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Primate Neuroethology$

Michael Platt and Asif Ghazanfar

Print publication date: 2010

Print ISBN-13: 9780195326598

Published to Oxford Scholarship Online: February 2010

DOI: 10.1093/acprof:oso/9780195326598.001.0001

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Chapter 10 Chapter 10 Sensory and Motor Systems in Primates

Chapter 10 Chapter 10 Sensory and Motor Systems in Primates

Chapter:
(p.177) Chapter 10 Sensory and Motor Systems in Primates
Source:
Primate Neuroethology
Author(s):

Jon H. Kaas

Publisher:
Oxford University Press
DOI:10.1093/acprof:oso/9780195326598.003.0010

Abstract and Keywords

This chapter reviews the evolution of primate sensory and motor systems, especially with regard to the evolution of a parietal-frontal cortical system that uses information produced by early stages of sensory processing to guide ongoing behavior. It begins with an overview of the components of sensory and motor systems that have been retained from non-primate ancestors. It then attempts to reconstruct the organization of these systems from early primates to branches of the anthropoid radiation, including humans.

Introduction

The task of describing the sensory and motor systems of primates, and how they interrelate to mediate complex behaviors, is clearly daunting. There are a number of systems, all of which are variable in organization and function across primate taxa, and they are incompletely understood, some more than others. In addition, this review needs to be reasonably short, although much can be said, as a recent six-volume series on sensory systems demonstrates (Basbaum et al., 2008). Thus, this review is necessarily selective, with a focus on the evolution of primate sensory and motor systems, especially in regard to the evolution of a parietal-frontal cortical system that uses information produced by early stages of sensory processing to guide ongoing behavior. We start with an overview of the components of sensory and motor systems that have been retained from non-primate ancestors, and proceed to an attempt to reconstruct the organization of these systems from early primates to branches of the anthropoid radiation, including humans. Aspects of the present discussion can be found in previous reviews (Kaas, 2007a b; Kaas & Preuss, 2008; see also Preuss, this volume).

Our Legacy: Sensory and Motor Systems of Early Mammals

The sensory and motor systems of early mammals are of interest because early primates inherited these systems around 60 to 80 Mya and modified them. Early mammals had small brains with proportionately little neocortex. We can infer a lot about how sensory and motor systems were organized in these mammals by seeing how features or traits of these systems are presently distributed across present-day mammals (Kaas, 2007b). It has been especially informative to study the organizations of these systems in those present-day mammals that have small brains and proportionately little cortex (Fig. 10.1). A survey of such brains indicates that early mammals likely had, as one might expect, rather simple sensory and motor systems, with few cortical areas devoted to each system. Remarkably, there was probably no motor cortex that was distinct from somatosensory cortex in the first mammals. Separate motor areas appear to have emerged with the evolution of placental mammals. The major features of sensory and motor systems of early mammals are outlined below.

Chapter 10 Chapter 10 Sensory and Motor Systems in Primates

Figure 10.1 A dorsolateral view of the brain of a Madagascar tenrec (Echinops telfairi), a small Afrotherian mammal. Unlike most extant mammals, the neocortex is only a small cap on the brain. The primary visual (V1), somatosensory (S1), and auditory (A1) and motor (M1) areas have been identified, as well as a secondary somatosensory area (S2). Cortex caudal to A1 may be visual (V?) or multisensory. Notice how much of the forebrain is devoted to olfaction (olf trac = olfactory tract, olf tub = olfactory tubercle). Because of the limited extent of neocortex, the inferior colliculus (IC) and superior colliculus (SC) of the midbrain are exposed. Based on Krubitzer, L.A., Künzle, H., and Kaas, J. (1997). The organization of sensory cortex in a Madagascan insectivore, the tenrec (Echinaps telfairi). Journal of Comparative Neurology, 379, 399–414.

