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The Evolution of the Cerebellum in Anthropoid Primates
4.10 The Evolution of the Cerebellum in Anthropoid Primates J K Rilling, Emory University, Atlanta, GA, USA ª 2007 Elsevier Inc. All rights reserved.
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4.10.1 Anatomy of the Cerebellum 4.10.2 Cerebellar Connectivity and Function 4.10.2.1 The Flocculonodular Lobe 4.10.2.2 The Vermis 4.10.2.3 The Intermediate Hemispheres 4.10.2.4 The Lateral Hemispheres 4.10.3 Comparative Cerebellar Anatomy 4.10.4 The Ape Cerebellum Is Not an Allometrically Enlarged Monkey Cerebellum 4.10.5 Is the Human Cerebellum an Allometrically Enlarged Ape Cerebellum? 4.10.6 Conclusion
Glossary afferents cerebellar vermis dentate nucleus efferents hominid
hominoid neocortex
premotor cortex
Incoming connections. The narrow, middle zone between the two hemispheres of the cerebellum. The most lateral and largest of the cerebellar deep nuclei. Outgoing connections. Any living or extinct habitually bipedal hominoid, including members of the genus Homo and Australopithecus. Any living or extinct ape or human. A uniquely mammalian type of cerebral cortex involved in perception, thought, and reasoning, and consisting of six cytoarchitectonic layers. An area of cortex anterior to motor cortex, corresponding to Brodmann’s area 6, that is involved in motor planning.
4.10.1 Anatomy of the Cerebellum Much like the cerebrum, the cerebellum (Figure 1) consists of cortical gray matter overlying white matter within which lie subcortical nuclei, known as the cerebellar deep nuclei (Figure 2). However, in contrast to the six-layered cerebral cortex (see The Development and Evolutionary Expansion of the Cerebral Cortex in Primates), the cerebellar cortex has only three layers. Within it, Purkinje cells are responsible for integrating excitatory and inhibitory inputs and providing output to the cerebellar deep nuclei, which in turn send projections out of the cerebellum (Figure 3). Thus, most cerebellar efferents originate in the deep cerebellar nuclei. In contrast to the cerebral cortex, cerebellar cortex is
Cerebellum Figure 1 Location of cerebellum in lateral view of human brain. Reproduced from Memory Loss and the Brain. Copyright ª Ann L. Myers/Memory Loss and the Brain.
cytoarchitectonically homogenous and intercortical connectivity is minimal. The cerebellum is composed of four different anatomical regions: the flocculonodular lobe (or vestibulocerebellum), the vermis, the intermediate hemispheres, and the lateral hemispheres. The flocculonodular lobe is on the ventral surface of the cerebellum, abutting the brainstem. The vermis occupies the midline of the cerebellum and is separated from the cerebellar hemispheres by longitudinal furrows on either side. The intermediate portion of the hemispheres is just lateral to the vermis and just medial to the lateral portion of the hemispheres (Figure 3).
4.10.2 Cerebellar Connectivity and Function 4.10.2.1 The Flocculonodular Lobe
The flocculonodular lobe receives input from the primary vestibular afferents and projects back to the vestibular nuclei. This portion of the cerebellum
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Paravermis + Hemisphere
Vermis
Paravermis + Hemisphere
Human Cortical gray matter
White matter
Subcortical nucleus (dentate)
Figure 2 Cerebellar anatomy. Reproduced in full from Altman, J. and Bayer, S. A. 1997. Development of the Cerebellar System in Relation to Its Evolution, Structure and Functions. CRC Press.
governs eye movements and body equilibrium during stance and gait.
found in the cortex of the vermis and intermediate hemispheres (see Figure 3).
4.10.2.2 The Vermis
4.10.2.4 The Lateral Hemispheres
The primary sources of input to the cerebellar cortex of the vermis are the spinocerebellar tracts, which carry somatosensory information from axial and proximal body parts. This information is relayed from the cortex of the vermis to the most medial of the deep cerebellar nuclei: the fastigial nucleus. All of the deep cerebellar nuclei have both ascending (to midbrain, thalamus, and cortex) and descending (to brainstem and spinal cord) efferents. Fastigial efferents are predominantly descending, projecting to brainstem nuclei that control proximal muscles of the body and limbs (see Figure 3).
In contrast to the vermis and intermediate hemispheres, the lateral hemispheres receive little somatosensory input from the periphery. Instead, the main source of afferents to the cortex of the lateral hemispheres is the cerebral cortex. In macaques, these corticopontocerebellar fibers originate in motor, premotor, posterior parietal, cingulate, and prefrontal cortex and project to the lateral cerebellar hemispheres by way of the pontine gray matter (Brodal, 1978; Glickstein et al., 1985; Schmahmann and Pandya, 1997). Output from the lateral hemispheres is directed to the most lateral of the deep cerebellar nuclei, the dentate nucleus. Most of the dentate’s efferents ascend to either the parvicellular portion of the red nucleus or the ventrolateral thalamus, which in turn projects to motor, premotor, prefrontal, and posterior parietal cortices (Kelly and Strick, 2003), thereby forming a loop that links lateral cerebellar and cerebral cortex. Based on tract-tracing studies, Strick and colleagues have introduced the notion of closed cerebellar loops in which inputs from cerebral cortical areas are spatially segregated in both cerebellar cortex and the dentate nucleus. For example, projections from motor (e.g., BA4) and nonmotor (e.g., BA46) cortex
4.10.2.3 The Intermediate Hemispheres
The spinocerebellar tracts are also the primary source of input to the cortex of the intermediate hemispheres. The intermediate hemispheres relay information to the interposed cerebellar nuclei (globose and emboliform), which send both ascending and descending efferents to nuclei involved in coordination of distal limb muscles. The ascending projections reach the magnocellular portion of the red nucleus, which gives rise to the rubrospinal tract. Two somatotopic maps of the body are
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Cerebral cortex
Motor
Parietal
Premotor Prefrontal
Red nucleus
Ventrolateral thalamus
Pons M
Lateral
Intermediate
P
Vermis
Cerebellum
F
I
D
Brainstem and spinal cord Figure 3 Schematic of cerebrocerebellar system showing prominent cerebellar afferents (solid lines) and efferents (dashed lines). M, magnocellular portion of red nucleus; P, parvicellular portion of red nucleus; F, fastigial nucleus; I, interposed nucleus; D, dentate nucleus.
have distinct, nonoverlapping representations in the cerebellum, both in the cortex (where they enter) and in the dentate nucleus (where they exit). Specifically, motor cortex projects to lobules IV–VI and nonmotor area 46 projects to crus II. In the dentate, the motor domain is dorsal and the nonmotor domain is ventral (Dum and Strick, 2003). The existence of these closed cerebellar loops is consistent with the suggestion that corticocortical projections are absent within the cerebellar cortex (Braitenberg et al., 1997), in stark contrast to the cerebral cortex (see Figure 3). Consistent with these anatomical data, evidence from neurological patients and functional neuroimaging experiments suggests that the lateral cerebellum of humans has both motor and nonmotor functions. Motor-related functions of the cerebellum include fine motor coordination, motor planning, and motor learning (Ghez and Thach, 2000). The cerebellum has also been implicated in a bewildering array of nonmotor functions, including sensory discrimination,
spatial cognition, visuospatial problem solving, attention and attention switching, procedural learning, verbal working memory, verb generation, verbal fluency, lexical retrieval, syntax, semantic and phonological word retrieval, syntactic processing, and abstract reasoning (Dow, 1988; Leiner et al., 1989; Courchesne et al., 1994; Allen et al., 1997; Desmond and Fiez, 1998; Schmahmann, 1998; Ghez and Thach, 2000; Rapoport et al., 2000; Marien et al., 2001). It seems unlikely that all of these processes can be subsumed under a single overarching function that the cerebellum performs. More likely, as originally suggested by Snider (1950), the cerebellum may be ‘‘the great modulator of neurologic function.’’ That is, it improves the skilled performance of any cerebral area to which it is linked by two-way neural connections (Leiner et al., 1989). Connections with motor areas would increase the speed and skill of movement and connections with cognitive areas would improve the speed and skill of cognition.
