AND METHODS

A brief description of the specimens and methodology i s given in this paper; details are provided elsewhere (Armstrong, '79). The specimens included two sides of a gibbon brain of which the species, age, and sex were un-

known, and the brains from a male Hylobates lar that was presumed to have lived in the wild, from a 10-to 12-year-old male chimpanzee and a 14-year-old male gorilla that had spent most of their lives in zoos, and from three relatively young human adults, ages 19, 28, and 32. The body weights for t h e gibbon ofunknown species and two humans (referred to as Homo-s and -t) were estimated at 5.5 kg, 136.1 kg, and 49 kg, respectively. The others were measured at time of death tH. lar, 5.9; chimpanzee, 63.5 kg; gorilla, 203 kg; Homo-c, 113.6 kg). Because the specimens came from different laboratories, some variations in the size of the brain due to different preparative techniques could be expected. The use of relative or proportionate values for comparison minimized differential processing effects. Relative volumes such as the percent of the whole thalamus occupied by the nucleus and estimates of the total number of neurons tdensity per volume per total nucleus) a r e quantitative yet proportionate and thus suitable for comparative work. Estimates of absolute volumes, neuronal density, and sizes of neuronal perikarya are also recorded. The relative frequencies of the different sizes of nerve cell perikarya were compared. The differences between the gibbon brain whose two sides were cut horizontally or sagittally and the other hominoids whose brains were all sectioned coronally were compared only if both sides of the gibbon brain resembled each other. Also, effects from sectioning or shrinkage should be evident in both nuclear segments of VL (designated VLo and VLcm, as described later). A finding in one, but not both, nuclei suggests a biological difference. VL and its subdivisions were identified according to the appearance and arrangement of neurons. Outlines of VL were traced through serial sections. Nuclear volumes were determined by summing the measured areas, multiplying them by the tissue thickness and distance between them, and dividing by the magnification (Bauchot, '63). Estimates ofneuronal density were made from counting nucleoli. Within specimen comparisons of neuronal densities and perikaryal sizes used Student's two-tailed t test. Allometric analyses were done by the least squares method. Step-wise regression followed the SPSS program and was used to determine which variables best predicted the volume of VL. Lack of number of specimens precluded use of all t h e variables te.g., volume of motor cortex and dentate nucleus). Widely varied nomenclature describes the lateral tier of nuclei in the dorsal thalamus.

HOMINOID VENTROLATERAL COMPLEX

407

The names for the populations of nerve cells, nuclei, in this work and other papers (Arms t r o n g , '76, '79a), are based on t h e n e u roanatomical studies of W a l k e r ('38) a n d Olszewski ('52). Observations of the macaque monkey iM. rnulutta and to a lesser extent t h e chimpanzee tP. troglodytes determined t h e primate paradigm in this nomenclature. Most researchers using experimental animals recognize three divisions (pars oralis, medialis, and caudalis) of the ventrolateral nucleus. An a l t e r n a t i v e terminology i s derived primarily from the work of Hassler ('59) and Van Buren and Borke ('72). The nomenclature and division come from studies on humans and a r e important in the clinical literature. The same general region of the lateral thalamus is divided into nuclei ventro-oralis and dorsooralis. A correspondence between t h e two t e r minologies h a s yet to be worked out. The heterogeneous cytoarchitecture and poorly defined borders produce disagreement. P a r t of the difficulty has been a lack of evolutionary perspective of the differences. The nuclear labels, even though they sound topographic, should not be considered topographically accurate for any one species. The patterns exemplified i n the Nissl-stained sections of the present study appeared to resemble the descriptions by Hassler ('59)and Van Buren and Borke ('72).In all the hominoids, however, I could identify a region in the lateral thalamus between the ventroanterior nucleus and the ventrobasal complex or the lateral posterior nucleus. Following I called this the nomenclature of Walker ('38), region the ventrolateral tVL) complex. Two groups of nuclei were consistently observed in the VL region of the hominoids of this study. One population of neurons was found in t h e ventrolateral segment of VL. The neuronal architecture resembled that of ventro-oralis exand Van Buren and ternus of Hassler ('59) Borke ('72). Because of the strong cytoarchitectural agreement of the ventrolateral segment ofVL with ventro-oralis externus, I labelled the region ventrolaternl oralis t VLoj. The ventrolateral oralis discussed here is probably equivalent to the ventroventralis of Krieg ('48) and possibly to part of the ventrolateral medialis of Carpenter ( ' 7 6 ) . I combined the remainder of VL and labelled it V L caudalis and rnedialis tVLcm).
RESULTS