The Visual System

Early mammals had most of the subcortical components of the visual system that are now found in primates. The retina had several classes of ganglion cells, and they projected to the superchiasmatic nucleus of the hypothalamus, the nuclei of the accessory optic system, the ventral lateral geniculate nucleus, the dorsal lateral geniculate nucleus, the pretectum, and the superior colliculus (Berson, 2008). The dorsal lateral geniculate nucleus provided the major activating input to visual cortex (Kaas et al., 1972). Retinal ganglion cell classes resembling the P and M classes of primates (see later) (p.178) innervated about half of the neurons in the dorsal lateral geniculate, and retinal inputs were segregated to form cryptic contralaterally and ipsilaterally innervated layers. A more caudal portion of the geniculate received inputs from thin, more slowly conducting axons resembling those of the primate K-cell class (see later). Most of the geniculate outputs were to primary visual cortex (V1), which projected broadly to other visual and nonvisual areas of cortex, including somatosensory and auditory fields (Wang & Burkhalter, 2007). Major visual targets were the second visual area, V2, along the lateral border of V1, and a small visual temporal region caudolateral to V2. Cortex on the medial border of V1, a limbic or retrosplenial field, now identified in primates as prostriata, also received V1 inputs (Lyon, 2007). These areas also distributed visual information to other regions of cortex, including somatosensory, auditory, motor, frontal, limbic, and multisensory fields. Finally, the visual thalamus included a small pulvinar, usually identified in nonprimates as the lateral posterior nucleus or complex. Different parts of this small pulvinar received inputs from the superior colliculus and visual cortex, and this information was relayed to visual cortex. Another part of this poorly differentiated pulvinar received inputs from visual cortex and relayed back to visual cortex. Thus, the visual pulvinar possibly had three divisions, and visual cortex had three or four. A sector of the reticular nucleus of the ventral thalamus had inputs from visual cortex and the visual thalamus, projecting via inhibitory neurons into the visual thalamus (Crabtree & Killackey, 1989).

The Somatosensory System

Early mammals retained from reptilian ancestors most of the afferent systems that brought sensory information into the central nervous system (Kaas, 2007b). Obviously, new sensory opportunities arose with the evolution of body hair. Thus, early mammals had receptor afferents sensitive to touch, hair movement, vibration, muscle and joint movement, temperature, and painful stimuli. Longer sensory hairs (vibrissae) evolved to detect objects at short distances from the skin via receptors around the base of each hair. In early mammals, afferents (p.179) from the face, facial vibrissae, and mouth were especially important, as they are in most mammals today.

Sensory afferents from the skin and deeper tissue entered the spinal cord or brainstem, where they terminated in specific layers of the dorsal horn of the spinal cord or in sensory brainstem nuclei (Fig. 10.2). The large fiber afferents related to tactile or muscle spindle receptors also sent branches that coursed in the brainstem or dorsal columns of the spinal cord to terminate in a complex of nuclei, the trigeminal–dorsal column complex, at the junction of the cervical spinal cord and brainstem. The traditional gracile, cuneate, and trigeminal nuclei for tactile inputs formed a medial to lateral sequence of subnuclei of a single functional unit that systematically represents the body from the hindlimb to the forelimb to the face and mouth. Neurons in this dorsal column–trigeminal nucleus projected to the ventroposterior nucleus of the contralateral thalamus. Neurons representing at least part of the mouth, the tongue, and teeth projected to the ipsilateral ventroposterior nucleus as well (Bombardieri et al., 1975). As in present-day mammals, the ventroposterior nucleus (VP) represented the body from hindlimb (and tail) to the mouth in a lateromedial sequence. In early mammals, and most mammals today, many or most of the tactile inputs were from the face and mouth, and a large subnucleus of VP, distinguished as the ventroposterior medial “nucleus” (VPM), represented the face and mouth. The remaining, more lateral part of VP, representing the rest of the body, is typically called the ventroposterior lateral “nucleus” (VPL). Functionally, VPM and VPL are subdivisions of VP.