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4.10.3 Comparative Cerebellar Anatomy Evidence with respect to the evolution of the primate cerebellum (see Primate Brain Evolution in Phylogenetic Context) comes mainly from cross-species, comparative studies of living primate brains. Some of these studies are based on postmortem specimens (Stephan et al., 1981), whereas others are based on MRI scans obtained from living primates (Rilling and Insel, 1999). Each data set has both advantages and disadvantages. The primary advantage of the postmortem sample is that it permits analysis of microscopic cytoarchitecture, which cannot be observed in MRI scans. On the other hand, the in vivo MRI scans (Figure 4) were obtained from healthy (not old or sick) animals and do not suffer from shrinkage artifacts caused by the postmortem tissue fixation process. Using these data sets, various authors have compared both the size and the histology of the cerebellum and its component structures across the primate order. Below is a summary of what these comparisons have revealed. To begin with, Figure 5a illustrates variation in absolute cerebellum volume across a sample of 11 anthropoid primate species. At least some of this variation is likely attributable to variation in body weight, since most structures are larger in larger animals. Furthermore, the cerebellum is in close contact with the body surface, receiving
Figure 4 MRIs of primate cerebella. Coronal MRI through the cerebellum of: a, rhesus macaque; b, gibbon; c, chimpanzee; and d, human. Reproduced from Rilling, J. K. and Insel, T. R. 1998. Evolution of the cerebellum in primates: Differences in relative volume among monkeys, apes and humans. Brain Behav. Evol. 52, 308–314, with permission from Karger.
somatosensory information from the periphery and modulating descending motor systems that control movement, so that we might expect cerebellar size to track body size. As can be seen in Figure 5a in which species are listed in ascending order of body weight, there is indeed a relationship between body weight and cerebellar volume. In fact, for the sample of 44 anthropoid primates in the Yerkes MRI data set, (log) body weight explained 87% of the variance in (log) cerebellar size (r¼0.93, p<0.001; Figure 5b). Figure 5a demonstrates that the human cerebellum is larger than expected for a primate of our body weight. This is confirmed by Figure 5b in which cerebellar volume is plotted against body weight and a least-squares regression line is fit through the data. Much of the unexplained variance can be attributed to the human data points, which lie well above the prediction based on the regression line. Is the cerebellum unusual in this respect or are other human brain structures also disproportionately large relative to body weight? In fact, the cerebellum is second only to the neocortex, albeit a distant second, in terms of its size relative to body size (Stephan et al., 1988). The fact that the neocortex and cerebellum are the two structures that enlarged most relative to body size in humans, coupled with the existence of extensive connections between the two, suggests the possibility that the neocortex and cerebellum have evolved in tandem as a coordinated system (Barton and Harvey, 2000). Using the method of independent contrasts to eliminate the effect of common inheritance, Barton and Harvey showed that this is indeed the case for primates. Cerebellar contrasts are significantly correlated with neocortex contrasts, and this relationship is stronger than that of cerebellar contrasts and other major brain divisions, such as the medulla, mesencephalon, and diencephalon. In a subsequent analysis, Whiting and Barton (2003) demonstrated correlated evolution in other components of this cerebrocerebellar system among primates. For example, after partialing out evolutionary change in the size of the rest of the brain, they found that evolutionary changes in the size of the pons were positively correlated with changes in the size of both neocortex and cerebellar cortex. In other words, the corticopontocerebellar system that provides input to the cerebellum appears to evolve in concert. There was no significant correlation between pons and the deep cerebellar nuclei, in accord with the lack of direct connectivity between these two structures. On the other hand, there was a strong positive correlation between relative contrasts in deep cerebellar nuclei and relative contrasts in the thalamus, to
The Evolution of the Cerebellum in Anthropoid Primates
Monkeys Apes Humans
2.0000
log cerebellum volume (cc)
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50.00
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r 2 = 0.87 Y = 0.81X + 0.31
1.5000
1.0000
0.5000 0.00
(a)
Squirrel Gibbon Rhesus Bonobo Gorilla Orang Capuchin Mangabey Baboon Chimp Human
Species
–0.5000 0.0000 0.5000 1.0000 1.5000 2.0000
log body weight (kg)
(b)
Figure 5 Comparison of cerebellum volume in anthropoid primates. a, Mean absolute cerebellum volume from MRI scans in 11 anthropoid primate species, in ascending order of body weight. Note that the gorilla body weight is low for the MRI data set because it is based on one small female and one subadult male. Error bars are 1 SE. b, Regression of log cerebellum volume against log body weight, with least squares regression line fit through the entire sample.
which the nuclei send much of their output en route to the neocortex (see Figure 3).
Monkeys Apes Humans
4.10.4 The Ape Cerebellum Is Not an Allometrically Enlarged Monkey Cerebellum Despite this tendency for the cerebrocerebellar system to evolve as a coordinated whole, it is clear that the relationship between the two structures was altered with the evolution of hominoids (Rilling and Insel, 1998; Semendeferi and Damasio, 2000). When cerebellum volume is regressed on cerebral cortex volume for anthropoid primates, there is a clear grade shift between apes and monkeys, indicating that apes have larger cerebella for any given cerebrocortical volume (Figure 6), and this difference is concentrated in the cerebellar hemispheres as opposed to the vermis (MacLeod et al., 2003). Important differences between apes and monkeys are also found in cerebellar components. Matano and Hirasaki (1997) regressed the volume of the dentate nucleus on the volume of the medulla oblongata for a sample of 26 anthropoid primate species (from Stephan et al., 1981) and found that apes have relatively larger dentate nuclei than monkeys. This was equally true of greater and lesser apes; however, there was an interesting difference between the two in the relative size of the interposed nucleus, which
log cerebellar volume (cc)
2.0000
Apes: Y = 1.01X – 0.56 1.5000
1.0000
Monkeys: Y = 1.07X – 0.81 0.5000
1.0000
1.5000
2.0000
2.5000
3.0000
log cortical volume (cc) Figure 6 Comparison of cerebellum volume relative to cerebral cortical volume in anthropoid primates. Regression of log cerebellum volume on log cerebral cortical volume, with separate least-squares regression lines fit through the monkey and ape data. Human data points are plotted but not included in either regression. Data are from Rilling and Insel (1998, 1999).
was found to be markedly larger in lesser apes. This raises the possibility that Hylobatidae and Pongidae independently evolved to a similar grade of overall cerebellar development.
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Given the anatomical connections between the cortex of the lateral cerebellar hemisphere and the dentate nuclei, the larger relative size of the ape dentate suggests that the expansion of the cerebellar hemispheres in apes may be concentrated in the lateral, rather than intermediate portion of the hemisphere. Detailed comparisons of the dentate nuclei reveal further differences between monkey and hominoid cerebella. On the basis of morphological, histological, embryological, histochemical, and pathological evidence, the dentate nucleus is thought to consist of two parts: an older dorsomedial and newer ventrolateral part (Dow, 1988) (Figure 7). Among anthropoid primates, the ventrolateral part is unique to humans and apes (Leiner et al., 1991). Based on neuropsychological and neurophysiological evidence, Leiner et al. (1991) argue that the ventrolateral dentate sends output to nonmotor regions of the frontal lobe by way of the ventrolateral thalamus. This hypothesis will require further testing, perhaps with noninvasive in vivo methods such as diffusion tensor imaging (DTI) that allow visualization of white matter fiber tracts. However, if the hypothesis proves accurate, then the emergence of the ventrolateral dentate in hominoids could reflect a qualitative shift toward increased cerebellar involvement with cognition by virtue of connections with nonmotor frontal lobe regions.