cleus tVA) and posteriorly by the ventrobasal complex (VB) and lateral-posterior nucleus (LP). The external and internal medullary laminae are located laterally and medially (Fig. 1-3). The border between VA and VL was difficult to delineate, particularly in coronal sections. The more frequent occurrence of fusiform cells in VL (Van Buren and Borke, '72) was t h e best criterion for separating these two nuclei in the great ape and human specimens. The neuronal morphology of t h e gibbons was less differentiated. A lighter intensity of staining in VL was the major criterion for separating VA from VL in the gibbons. A difference in staining between VA and VI, was not noticeable in the other hominoids, but had been noted by others in the gibbon (Kanagasuntheram and Wong, '68). The higher density of nerve cells in VL than in VA aided in the separation iFig. 3 ) ,but the variability within each nucleus was high. No significant differences in neuronal density were observed between VA and the neighboring part of VL, VLcm, in any of these specimens where neuronal densities were measured [saggittal and horizontal sections of the two sides of the gibbon brain (gibbon -sand -h),t = 0.25 and 0.52, respectively; gorilla, t = 1.6; human, t = 0.251. The posterior border with VB was established by the presence of very large neurons in VB. The border with L P was defined by the larger neurons and lower neuronal density of VL. The differences in neuronal density were not statistically significant (in gibbons-s and -h, t = 1.07 and 0.83, respectively, gorilla, t = 1.4; and human, t = 0.3). The two components of VL, which were studied separately, were delineated on the basis of the arrangement and staining characteristics
Ahhrwintions

The ventrolateral complex tVL) is located in the lateral portion of the dorsal thalamus. VL is bounded anteriorly by the ventroanterior nu-

CC - corpus callosum CM - centromedianum nucleus ILA - interlaminary nuclei LD - lateral dorsal nucleus LGB - lateral yeniculate body LP - lateral posterior nucleus MD - medial dorsal nucleus MGH - medial geniculate body MID - midline nuclei PC - paracentral nucleus R - reticular nucleus VA - ventroanterior nucleus VB - ventrohasal complex VLc - ventrolateral nucleus, pars caudalis VLm - \entrolateral nucleus, pars medialis VLo - ventrolateral nucleus, pars oralis

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ESTE ARMSTRONG

Fig. 1. Coronal section through the thalamic ventrolateral complex ofthe gorilla. Nissl stain. Fig. 2. Coronal section through the chimpanzees ventrolateral complex. Nissl stain.

HOMINOID VENTKOLATEKAL COMPLEX

409

Fig. 3 . Horizontal section through gibbon thalamus. Nissl stain

of the nerve cells. In all of the hominoids, VLcm had a more regular dispersion of neurons than did VLo, whose neurons were clumped by coursing fibers iFig. 1 and 2 ) ; the arrangement was not correlated with neuronal density. The human specimen was the only hominoid with VLo less densely packed than VLcm (Table 1). This intraspecimen difference was statistically 0.001, t = 30). Nerve cells in significant ip VLcm were more irregular than those of VLo in their take-up of Nissl stain. The neuronal perikarya were slightly smaller in human VLo than VLcm, but slightly larger in the other hominoids (Table 2 ) . The differences were not significant in humans, gorilla, or chimpanzee ( t = 1.36,t = 1.36, and t = 0.25, respectively),but were significant in gibbons (t = 5.36, p < 0.01). The volume of VL was correlated with different factors. A step-wise regression determined that in hominoids VL volume was best predicted by brain weight (RL = 0.99475). The addition of neuronal density to brain weight decreased the residuals further (R' = 0.9984), and when t h e volume of t h e rest of t h e thalamus was added to the above two factors,

the predictive value became close to perfect RL = 1.00000. Body weight did not predict VL volume as well as the above factors. The independent variables will be analyzed separately. The volume of VL is larger in the larger brains (Table 3, Fig. 4). When log. VL is regressed against log. brain weight (E),the slope is 0.858 (with r = 0.99, p 0.001) and is significantly less than one ~p 0.01). A slope less than 1shows that the rest of the brain has expanded a t a greater rate than has VL. The cortex is the most likely region for greater expansion (Stephan et al., '70). The part of the cortex with which VL has reciprocal connections and, therefore, where changes are most likely to covary with VL is the motor cortex. As an initial analysis, I compared the differences I found in VL in a gibbon, chimpanzee, and human with those in cortical precentral surface (areas 4 & 6) in the same species (Glezer, '68). Since there is a wide range of individual variation in regions of the brain (e.g., Towe, '73; Armstrong, '801, these figures must be considered tentative. When the total precentral region is regressed against the total

