Evolution of somatosensory and motor cortex in primates

Abstract

Inferences about how the complex somatosensory systems of anthropoid primates evolved are based on comparative studies of such systems in extant mammals. Experimental studies of members of the major clades of extant mammals suggest that somatosensory cortex of early mammals consisted of only a few areas, including a primary area, S1, bordered by strip-like rostral and caudal somatosensory fields, SR and SC. In addition, the second somatosensory area, S2, and the parietal ventral area, PV, were probably present. S1, S2, and PV were activated independently via parallel projections from the ventroposterior nucleus, VP. Little posterior parietal cortex existed, and it was unlikely that a separate primary motor area, M1, existed until placental mammals evolved. Early primates retained this basic organization and also had a larger posterior parietal region that mediated sensorimotor functions via connections with motor and premotor areas. The frontal cortex included M1, dorsal and ventral premotor areas, supplementary motor area, and cingulate motor fields. Ventroposterior superior and ventroposterior inferior nuclei were distinct from the ventroposterior nucleus in the thalamus. In early anthropoid primates, areas S1, SR, and SC had differentiated into the fields now recognized as areas 3b, 3a, and 1. Areas 3b and 1 contained parallel mirror-image representations of cutaneous receptors and a parallel representation in area 2 was probable. Serial processing became dominant, so that neurons in areas 1, S2, and PV became dependent on area 3b for activation. Posterior parietal cortex expanded into more areas that related to frontal cortex. Less is known about changes that might have occurred with the emergence of apes and humans, but their brains were larger and posed scaling problems most likely solved by increasing the number of cortical areas and reducing the proportion of long connections. © 2004 Wiley-Liss, Inc. Key words: galago; premotor; sensorimotor; tarsier; thalamus; ventroposterior nucleusHumans have exceptional sensorimotor skills that appear to be unique in the extent to which they can be individualized and specialized by experience and training. We commonly observe remarkable skills as we view highly trained athletes and musicians, and there are many examples from other activities as well. Such performances stand in contrast to the simple and sometimes clumsy sensorimotor behavior of opossums and laboratory rats. However, vast differences in abilities are to be expected if we consider the differences in the sensorimotor systems of various mammals.The first premise of this review is that early mammals had small brains in proportion to body size, and these brains contained rather simple sensorimotor systems. Furthermore, these simple sensorimotor systems have been retained with little modification in a range of distantly related extant mammals. By using the methods of modern neuroscience to study the sensorimotor systems of these mammals, together with a cladistic character anal-*Correspondence to:

Cortical dopaminergic innervation among humans, chimpanzees, and macaque monkeys: A comparative study

“…The differences between these two groups in both the organization of the frontal cortex and in DAergic innervation of this area are striking and suggest evolutionary changes that paralleled increases in both the size and functional differentiation of the cerebral cortex (e.g., van Eden et al, 1987;Berger et al, 1991;Preuss, 1995;Sesack et al, 1995;Williams and Goldman-Rakic, 1998). For example, the primary motor cortex is thought to be the latest development of a primary cortical field in mammalian neocortical evolution (Sanides, 1970;Kaas, 2004), and is the most densely DA-innervated cortical area in primates (Lewis et al, 1987;Gaspar et al, 1989;Berger et al, 1991). However, homologous motor areas in rodents are sparsely innervated (Berger et al, 1991).…”

“…For comparison, the primary motor cortex (area 4) was also examined. Species differences were not expected in area 4, as it is not associated with cognition and is thought to perform a similar function across primates (Rizzolatti et al, 1998;Kaas, 2004).…”

Microstimulation reveals specialized subregions for different complex movements in posterior parietal cortex of prosimian galagos

“…In either case, the important conclusion to be drawn from the results in macaques and galagos is that circuits for ethologically relevant behaviors can be activated by electrically stimulating given locations in the cortex of both primates. Given the distant relationship of prosimian galagos and anthropoid macaques, with perhaps 70 millions years of separation (16), it is likely that all primates have brain circuits for such ethologically relevant behaviors. It remains to be seen when these circuits emerge in development and whether they depend on or are modified by experience.…”

“…These prosimian primates have many of the functional subdivisions of neocortex of anthropoid primates (monkeys, apes and humans), but galagos have generally simpler brains (16). Thus, galagos have the major divisions of premotor cortex of anthropoid primates (17), while having a less expansive PPC of possibly simpler organization.…”

The thalamic connections of motor, premotor, and prefrontal areas of cortex in a prosimian primate (Otolemur garnetti)

“…PMV in galagos includes mostly orofacial movements and a few upper trunk movements, and the caudal PMD includes hindlimb/trunk and forelimb movements. Motor areas are shown relative to somatosensory, auditory, and visual areas described elsewhere (Kaas, 2004). Somatosensory areas include the primary area, S1 or area 3b, and areas 3a and 1-2 of anterior parietal (AP) cortex.…”