What might be the functional significance of the elaborated cerebellum in hominoids? As suggested above, the enlarged ape cerebellum might improve the functioning of all cortical regions with which it is connected. One cortical target of lateral cerebellar efferents is motor and premotor cortex, and it has been argued that apes have a greater complexity of movement than monkeys (Povinelli and Cant, 1995; MacLeod et al., 2003). Also compatible with this augmentation of function in motor and premotor cortex is Ott’s observation that, in contrast to apes and humans, baboons apparently lack presyntactical motor planning, the ability to modify current movements based on awareness of movements to follow (Ott et al., 1994). Other skills that apes excel at relative to monkeys are also likely to be dependent on the motor and premotor cortex. For example, when reaching for an object, apes and humans exhibit more complex preshaping of their hand compared with monkeys (Christel, 1993; Christel et al., 1998). In addition to these differences in motor-related functions, apes and monkeys also possess numerous cognitive differences. It is conceivable that cerebellar augmentation of prefrontal function could be involved in apes’ putative capacity for self-awareness (Gallup, 1970), components of theory of mind (Tomasello et al., 2003), and capacity for symbolic thought (Tomasello and Call, 1997). Each of these abilities is known to depend upon prefrontal cortex in humans (Deacon, 1997; Frith and Frith, 1999; Gusnard et al., 2001; Gallagher and Frith, 2003).
4.10.5 Is the Human Cerebellum an Allometrically Enlarged Ape Cerebellum?
Figure 7 Dorsal and ventral aspects of the cerebellar dentate nucleus. Coronal section through dentate nucleus, showing dorsal and ventral halves. d, dorsal; v, ventral. Reprinted from Matano, S. 2001. Brief communication: Proportions of the ventral half of the cerebellar dentate nucleus in humans and great apes. Am. J. Phys. Anthropol. 114, 163–165. Copyright ª 2001, Wiley-Liss. Reprinted with permission of Wiley-Liss, Inc., a subsidiary of John Wiley & Sons, Inc.
The human cerebellum is remarkably larger than the ape cerebellum, even after adjusting for differences in body weight (Figure 5). In fact, it is 2.8 times larger than expected for a nonhuman primate of equivalent body weight. Humans also have a larger dentate nucleus for their body size than apes (Matano and Hirasaki, 1997), and the difference is concentrated in the ventrolateral portion of the nucleus (Matano, 2001). Matano (2001) measured the area of the dorsal and ventral halves of the dentate in gorillas, chimps, and humans and calculated a ratio of ventral to dorsal areas in each species. The average human ratio (2.11) was much larger than the average ape ratio (1.64), indicating expansion of the ventral half in humans. Although there are certainly absolutely more cerebrocerebellar connections in humans compared with apes, the degree of connectivity in humans is
The Evolution of the Cerebellum in Anthropoid Primates
probably less than what would be expected for an ape brain of human size. This is because humans fall below the ape regression line of cerebellar volume against cortical volume (Figure 6). This indicates that either (1) humans have small cerebella for their cortex size or (2) humans have large cortices for their cerebellar size. In fact, the existing data support the latter possibility given that the human cerebral cortex is disproportionately large when regressed on other brain structures, and the cerebellum is not disproportionately small when regressed on other brain structures (Deacon, 1988; Rilling and Insel, 1999). This result suggests that some of the cortical regions that expanded in humans did not maintain the degree of connectivity with the cerebellum that is found in apes or that cortical expansion was concentrated in regions that do not receive many cerebellar efferents. A likely candidate is temporal cortex, which is not intimately connected with the cerebellum and known to have expanded extra-allometrically in humans (Rilling and Seligman, 2002). Prefrontal cortex, when defined cytoarchitectonically, is also disproportionately large in humans (Passingham, 1973; Deacon, 1997; Preuss, 2000). What could be the functional significance of the enlarged cerebellar hemispheres and ventrolateral dentate in humans? One possibility is accurate overhand throwing, which likely represented a strong selective pressure throughout our hunting and gathering past (Isaac, 1987; Calvin, 1993). Accurately throwing rocks and projectiles may have been crucial for hunting and scavenging prey, predator defense, and intergroup hostilities. Another possibility is that the enlarged human cerebellum supports fine motor coordination involved in the manufacture and use of tools (see Neurological Specializations for Manual Gesture and Tool Use in Humans). Humans are superior to apes in terms of manual dexterity. However, it is also clear that the cerebellum does indeed take on a cognitive role in humans, being involved in a wide range of mental operations (as discussed above). Leiner et al. (1993) have emphasized its role in language in view of neuropsychological evidence and hypothesized connections with BA44 (Broca’s area). One attractive possibility is that the human cerebellum is involved in a more global augmentation of frontal lobe function that extends to cognitive domains beyond language.
4.10.6 Conclusion 1. Compared with monkeys, apes have larger cerebellar hemispheres for their brain size. 2. The dentate nucleus, the cerebellar deep nucleus that receives input from lateral cerebellar cortex,
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is also relatively larger in apes than in monkeys and relatively larger in humans than in apes. 3. The ventrolateral portion of the dentate, which may project to nonmotor regions of frontal cortex that are involved in higher cognition, is reportedly absent in monkeys and more developed in humans than in apes. 4. Although the human cerebellum is large relative to body size, the human cerebral cortex is even larger. Consequently, we have a large cerebral cortex for our cerebellum size, and the relative degree of cerebrocerebellar connectivity is probably reduced in humans compared with apes. 5. Given evidence for cerebellar connections with both motor and higher-order association cortex, the above differences in cerebellar anatomy among monkeys, apes, and humans could support motor and cognitive specializations of the three groups.
References Allen, G., Buxton, R. B., Wong, E. C., and Courchesne, E. 1997. Attentional activation of the cerebellum independent of motor involvement. Science 275, 1940–1943. Altman, J. and Bayer, S. A. 1997. Development of the Cerebellar System in Relation to its Evolution, Structure and Functions. CRC Press. Barton, R. A. and Harvey, P. H. 2000. Mosaic evolution of brain structure in mammals. Nature 405, 1055–1058. Braitenberg, V., Heck, D., and Sultan, F. 1997. The detection and generation of sequences as a key to cerebellar function: Experiments and theory. Behav. Brain Sci. 20, 229–245. Brodal, P. 1978. The corticopontine projection in the rhesus monkey. Origin and principles of organization. Brain 101, 251–283. Calvin, W. H. 1993. The unitary hypothesis: A common neural circuitry for novel manipulations, language, plan-ahead, and throwing? In: Tools, Language and Cognition in Human Evolution (eds. K. Gibson and T. Ingold), pp. 230–250. Cambridge University Press. Christel, M. 1993. Grasping techniques and hand preferences in Hominoidea. In: Hands of Primates (eds. H. Preuschoft and D. J. Chivers), pp. 91–108. Springer. Christel, M., Kitzel, S., and Niemitz, C. 1998. How precisely do bonobos (Pan paniscus) grasp small objects? Int. J. Primatol. 19, 165–194. Courchesne, E., Townsend, J., Akshoomoff, N. A., et al. 1994. Impairment in shifting attention in autistic and cerebellar patients. Behav. Neurosci. 108, 848–865. Deacon, T. 1997. The Symbolic Species. W. W. Norton. Deacon, T. W. 1988. Human brain evolution: II. Embryology and brain allometry. In: Intelligence and Evolutionary Biology (eds. H. Jerison and I. Jerison), pp. 383–416. Springer. Desmond, J. E. and Fiez, J. A. 1998. Neuroimaging studies of the cerebellum: Language, learning and memory. Trends Cogn. Sci. 2, 355–362. Dow, R. S. 1988. Contribution of electrophysiological studies to cerebellar physiology. J. Clin. Neurophysiol. 5, 307–323. Dum, R. P. and Strick, P. L. 2003. An unfolded map of the cerebellar dentate nucleus and its projections to the cerebral cortex. J. Neurophysiol. 89, 634–639.