VLcm
~ ~~

~~

VLo ~ -

~
SE
19.4 10.4 11.4 16.4 90.0

~
Median
228.3 159.5 97.1 125 3 43.3

Number

of

Specimen
52.3 46.4 29.4 48.9 25.9 9.9 8.0 6.1 7.4 3.5 149.3 127.5 83.9 98.0 68.5 10 11 11 6 17 212.9 160.8 99.5 125.3 46.2 64.4 32.8 37.7 40.2 25.0

fields

Mean # of neurons per 0 0 1 mm

bD

Sh
Median

Number of fields

Mean # of neuroni per 0 0 1 mm

SD

Hylo. sp:s Hylo. sp.-h Gorilla g. Pan t. Homo b:ci

28 34 23 44 56

149.2 140.5 88.3 104.9 66.2

Key to ;ihbreviatiuns Indicating how bpecimens were iectloned L., a q t t a l l y . h. h o r ~ . m n t ~ ~ lc. l ytran.vei-hely , mwol-ondliyi iThih specimen used for cell count only see Armstrong. '791 The other two hunlan speclmena (Homo s-h a n d -tl were used lor nuclear volume m e a s u r e m e n t

c ? ul

* n

TABLE 2. N r u ronn 1 Volume.

VLcm
~~~

~
Median

VLo Mean neuron vol in u

~
SU

Specimen

N
bD

Mean neuron vol in u

bE

SE

Median

142

170

Hylo. sp:s Hylo. sp:h Gorilla g. Pan t. Homo S:C+

1461.6 1277.1 2311.4 2597.6 2100.6 122.7 97.9 215.5 298.0 124.9 3064.7 2579.9 2714.5 3273.8 2829.8

115 105 283

3244.3 2648.7 3 18:3.5 3704.9 3129.0

56 50 56 34 85

2124.9 230s. 1 2716.8 3571.0 2i88.6

840.4 800.3 1605.4 2657.6 1727.3

for nuclear vulume meaburement

112.3 113.2 214.5 455.8 187.4

2024.5 2310.7 2669.5 2967.4 2326.5

Key to ahhrevintions indicating how ipecimcns were sectioned s, sagittally; h. honzontally, c, tran*\crsely icol-onallyl -./ , 1 h i s specimen u s r d for cell count only lSee Armstrong. '791 T h e o t h e r t w o h u m a n 5pecimens ~ H o r n o S-s a n d - t Jwere used

TABLE 9. Volurnrs of V L und

its

nuclei.
~

Nucleus volume In mm
~~~ ~~

.-

-?r

of total thalamus

Estimated _ _numher of neurons

~

Specimen

VL
VLcm
VLO

___
740,000 739,000 1,940,000 2,064,000 2,306,000;
i~

VL 12.1

VLcm

VLO

VL

VLcm
GY9,00U 580,000 1,630,000 1,714,000 2,864,000

VLO
101,000 159,000 310,000 350,000 442,000

6.Y 7.5 10.8 Y 1.2

Hylo. sp.-h Hylo. sp.-s Hylo. lar-t Gorilla g. Pan t. Homo s.-s Homo s.-t
45.5 38.9 48.9 184.6 163.4 547.7 317.5