156 The Evolution of the Cerebellum in Anthropoid Primates Frith, C. D. and Frith, U. 1999. Interacting minds: A biological basis. Science 286, 1692–1695. Gallagher, H. L. and Frith, C. D. 2003. Functional imaging of ‘theory of mind’. Trends Cogn. Sci. 7, 77–83. Gallup, G. 1970. Chimpanzees: Self-recognition. Science 167, 86–87. Ghez, C. and Thach, W. T. 2000. The cerebellum. In: Principles of Neural Science (eds. E. R. Kandel, J. H. Schwartz, and T. M. Jessel), pp. 832–885. McGraw-Hill. Glickstein, M., May, J. G., 3rd, and Mercier, B. E. 1985. Corticopontine projection in the macaque: The distribution of labelled cortical cells after large injections of horseradish peroxidase in the pontine nuclei. J. Comp. Neurol. 235, 343–359. Gusnard, D. A., Akbudak, E., Shulman, G. L., and Raichle, M. E. 2001. Medial prefrontal cortex and self-referential mental activity: Relation to a default mode of brain function. Proc. Natl. Acad. Sci. USA 98, 4259–4264. Isaac, B. 1987. Throwing and human evolution. Afr. Archaeol. Rev. 5, 3–17. Kelly, R. M. and Strick, P. L. 2003. Cerebellar loops with motor cortex and prefrontal cortex of a nonhuman primate. J. Neurosci. 23, 8432–8444. Leiner, H. C., Leiner, A. L., and Dow, R. S. 1989. Reappraising the cerebellum: What does the hindbrain contribute to the forebrain? Behav. Neurosci. 103, 998–1008. Leiner, H. C., Leiner, A. L., and Dow, R. S. 1991. The human cerebro-cerebellar system: Its computing, cognitive, and language skills. Behav. Brain Res. 44, 113–128. Leiner, H. C., Leiner, A. L., and Dow, R. S. 1993. Cognitive and language functions of the human cerebellum. Trends Neurosci. 16, 444–447. MacLeod, C. E., Zilles, K., Schleicher, A., Rilling, J. K., and Gibson, K. R. 2003. Expansion of the neocerebellum in Hominoidea. J. Hum. Evol. 44, 401–429. Marien, P., Engelborghs, S., Fabbro, F., and De Deyn, P. P. 2001. The lateralized linguistic cerebellum: A review and a new hypothesis. Brain Lang. 79, 580–600. Matano, S. 2001. Brief communication: Proportions of the ventral half of the cerebellar dentate nucleus in humans and great apes. Am. J. Phys. Anthropol. 114, 163–165. Matano, S. and Hirasaki, E. 1997. Volumetric comparisons in the cerebellar complex of anthropoids, with special reference to locomotor types. Am. J. Phys. Anthropol. 103, 173–183. Ott, I., Schleidt, M., and Kien, J. 1994. Temporal organisation of action in baboons: Comparisons with the temporal segmentation in chimpanzee and human behaviour. Brain Behav. Evol. 44, 101–107. Passingham, R. E. 1973. Anatomical differences between the neocortex of man and other primates. Brain Behav. Evol. 7, 337–359. Povinelli, D. J. and Cant, J. G. 1995. Arboreal clambering and the evolution of self-conception. Quart. Rev. Biol. 70, 393–421. Preuss, T. 2000. What’s human about the human brain. In: The New Cognitive Neurosciences (ed. M. S. Gazzaniga), pp. 1219–1234. MIT Press. Rapoport, M., van Reekum, R., and Mayberg, H. 2000. The role of the cerebellum in cognition and behavior: A selective review (see comment). J. Neuropsychiatry Clin. Neurosci. 12, 193–198. Rilling, J. K. and Insel, T. R. 1998. Evolution of the cerebellum in primates: Differences in relative volume among monkeys, apes and humans. Brain Behav. Evol. 52, 308–314. Rilling, J. K. and Insel, T. R. 1999. The primate neocortex in comparative perspective using magnetic resonance imaging. J. Hum. Evol. 37, 191–223.
Rilling, J. K. and Seligman, R. A. 2002. A quantitative morphometric comparative analysis of the primate temporal lobe. J. Hum. Evol. 42, 505–533. Schmahmann, J. D. 1998. Dysmetria of thought: Clinical consequences of cerebellar dysfunction on cognition and affect. Trends Cogn. Sci. 2, 362–371. Schmahmann, J. D. and Pandya, D. N. 1997. Anatomic organization of the basilar pontine projections from prefrontal cortices in rhesus monkey. J. Neurosci. 17, 438–458. Semendeferi, K. and Damasio, H. 2000. The brain and its main anatomical subdivisions in living hominoids using magnetic resonance imaging. J. Hum. Evol. 38, 317–332. Snider, R. S. 1950. Recent contributions to the anatomy and physiology of the cerebellum. Arch. Neurol. Psychiatry. 64, 196–219. Stephan, H., Baron, G., and Frahm, H. 1988. Comparative size of brain and brain components. Comp. Primate Biol. 4, 1–38. Stephan, H., Frahm, H., and Baron, G. 1981. New and revised data on volumes of brain structures in insectivores and primates. Folia Primatol. 35, 1–29. Tomasello, M. and Call, J. 1997. Primate Cognition. Oxford University Press. Tomasello, M., Call, J., and Hare, B. 2003. Chimpanzees understand psychological states – the question is which ones and to what extent. Trends Cogn. Sci. 7, 153–156. Whiting, B. A. and Barton, R. A. 2003. The evolution of the cortico-cerebellar complex in primates: Anatomical connections predict patterns of correlated evolution. J. Hum. Evol. 44, 3–10.
Further Reading Altman, J. and Bayer, S. A. 1997. Development of the Cerebellar System: In Relation to Its Evolution, Structure and Functions. CRC Press. Ghez, C. and Thach, W. T. 2000. The cerebellum. In: Principles of Neural Science (eds. E. R. Kandel, J. H. Schwartz, and T. M. Jessel), pp. 832–852. McGraw-Hill. Kelly, R. M. and Strick, P. L. 2003. Cerebellar loops with motor cortex and prefrontal cortex of a nonhuman primate. J. Neurosci. 23, 8432–8444. Leiner, H. C., Leiner, A. L., and Dow, R. S. 1993. Cognitive and language functions of the human cerebellum. Trends Neurosci. 16, 444–447. MacLeod, C. E., Zilles, K., Schleicher, A., Rilling, J. K., and Gibson, K. R. 2003. Expansion of the neocerebellum in Hominoidea. J. Hum. Evol. 44, 401–429. Matano, S. 2001. Brief communication: Proportions of the ventral half of the cerebellar dentate nucleus in humans and great apes. Am. J. Phys. Anthropol. 114, 163–165. Matano, S. and Hirasaki, E. 1997. Volumetric comparisons in the cerebellar complex of anthropoids, with special reference to locomotor types. Am. J. Phys. Anthropol. 103, 173–183. Rilling, J. K. and Insel, T. R. 1998. Evolution of the cerebellum in primates: Differences in relative volume among monkeys, apes and humans. Brain Behav. Evol. 52, 308–314. Whiting, B. A. and Barton, R. A. 2003. The evolution of the cortico-cerebellar complex in primates: Anatomical connections predict patterns of correlated evolution. J. Hum. Evol. 44, 3–10.
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4.10.1 Anatomy of the Cerebellum 4.10.2 Cerebellar Connectivity and Function 4.10.2.1 The Flocculonodular Lobe 4.10.2.2 The Vermis 4.10.2.3 The Intermediate Hemispheres 4.10.2.4 The Lateral Hemispheres 4.10.3 Comparative Cerebellar Anatomy 4.10.4 The Ape Cerebellum Is Not an Allometrically Enlarged Monkey Cerebellum 4.10.5 Is the Human Cerebellum an Allometrically Enlarged Ape Cerebellum? 4.10.6 Conclusion
Glossary afferents cerebellar vermis dentate nucleus efferents hominid
hominoid neocortex
premotor cortex
Incoming connections. The narrow, middle zone between the two hemispheres of the cerebellum. The most lateral and largest of the cerebellar deep nuclei. Outgoing connections. Any living or extinct habitually bipedal hominoid, including members of the genus Homo and Australopithecus. Any living or extinct ape or human. A uniquely mammalian type of cerebral cortex involved in perception, thought, and reasoning, and consisting of six cytoarchitectonic layers. An area of cortex anterior to motor cortex, corresponding to Brodmann’s area 6, that is involved in motor planning.
4.10.1 Anatomy of the Cerebellum Much like the cerebrum, the cerebellum (Figure 1) consists of cortical gray matter overlying white matter within which lie subcortical nuclei, known as the cerebellar deep nuclei (Figure 2). However, in contrast to the six-layered cerebral cortex (see The Development and Evolutionary Expansion of the Cerebral Cortex in Primates), the cerebellar cortex has only three layers. Within it, Purkinje cells are responsible for integrating excitatory and inhibitory inputs and providing output to the cerebellar deep nuclei, which in turn send projections out of the cerebellum (Figure 3). Thus, most cerebellar efferents originate in the deep cerebellar nuclei. In contrast to the cerebral cortex, cerebellar cortex is
Cerebellum Figure 1 Location of cerebellum in lateral view of human brain. Reproduced from Memory Loss and the Brain. Copyright ª Ann L. Myers/Memory Loss and the Brain.
cytoarchitectonically homogenous and intercortical connectivity is minimal. The cerebellum is composed of four different anatomical regions: the flocculonodular lobe (or vestibulocerebellum), the vermis, the intermediate hemispheres, and the lateral hemispheres. The flocculonodular lobe is on the ventral surface of the cerebellum, abutting the brainstem. The vermis occupies the midline of the cerebellum and is separated from the cerebellar hemispheres by longitudinal furrows on either side. The intermediate portion of the hemispheres is just lateral to the vermis and just medial to the lateral portion of the hemispheres (Figure 3).
4.10.2 Cerebellar Connectivity and Function 4.10.2.1 The Flocculonodular Lobe
The flocculonodular lobe receives input from the primary vestibular afferents and projects back to the vestibular nuclei. This portion of the cerebellum
150 The Evolution of the Cerebellum in Anthropoid Primates
Paravermis + Hemisphere
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Human Cortical gray matter
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Figure 2 Cerebellar anatomy. Reproduced in full from Altman, J. and Bayer, S. A. 1997. Development of the Cerebellar System in Relation to Its Evolution, Structure and Functions. CRC Press.
governs eye movements and body equilibrium during stance and gait.
found in the cortex of the vermis and intermediate hemispheres (see Figure 3).
4.10.2.2 The Vermis
4.10.2.4 The Lateral Hemispheres
The primary sources of input to the cerebellar cortex of the vermis are the spinocerebellar tracts, which carry somatosensory information from axial and proximal body parts. This information is relayed from the cortex of the vermis to the most medial of the deep cerebellar nuclei: the fastigial nucleus. All of the deep cerebellar nuclei have both ascending (to midbrain, thalamus, and cortex) and descending (to brainstem and spinal cord) efferents. Fastigial efferents are predominantly descending, projecting to brainstem nuclei that control proximal muscles of the body and limbs (see Figure 3).
In contrast to the vermis and intermediate hemispheres, the lateral hemispheres receive little somatosensory input from the periphery. Instead, the main source of afferents to the cortex of the lateral hemispheres is the cerebral cortex. In macaques, these corticopontocerebellar fibers originate in motor, premotor, posterior parietal, cingulate, and prefrontal cortex and project to the lateral cerebellar hemispheres by way of the pontine gray matter (Brodal, 1978; Glickstein et al., 1985; Schmahmann and Pandya, 1997). Output from the lateral hemispheres is directed to the most lateral of the deep cerebellar nuclei, the dentate nucleus. Most of the dentate’s efferents ascend to either the parvicellular portion of the red nucleus or the ventrolateral thalamus, which in turn projects to motor, premotor, prefrontal, and posterior parietal cortices (Kelly and Strick, 2003), thereby forming a loop that links lateral cerebellar and cerebral cortex. Based on tract-tracing studies, Strick and colleagues have introduced the notion of closed cerebellar loops in which inputs from cerebral cortical areas are spatially segregated in both cerebellar cortex and the dentate nucleus. For example, projections from motor (e.g., BA4) and nonmotor (e.g., BA46) cortex
4.10.2.3 The Intermediate Hemispheres
The spinocerebellar tracts are also the primary source of input to the cortex of the intermediate hemispheres. The intermediate hemispheres relay information to the interposed cerebellar nuclei (globose and emboliform), which send both ascending and descending efferents to nuclei involved in coordination of distal limb muscles. The ascending projections reach the magnocellular portion of the red nucleus, which gives rise to the rubrospinal tract. Two somatotopic maps of the body are
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Pons M
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Brainstem and spinal cord Figure 3 Schematic of cerebrocerebellar system showing prominent cerebellar afferents (solid lines) and efferents (dashed lines). M, magnocellular portion of red nucleus; P, parvicellular portion of red nucleus; F, fastigial nucleus; I, interposed nucleus; D, dentate nucleus.
have distinct, nonoverlapping representations in the cerebellum, both in the cortex (where they enter) and in the dentate nucleus (where they exit). Specifically, motor cortex projects to lobules IV–VI and nonmotor area 46 projects to crus II. In the dentate, the motor domain is dorsal and the nonmotor domain is ventral (Dum and Strick, 2003). The existence of these closed cerebellar loops is consistent with the suggestion that corticocortical projections are absent within the cerebellar cortex (Braitenberg et al., 1997), in stark contrast to the cerebral cortex (see Figure 3). Consistent with these anatomical data, evidence from neurological patients and functional neuroimaging experiments suggests that the lateral cerebellum of humans has both motor and nonmotor functions. Motor-related functions of the cerebellum include fine motor coordination, motor planning, and motor learning (Ghez and Thach, 2000). The cerebellum has also been implicated in a bewildering array of nonmotor functions, including sensory discrimination,
spatial cognition, visuospatial problem solving, attention and attention switching, procedural learning, verbal working memory, verb generation, verbal fluency, lexical retrieval, syntax, semantic and phonological word retrieval, syntactic processing, and abstract reasoning (Dow, 1988; Leiner et al., 1989; Courchesne et al., 1994; Allen et al., 1997; Desmond and Fiez, 1998; Schmahmann, 1998; Ghez and Thach, 2000; Rapoport et al., 2000; Marien et al., 2001). It seems unlikely that all of these processes can be subsumed under a single overarching function that the cerebellum performs. More likely, as originally suggested by Snider (1950), the cerebellum may be ‘‘the great modulator of neurologic function.’’ That is, it improves the skilled performance of any cerebral area to which it is linked by two-way neural connections (Leiner et al., 1989). Connections with motor areas would increase the speed and skill of movement and connections with cognitive areas would improve the speed and skill of cognition.