51.8 45.4 59.7 215.6 191.3 644.9 411.6

27.9
97.2 94.1

1Y.X 12.4 10.4 13.5 13.1 15.45 12.2

10.6 8.5 11.5 11.2 13.0 9.4 1.7 2.0 1.9 2.0 1.9 2.3 2.8

j r l

Key to abbreviations indicating how >pecimenb were hectioned a, ,agitt:rlly. h. horizontally; t. transversel?. I h e estimated n u m h e r of neurons Sor human. ii a n average of t h e fikwres for t h e t h r e e h u m a n specimen&,mciudlng Homo

c which , was w e d tor cell count only ( S e e Armstrong, ' ~ Y I

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ESTIS ARMSTRONG

Fig. 4. Volume of ventrolateml complex relative to brain weight

VL complex, the slope produced is 1.008, with r = 0.989, t, = 6.76, p c 0.05 iFig. 5). If the surface area of t h e cortex changed among the species at the same rate as the thalamic volume, a slope a s derived from least-squares method would be about 0.67 (Huxley, '72; Jerison, '73). The slope found here differs significantly from 0, but while it is strongly suggestive that the slope is higher than the 0.67 slope of equal development, the difference does not quite reach statistical significance (t, = 2.29, p = 0.1). In addition to its reciprocal connections with the motor cortex, VL receives fibers from the dentate nucleus of the cerebellum. The dentate nucleus has been studied volumetrically in humans, a gorilla, and a chimpanzee (Daron, '60; Fix, '67; Hopker, '51). Ifthe logarithm of VL volume i s a n a l y z e d as a function of t h e logarithm of the volume of the dentate nucleus, isometry would be represented by I. The slope actually produced, 1.41, significantly differs . 0.05), but not from 1 from 0 (T, = 4.98, p < (t, = 1.44, .2 > p > .1). VL has increased at the same or a slightly greater rate t h a n has the dentate nucleus. The rate of divergence in the volume of VL is also similar to that of the rest of the thalamus. VL occupies about 13%in all hominoid thalami (Table 3).An allometric analysis of the volumes by the least squares method produces a slope

close to the isometric value of 1 iFig. 6). The slopes with and without human values are close (1.055 and 1.039, respectively, both r = 0.99). The two parts of VL have different rates of change. The growth coefficient is slightly higher for VLo than for VLcm (Fig. 6, Table 3). The difference between the two components is the result of human values in VLo (slope 1.12 with human values and 1.03 without; r = 0.995 both). More specimens must be analyzed before a n evolutionary effect can be separated from one due to individual variation. The volumes of VL were correlated with body weight ir = 0.85, p 0.05),(Fig.7 ) .The correlation could be strengthened by restricting the correlation to apes ( r = 0.975, p < . 0.01) or to gibbons and humans ( r = 0.993, p <-. 0.001). The line derived from all apes predicts a smaller human VL volume than was found. The significance ofthis must await more specimens. Use of representative body weights decreased the correlation to nonsignificant levels. The density of nerve cells in VL was less in the larger brains (Table I).The two parts of VL, however, varied i n t h e r a t e of decrease in neuronal density, VLo having a greater deceleration than VLcm (slopes-0.486 r = 0.98; and -0.33 r = 0.94, respectively). The differences in the slopes describing the decrease in density strongly suggest t h a t different populations were being samples (0.1 > p > 0.05). The

HOMINOID VENTHOLAI'EKAL COMPLEX

413

Ly X

c
0

u m

-,

1.5

c
I -

2
Ly

Y
Ly

c
0

#a
0

*
1.0

1.5 LOG.
YL

2.0

2.5

VOLUME

Fig. 5, Relationship between area of precentral cortex (areas4 and 6 )and ventrolateral volume. Bars represent

SD of VL volume. G represents hypothetical position for gorilla. Slope is 1.008.

human values in VLo produced the largest alteration in the slope (slope of VLo with human values included = - 0.486 and without human values =-0.338, 0.1 > p > 0.05). The estimated numbers of neurons are listed i n Table 3. The great apes have about twoand-a-half times as many motor neurons as do the gibbons. The human values are estimated a t one-and-a-half times as many as the great apes. For gibbons, chimpanzees, and humans the number of pyramidal tract neurons (Towe, '73) correlates strongly with the number of VL neurons ir = 0.995, p < 0.01). When t h e logarithm of t h e number of pyramidal tract neurons is regressed against the logarithm of t h e number of VL neurons, the slope is 0.85. The larger rate of increase in numbers of VL neurons is probably because both integrative and relay neurons were counted, whereas the estimates of pyramidal tract axons involve only relay neurons. The relative sizes of the neuronal perikarya a r e similar in all three specimens (Table2 , Fig. 8 and 9). There i s a slightly greater separation of the taxonomic groups in VLo than in VLcm.