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4.10.3 Comparative Cerebellar Anatomy Evidence with respect to the evolution of the primate cerebellum (see Primate Brain Evolution in Phylogenetic Context) comes mainly from cross-species, comparative studies of living primate brains. Some of these studies are based on postmortem specimens (Stephan et al., 1981), whereas others are based on MRI scans obtained from living primates (Rilling and Insel, 1999). Each data set has both advantages and disadvantages. The primary advantage of the postmortem sample is that it permits analysis of microscopic cytoarchitecture, which cannot be observed in MRI scans. On the other hand, the in vivo MRI scans (Figure 4) were obtained from healthy (not old or sick) animals and do not suffer from shrinkage artifacts caused by the postmortem tissue fixation process. Using these data sets, various authors have compared both the size and the histology of the cerebellum and its component structures across the primate order. Below is a summary of what these comparisons have revealed. To begin with, Figure 5a illustrates variation in absolute cerebellum volume across a sample of 11 anthropoid primate species. At least some of this variation is likely attributable to variation in body weight, since most structures are larger in larger animals. Furthermore, the cerebellum is in close contact with the body surface, receiving
Figure 4 MRIs of primate cerebella. Coronal MRI through the cerebellum of: a, rhesus macaque; b, gibbon; c, chimpanzee; and d, human. Reproduced from Rilling, J. K. and Insel, T. R. 1998. Evolution of the cerebellum in primates: Differences in relative volume among monkeys, apes and humans. Brain Behav. Evol. 52, 308–314, with permission from Karger.
somatosensory information from the periphery and modulating descending motor systems that control movement, so that we might expect cerebellar size to track body size. As can be seen in Figure 5a in which species are listed in ascending order of body weight, there is indeed a relationship between body weight and cerebellar volume. In fact, for the sample of 44 anthropoid primates in the Yerkes MRI data set, (log) body weight explained 87% of the variance in (log) cerebellar size (r¼0.93, p<0.001; Figure 5b). Figure 5a demonstrates that the human cerebellum is larger than expected for a primate of our body weight. This is confirmed by Figure 5b in which cerebellar volume is plotted against body weight and a least-squares regression line is fit through the data. Much of the unexplained variance can be attributed to the human data points, which lie well above the prediction based on the regression line. Is the cerebellum unusual in this respect or are other human brain structures also disproportionately large relative to body weight? In fact, the cerebellum is second only to the neocortex, albeit a distant second, in terms of its size relative to body size (Stephan et al., 1988). The fact that the neocortex and cerebellum are the two structures that enlarged most relative to body size in humans, coupled with the existence of extensive connections between the two, suggests the possibility that the neocortex and cerebellum have evolved in tandem as a coordinated system (Barton and Harvey, 2000). Using the method of independent contrasts to eliminate the effect of common inheritance, Barton and Harvey showed that this is indeed the case for primates. Cerebellar contrasts are significantly correlated with neocortex contrasts, and this relationship is stronger than that of cerebellar contrasts and other major brain divisions, such as the medulla, mesencephalon, and diencephalon. In a subsequent analysis, Whiting and Barton (2003) demonstrated correlated evolution in other components of this cerebrocerebellar system among primates. For example, after partialing out evolutionary change in the size of the rest of the brain, they found that evolutionary changes in the size of the pons were positively correlated with changes in the size of both neocortex and cerebellar cortex. In other words, the corticopontocerebellar system that provides input to the cerebellum appears to evolve in concert. There was no significant correlation between pons and the deep cerebellar nuclei, in accord with the lack of direct connectivity between these two structures. On the other hand, there was a strong positive correlation between relative contrasts in deep cerebellar nuclei and relative contrasts in the thalamus, to
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Squirrel Gibbon Rhesus Bonobo Gorilla Orang Capuchin Mangabey Baboon Chimp Human
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–0.5000 0.0000 0.5000 1.0000 1.5000 2.0000
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(b)
Figure 5 Comparison of cerebellum volume in anthropoid primates. a, Mean absolute cerebellum volume from MRI scans in 11 anthropoid primate species, in ascending order of body weight. Note that the gorilla body weight is low for the MRI data set because it is based on one small female and one subadult male. Error bars are 1 SE. b, Regression of log cerebellum volume against log body weight, with least squares regression line fit through the entire sample.
which the nuclei send much of their output en route to the neocortex (see Figure 3).
Monkeys Apes Humans
4.10.4 The Ape Cerebellum Is Not an Allometrically Enlarged Monkey Cerebellum Despite this tendency for the cerebrocerebellar system to evolve as a coordinated whole, it is clear that the relationship between the two structures was altered with the evolution of hominoids (Rilling and Insel, 1998; Semendeferi and Damasio, 2000). When cerebellum volume is regressed on cerebral cortex volume for anthropoid primates, there is a clear grade shift between apes and monkeys, indicating that apes have larger cerebella for any given cerebrocortical volume (Figure 6), and this difference is concentrated in the cerebellar hemispheres as opposed to the vermis (MacLeod et al., 2003). Important differences between apes and monkeys are also found in cerebellar components. Matano and Hirasaki (1997) regressed the volume of the dentate nucleus on the volume of the medulla oblongata for a sample of 26 anthropoid primate species (from Stephan et al., 1981) and found that apes have relatively larger dentate nuclei than monkeys. This was equally true of greater and lesser apes; however, there was an interesting difference between the two in the relative size of the interposed nucleus, which
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log cortical volume (cc) Figure 6 Comparison of cerebellum volume relative to cerebral cortical volume in anthropoid primates. Regression of log cerebellum volume on log cerebral cortical volume, with separate least-squares regression lines fit through the monkey and ape data. Human data points are plotted but not included in either regression. Data are from Rilling and Insel (1998, 1999).
was found to be markedly larger in lesser apes. This raises the possibility that Hylobatidae and Pongidae independently evolved to a similar grade of overall cerebellar development.
154 The Evolution of the Cerebellum in Anthropoid Primates
Given the anatomical connections between the cortex of the lateral cerebellar hemisphere and the dentate nuclei, the larger relative size of the ape dentate suggests that the expansion of the cerebellar hemispheres in apes may be concentrated in the lateral, rather than intermediate portion of the hemisphere. Detailed comparisons of the dentate nuclei reveal further differences between monkey and hominoid cerebella. On the basis of morphological, histological, embryological, histochemical, and pathological evidence, the dentate nucleus is thought to consist of two parts: an older dorsomedial and newer ventrolateral part (Dow, 1988) (Figure 7). Among anthropoid primates, the ventrolateral part is unique to humans and apes (Leiner et al., 1991). Based on neuropsychological and neurophysiological evidence, Leiner et al. (1991) argue that the ventrolateral dentate sends output to nonmotor regions of the frontal lobe by way of the ventrolateral thalamus. This hypothesis will require further testing, perhaps with noninvasive in vivo methods such as diffusion tensor imaging (DTI) that allow visualization of white matter fiber tracts. However, if the hypothesis proves accurate, then the emergence of the ventrolateral dentate in hominoids could reflect a qualitative shift toward increased cerebellar involvement with cognition by virtue of connections with nonmotor frontal lobe regions.
What might be the functional significance of the elaborated cerebellum in hominoids? As suggested above, the enlarged ape cerebellum might improve the functioning of all cortical regions with which it is connected. One cortical target of lateral cerebellar efferents is motor and premotor cortex, and it has been argued that apes have a greater complexity of movement than monkeys (Povinelli and Cant, 1995; MacLeod et al., 2003). Also compatible with this augmentation of function in motor and premotor cortex is Ott’s observation that, in contrast to apes and humans, baboons apparently lack presyntactical motor planning, the ability to modify current movements based on awareness of movements to follow (Ott et al., 1994). Other skills that apes excel at relative to monkeys are also likely to be dependent on the motor and premotor cortex. For example, when reaching for an object, apes and humans exhibit more complex preshaping of their hand compared with monkeys (Christel, 1993; Christel et al., 1998). In addition to these differences in motor-related functions, apes and monkeys also possess numerous cognitive differences. It is conceivable that cerebellar augmentation of prefrontal function could be involved in apes’ putative capacity for self-awareness (Gallup, 1970), components of theory of mind (Tomasello et al., 2003), and capacity for symbolic thought (Tomasello and Call, 1997). Each of these abilities is known to depend upon prefrontal cortex in humans (Deacon, 1997; Frith and Frith, 1999; Gusnard et al., 2001; Gallagher and Frith, 2003).
4.10.5 Is the Human Cerebellum an Allometrically Enlarged Ape Cerebellum?
Figure 7 Dorsal and ventral aspects of the cerebellar dentate nucleus. Coronal section through dentate nucleus, showing dorsal and ventral halves. d, dorsal; v, ventral. Reprinted from Matano, S. 2001. Brief communication: Proportions of the ventral half of the cerebellar dentate nucleus in humans and great apes. Am. J. Phys. Anthropol. 114, 163–165. Copyright ª 2001, Wiley-Liss. Reprinted with permission of Wiley-Liss, Inc., a subsidiary of John Wiley & Sons, Inc.
The human cerebellum is remarkably larger than the ape cerebellum, even after adjusting for differences in body weight (Figure 5). In fact, it is 2.8 times larger than expected for a nonhuman primate of equivalent body weight. Humans also have a larger dentate nucleus for their body size than apes (Matano and Hirasaki, 1997), and the difference is concentrated in the ventrolateral portion of the nucleus (Matano, 2001). Matano (2001) measured the area of the dorsal and ventral halves of the dentate in gorillas, chimps, and humans and calculated a ratio of ventral to dorsal areas in each species. The average human ratio (2.11) was much larger than the average ape ratio (1.64), indicating expansion of the ventral half in humans. Although there are certainly absolutely more cerebrocerebellar connections in humans compared with apes, the degree of connectivity in humans is
The Evolution of the Cerebellum in Anthropoid Primates
probably less than what would be expected for an ape brain of human size. This is because humans fall below the ape regression line of cerebellar volume against cortical volume (Figure 6). This indicates that either (1) humans have small cerebella for their cortex size or (2) humans have large cortices for their cerebellar size. In fact, the existing data support the latter possibility given that the human cerebral cortex is disproportionately large when regressed on other brain structures, and the cerebellum is not disproportionately small when regressed on other brain structures (Deacon, 1988; Rilling and Insel, 1999). This result suggests that some of the cortical regions that expanded in humans did not maintain the degree of connectivity with the cerebellum that is found in apes or that cortical expansion was concentrated in regions that do not receive many cerebellar efferents. A likely candidate is temporal cortex, which is not intimately connected with the cerebellum and known to have expanded extra-allometrically in humans (Rilling and Seligman, 2002). Prefrontal cortex, when defined cytoarchitectonically, is also disproportionately large in humans (Passingham, 1973; Deacon, 1997; Preuss, 2000). What could be the functional significance of the enlarged cerebellar hemispheres and ventrolateral dentate in humans? One possibility is accurate overhand throwing, which likely represented a strong selective pressure throughout our hunting and gathering past (Isaac, 1987; Calvin, 1993). Accurately throwing rocks and projectiles may have been crucial for hunting and scavenging prey, predator defense, and intergroup hostilities. Another possibility is that the enlarged human cerebellum supports fine motor coordination involved in the manufacture and use of tools (see Neurological Specializations for Manual Gesture and Tool Use in Humans). Humans are superior to apes in terms of manual dexterity. However, it is also clear that the cerebellum does indeed take on a cognitive role in humans, being involved in a wide range of mental operations (as discussed above). Leiner et al. (1993) have emphasized its role in language in view of neuropsychological evidence and hypothesized connections with BA44 (Broca’s area). One attractive possibility is that the human cerebellum is involved in a more global augmentation of frontal lobe function that extends to cognitive domains beyond language.
4.10.6 Conclusion 1. Compared with monkeys, apes have larger cerebellar hemispheres for their brain size. 2. The dentate nucleus, the cerebellar deep nucleus that receives input from lateral cerebellar cortex,
155
is also relatively larger in apes than in monkeys and relatively larger in humans than in apes. 3. The ventrolateral portion of the dentate, which may project to nonmotor regions of frontal cortex that are involved in higher cognition, is reportedly absent in monkeys and more developed in humans than in apes. 4. Although the human cerebellum is large relative to body size, the human cerebral cortex is even larger. Consequently, we have a large cerebral cortex for our cerebellum size, and the relative degree of cerebrocerebellar connectivity is probably reduced in humans compared with apes. 5. Given evidence for cerebellar connections with both motor and higher-order association cortex, the above differences in cerebellar anatomy among monkeys, apes, and humans could support motor and cognitive specializations of the three groups.
References Allen, G., Buxton, R. B., Wong, E. C., and Courchesne, E. 1997. Attentional activation of the cerebellum independent of motor involvement. Science 275, 1940–1943. Altman, J. and Bayer, S. A. 1997. Development of the Cerebellar System in Relation to its Evolution, Structure and Functions. CRC Press. Barton, R. A. and Harvey, P. H. 2000. Mosaic evolution of brain structure in mammals. Nature 405, 1055–1058. Braitenberg, V., Heck, D., and Sultan, F. 1997. The detection and generation of sequences as a key to cerebellar function: Experiments and theory. Behav. Brain Sci. 20, 229–245. Brodal, P. 1978. The corticopontine projection in the rhesus monkey. Origin and principles of organization. Brain 101, 251–283. Calvin, W. H. 1993. The unitary hypothesis: A common neural circuitry for novel manipulations, language, plan-ahead, and throwing? In: Tools, Language and Cognition in Human Evolution (eds. K. Gibson and T. Ingold), pp. 230–250. Cambridge University Press. Christel, M. 1993. Grasping techniques and hand preferences in Hominoidea. In: Hands of Primates (eds. H. Preuschoft and D. J. Chivers), pp. 91–108. Springer. Christel, M., Kitzel, S., and Niemitz, C. 1998. How precisely do bonobos (Pan paniscus) grasp small objects? Int. J. Primatol. 19, 165–194. Courchesne, E., Townsend, J., Akshoomoff, N. A., et al. 1994. Impairment in shifting attention in autistic and cerebellar patients. Behav. Neurosci. 108, 848–865. Deacon, T. 1997. The Symbolic Species. W. W. Norton. Deacon, T. W. 1988. Human brain evolution: II. Embryology and brain allometry. In: Intelligence and Evolutionary Biology (eds. H. Jerison and I. Jerison), pp. 383–416. Springer. Desmond, J. E. and Fiez, J. A. 1998. Neuroimaging studies of the cerebellum: Language, learning and memory. Trends Cogn. Sci. 2, 355–362. Dow, R. S. 1988. Contribution of electrophysiological studies to cerebellar physiology. J. Clin. Neurophysiol. 5, 307–323. Dum, R. P. and Strick, P. L. 2003. An unfolded map of the cerebellar dentate nucleus and its projections to the cerebral cortex. J. Neurophysiol. 89, 634–639.