DISCUSSION

Comparison of the thalamic specific motor complex among extant hominoids shows a rate of divergence in tissue volume and number of neurons that is less than that for the whole brain, but similar to that of the rest of the thalamus (Fig. 4 and 6). The thalamus is one part of the diencephalon, and the lower rate of VL and thalamic divergence is concordant with the relatively slow expansion of the diencephalon among primates iStephan et al., '70). The data also suggest, however, t h a t during hominid evolution there was a small, but differential expansion in VL. Since the alterations in VL's volume are isometric with the rest of thalamus, a first inclination is to think that the changes, being proportional, represent a stabilization or a nonderived condition. Nevertheless, a more conservative status was recognized in all the thalamic sensory nuclei, whose volumes varied less t h a n those in the rest of the thalamus (Armstrong, '79). Furthermore, the visual and auditory thalamic nuclei have a similar number of neurons in great apes and humans, but VL h a s one-and-a-half times as

414

ESTE ARMSTRONG

Fig. 6. Volume of ventrolateral complex a n d nuclei as a function of the rest of the th;il;rmus. Line 1. total ventrolateral complex; line 2 , VLcm; line :3, VLo.

many neurons in humans as is found in great apes. The differences were less intense than those found in t h e thalamic limbic and association regions (Armstrong, '80). Both the degree of volumetric change and number of neurons argue for a n active selection in the motor nuclei during hominid evolution. Similar volumetric changes have been found among the different systems in the cortex. Human and chimpanzee motor cortices appear volumetrically more divergent than do the visual cortices (Shariff, '53).It is unclear whether the association and motor cortices have a similar or different degree of divergence among extant hominoids (Holloway, '68; Passingham a n d E t t i n g e r , '74; Shariff, '53). Among hominoids the motor cortex has expanded at a faster rate than VL (Fig. 5). The bigger growth of the motor cortex may represent a structural

corticalization of motor function Noback and Moskowitz, '63). Whether. the corticalization would be better considered as a neural substrate for new behaviors (Jerison, '731 or for the refinement and control of old ones (Noback and Moskowitz, '63) is presently unknown. A major output of t h e motor cortex, the pyramidal tract (PI'),has been measured in several hominoids (Towe, '73). The changes in the numbers of neurons in VL and PT are highly correlated, but the growth coefficient shows a larger relative increase in VL. Although some small axons may have been overlooked in the counts of P I ' axons (Towe, '73), there is no evidence that humans have more small axons t h a n do apes in this long distance hard-wired tract. Since the numbers of axons in F T have increased at a slower rate than the number of VL neurons, but the motor cortex

HOMINOID VENTROLATERAL COMPLEX

415

r
10

- -

HOMlNOlOS ~'005 APES p.001 AN0 HUMANS

_ _ _ _ _ _ 6lBBONS
p 0.01
100

RODV

WT.. K q

Fig. 7. Volume of ventrolateral complex relative to body weight.

has increased a t a greater rate than has VL, the structural corticalization may likely be the result of a n increase in integrative nerve cells or processes or both. The motor cortex is composed of overlapping subareas that project to specific targets via PT (Phillipsand Porter, ' 7 7 ) ,and a n increase in tissue not directly tied to PT would permit increased combinations and recombinations of motor programs. Such variation in motor programs may underlie skill and dexterity. Controlled tnovement requires continual adjustments. VL nerve cells send signals to the motor cortex that have been generated by external and internal feedback networks (Phillips and Porter, '77). The cerebellum is a major source of such feedback. The cerebellum has expanded among primates at a rate second only to the neocortex and certainly a t a greater rate than that of the diencephalon (Stephan et al., '70). Nevertheless, the major relay nucleus of t h e cerebellum, the dentate nucleus, appears to have increased in volume only as much as VL or

perhaps slightly less. That finding is not a discrepancy, because t h e dentate nucleus is a relay center, whereas VL is a n integrative one. The expansion in VL may be a n example of subcorticalization (Noback & Moskowitz, '63) and suggests that for a given function, integrative centers are likely to change more than relay centers. The above analyses do not account for the most clearly observed differences in motor behavior among extant apes, that of locomotion. The nucleus VLo may be a region to explore in this regard. The hominoid VLo occupies the topographic region that in cats is involved with limb muscles and postural adjustments (Massion, '76-'77; Smith e t al., '78). More pertinently, shifts in volume and sizes of neuronal perikarya among these specimens suggest species-specific differences in VLo, but not in VLcm. The human VLo manifests a bigger relative increase in volume accompanied by a slower addition of nerve cells than does VLcm (Fig. 6, Table 3). Changes of this nature might

416

ESTE ARMSTRONG

Human
37 5

c.

Gorilla

Neuron Volumes in mlcra'

"LO

Fig. 8. Comparison of the relative frequencies of nerve cell perikaryal sizes in VLcm

HOMINOID VENTROLATEKAL COMPLEX

417

247

Human

W W
O---O

v- I

Gorilla
Gibbon

800

I600

3200

4800

b400

8000" ,8000

Neuron Volumes in m i craj VLcrn

Fig. 9. Comparison of the relative frequencies of nerve cell perikaryal sizes in VLo.

418

ESTE ARMSTRONG Evarts, E.V. ( 1971) Activity of thalamic and cortical neurons in relation to learned movement In the monkey. Int. J . Neurol., 8:321-326. Fazio, C . , J. Sacco, and 0. Bugiani (1973) The thalamic hemorrhage. Europ. Neurol., 9:30-43. Fix, J.D. 11967) Unpublished dissertation. Figures in. 0 . Larsell and J . J a n s e n 1972. The Human Cerebellum, Cerebellar Connections and Cerebellar Cortex, Vol. 111. University of Minnesota Press, Minnesota. Frahm, H., R. Hassler, and S. Graisarn (1979)Comparative volumetric studies on pallidurn in insectivores and primates. Evolutionary aspects. Appl. Neurophysiol., 42: 9 1 - 94. Clezer, 1.1. i 1968) Area relationships in the precentral region in a comparative-anatomical series of primates. In: The Human Brain in Fihures and Tahles. S.M. Blinkov and 1.1. Glezer e d s . , translated by B. Haigh, Plenum Press, New York, pp. 17gF-181, :38:3. Harmon, P.J., and M.B. Carpenter i 1950) Volumetric comparisons of the basal ganglia of various primates, including man. J. Comp. Neurol Hasster, R. (1972) Hexapartition (if impulses as a primary role of the thalamus. In: Corticothalamic Projections and Sensorimotor Activities. T. FriWesi, E. Itinvik and M.D. Yahr, eds. Raven Press, New York, pp. 551-577. Hassler, R. i 1959)Anatomy ofthe thalamus. In. lntroduction to Stereotaxis with a n Atlas ofthe Human Brain. G. Schaltenbrand and D. Bailey, eds. Grune and Stratton, New York, pp. 230-290. Holloway, R.L., J r . ( 1975)Therole ol'Human Social Behavior in the Evolution ofthe Brain. 43rd James Arthur Lecture, 1973, New York, American Museum of Natural History. Holloway, K.L., J r . (1970)Neural parameters, hunting, and the evolution of the human brain. In: The Primate Brain. C.K. Noback and W. Montama. ', , tds. ADDktOn-CentUrVCrofts, N.Y., pp. 299-310. Holloway, K.L.,Jr. (1968)Theevolutionofthe primate brain: Some aspects of q u a n t i t a t i v e relations. Brain Res.,
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signal a different organization of neurons. On the other hand, fibers passing through VLo (Fig. 1 and 2 ) leaving from and terminating in other parts of the brain could, via a n increase in fiber number and/or size, create such a condition without active selection working in VLo. A relative decrease of larger neurons in the gibbon VLo, but not VLcm (Fig. 8 and 9), also supports a separation of locomotory groups in this nucleus. Further comparative studies are warranted.
ACKNOWLEDGMENTS

I thank C.R. Noback, H. Stephan, N. Moskowitz, W.I. Welker, The Max-Planck-Institut fur Hirnforschung, Frankfurt, and the Yakovlev Collection for the opportunity to study some of their primate brains; R. Holloway, C.R. Noback, and W.I. Welker for their technical advice; T. Hill for the excellent photographs of the chimpanzee brain; and S. Schmidt and L. Steiner for the typing of this manuscript. This Grant work was supported in part by NSF SOC. 74 20149 0113.24 019.00 and NINDS grants NB-3249 and NB-06225 from the USPHS.
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