156 The Evolution of the Cerebellum in Anthropoid Primates Frith, C. D. and Frith, U. 1999. Interacting minds: A biological basis. Science 286, 1692–1695. Gallagher, H. L. and Frith, C. D. 2003. Functional imaging of ‘theory of mind’. Trends Cogn. Sci. 7, 77–83. Gallup, G. 1970. Chimpanzees: Self-recognition. Science 167, 86–87. Ghez, C. and Thach, W. T. 2000. The cerebellum. In: Principles of Neural Science (eds. E. R. Kandel, J. H. Schwartz, and T. M. Jessel), pp. 832–885. McGraw-Hill. Glickstein, M., May, J. G., 3rd, and Mercier, B. E. 1985. Corticopontine projection in the macaque: The distribution of labelled cortical cells after large injections of horseradish peroxidase in the pontine nuclei. J. Comp. Neurol. 235, 343–359. Gusnard, D. A., Akbudak, E., Shulman, G. L., and Raichle, M. E. 2001. Medial prefrontal cortex and self-referential mental activity: Relation to a default mode of brain function. Proc. Natl. Acad. Sci. USA 98, 4259–4264. Isaac, B. 1987. Throwing and human evolution. Afr. Archaeol. Rev. 5, 3–17. Kelly, R. M. and Strick, P. L. 2003. Cerebellar loops with motor cortex and prefrontal cortex of a nonhuman primate. J. Neurosci. 23, 8432–8444. Leiner, H. C., Leiner, A. L., and Dow, R. S. 1989. Reappraising the cerebellum: What does the hindbrain contribute to the forebrain? Behav. Neurosci. 103, 998–1008. Leiner, H. C., Leiner, A. L., and Dow, R. S. 1991. The human cerebro-cerebellar system: Its computing, cognitive, and language skills. Behav. Brain Res. 44, 113–128. Leiner, H. C., Leiner, A. L., and Dow, R. S. 1993. Cognitive and language functions of the human cerebellum. Trends Neurosci. 16, 444–447. MacLeod, C. E., Zilles, K., Schleicher, A., Rilling, J. K., and Gibson, K. R. 2003. Expansion of the neocerebellum in Hominoidea. J. Hum. Evol. 44, 401–429. Marien, P., Engelborghs, S., Fabbro, F., and De Deyn, P. P. 2001. The lateralized linguistic cerebellum: A review and a new hypothesis. Brain Lang. 79, 580–600. Matano, S. 2001. Brief communication: Proportions of the ventral half of the cerebellar dentate nucleus in humans and great apes. Am. J. Phys. Anthropol. 114, 163–165. Matano, S. and Hirasaki, E. 1997. Volumetric comparisons in the cerebellar complex of anthropoids, with special reference to locomotor types. Am. J. Phys. Anthropol. 103, 173–183. Ott, I., Schleidt, M., and Kien, J. 1994. Temporal organisation of action in baboons: Comparisons with the temporal segmentation in chimpanzee and human behaviour. Brain Behav. Evol. 44, 101–107. Passingham, R. E. 1973. Anatomical differences between the neocortex of man and other primates. Brain Behav. Evol. 7, 337–359. Povinelli, D. J. and Cant, J. G. 1995. Arboreal clambering and the evolution of self-conception. Quart. Rev. Biol. 70, 393–421. Preuss, T. 2000. What’s human about the human brain. In: The New Cognitive Neurosciences (ed. M. S. Gazzaniga), pp. 1219–1234. MIT Press. Rapoport, M., van Reekum, R., and Mayberg, H. 2000. The role of the cerebellum in cognition and behavior: A selective review (see comment). J. Neuropsychiatry Clin. Neurosci. 12, 193–198. Rilling, J. K. and Insel, T. R. 1998. Evolution of the cerebellum in primates: Differences in relative volume among monkeys, apes and humans. Brain Behav. Evol. 52, 308–314. Rilling, J. K. and Insel, T. R. 1999. The primate neocortex in comparative perspective using magnetic resonance imaging. J. Hum. Evol. 37, 191–223.
Rilling, J. K. and Seligman, R. A. 2002. A quantitative morphometric comparative analysis of the primate temporal lobe. J. Hum. Evol. 42, 505–533. Schmahmann, J. D. 1998. Dysmetria of thought: Clinical consequences of cerebellar dysfunction on cognition and affect. Trends Cogn. Sci. 2, 362–371. Schmahmann, J. D. and Pandya, D. N. 1997. Anatomic organization of the basilar pontine projections from prefrontal cortices in rhesus monkey. J. Neurosci. 17, 438–458. Semendeferi, K. and Damasio, H. 2000. The brain and its main anatomical subdivisions in living hominoids using magnetic resonance imaging. J. Hum. Evol. 38, 317–332. Snider, R. S. 1950. Recent contributions to the anatomy and physiology of the cerebellum. Arch. Neurol. Psychiatry. 64, 196–219. Stephan, H., Baron, G., and Frahm, H. 1988. Comparative size of brain and brain components. Comp. Primate Biol. 4, 1–38. Stephan, H., Frahm, H., and Baron, G. 1981. New and revised data on volumes of brain structures in insectivores and primates. Folia Primatol. 35, 1–29. Tomasello, M. and Call, J. 1997. Primate Cognition. Oxford University Press. Tomasello, M., Call, J., and Hare, B. 2003. Chimpanzees understand psychological states – the question is which ones and to what extent. Trends Cogn. Sci. 7, 153–156. Whiting, B. A. and Barton, R. A. 2003. The evolution of the cortico-cerebellar complex in primates: Anatomical connections predict patterns of correlated evolution. J. Hum. Evol. 44, 3–10.
Further Reading Altman, J. and Bayer, S. A. 1997. Development of the Cerebellar System: In Relation to Its Evolution, Structure and Functions. CRC Press. Ghez, C. and Thach, W. T. 2000. The cerebellum. In: Principles of Neural Science (eds. E. R. Kandel, J. H. Schwartz, and T. M. Jessel), pp. 832–852. McGraw-Hill. Kelly, R. M. and Strick, P. L. 2003. Cerebellar loops with motor cortex and prefrontal cortex of a nonhuman primate. J. Neurosci. 23, 8432–8444. Leiner, H. C., Leiner, A. L., and Dow, R. S. 1993. Cognitive and language functions of the human cerebellum. Trends Neurosci. 16, 444–447. MacLeod, C. E., Zilles, K., Schleicher, A., Rilling, J. K., and Gibson, K. R. 2003. Expansion of the neocerebellum in Hominoidea. J. Hum. Evol. 44, 401–429. Matano, S. 2001. Brief communication: Proportions of the ventral half of the cerebellar dentate nucleus in humans and great apes. Am. J. Phys. Anthropol. 114, 163–165. Matano, S. and Hirasaki, E. 1997. Volumetric comparisons in the cerebellar complex of anthropoids, with special reference to locomotor types. Am. J. Phys. Anthropol. 103, 173–183. Rilling, J. K. and Insel, T. R. 1998. Evolution of the cerebellum in primates: Differences in relative volume among monkeys, apes and humans. Brain Behav. Evol. 52, 308–314. Whiting, B. A. and Barton, R. A. 2003. The evolution of the cortico-cerebellar complex in primates: Anatomical connections predict patterns of correlated evolution. J. Hum. Evol. 44, 3–10.