Chapter 10 Chapter 10 Sensory and Motor Systems in Primates

Figure 10.2 A diagram of the organization of the somatosensory system of early mammals. Processing starts with receptors and afferents of the skin, muscles, and joints. Rapidly (RA) and slowly (SA) adapting receptors in the skin mediate aspects of touch. Muscle spindle receptors help mediate proprioception. Other receptors include those that mediate pain, temperature, and aspects of touch and movement. Afferents terminate in the trigeminal–dorsal column complex where the face, hand, and foot are represented in a lateromedial sequence, and muscle spindle inputs terminate in separate nuclei. Afferents also activate spinal cord neurons that project to the contralateral thalamus. The somatosensory thalamus includes the ventroposterior nucleus for SA and RA inputs, and usually unnamed adjoining groups of cells corresponding to the ventroposterior superior nucleus (VPS) of primates for muscle spindle inputs and the ventroposterior inferior nucleus (VPI) of primates for spinothalamic inputs. The somatosensory segment of the reticular nucleus (RT) interacts with cortex and these nuclei. Somatosensory cortex includes the primary area, S1, with adjoining rostral somatosensory (SR) and caudal somatosensory (SC) areas, the second somatosensory area (S2), and the parietal ventral area (PV).

In all mammals, VP projects to primary somatosensory cortex (S1). In primates, this cortex is distinguished as area 3b of anterior parietal cortex, and it is appropriate to use the anatomical term 3b for S1 in other mammals, although various combinations of architectonic terms for S1 are in current use. Comparative evidence indicates that S1 of early mammals represented the contralateral body surface from tail to tongue in a mediolateral sequence in parietal cortex, with the limbs facing forward (rostrally or anteriorly). As in mammals today, part of the ipsilateral mouth, the tongue and teeth, were also represented via the ipsilateral inputs to VPM.

Primary somatosensory cortex of early mammals activated three or four adjoining fields. Cortex along the rostral and caudal margins of S1 were activated via topographically ordered projections in mediolateral sequences so that they formed narrow somatosensory representations on the margins of S1. Here these areas are called the rostral (SR) and caudal (CR) somatosensory areas (Fig. 10.1). In primates, these bordering bands of cortex constitute area 3a, with a major involvement in proprioception, and area 1, a secondary tactile area. One or two areas lateral to S1 also received topographically organized projections from S1. One of these areas, the second somatosensory area (S2), has been described in all adequately explored mammals, and was certainly present in early mammals. Another adjoining area, the parietal ventral area (PV), has been more recently identified in mammals, and the comparative evidence indicates that it exists in a broad range of mammals, and most probably was present in early mammals. S2 and PV represent the contralateral body as two small mirror images of each other. Both S2 and PV received activating inputs from the ventroposterior nucleus, as well as from S1. These somatosensory areas distributed to adjoining insular and cingulate and frontal areas of cortex. A small fringe of more posterior cortex was all that could be considered posterior parietal cortex, and this region received somatosensory and other sensory inputs, and had connections with frontal cortex. Connections also reached perirhinal cortex and the hippocampus (Fig. 10.2).

In addition to cortical representations of tactile receptors, muscle spindle and joint receptor information reached the somatosensory thalamus from separate subnuclei in the dorsal column–trigeminal complex. In primates, the relayed proprioceptive information terminates in a separate nucleus of the contralateral thalamus, the ventroposterior superior nucleus (VPS), but this nucleus has not been commonly distinguished in nonprimates. Yet, the available evidence suggests that the proprioceptive inputs (p.180) (p.181) to the thalamus of early mammals was likely to have been at least partly segregated in the dorsorostral part of VP, becoming more distinctly separated later with the evolution of primates, carnivores, and perhaps other lines of descent. Here, a VPS is shown as present in early mammals (Fig. 10.2), although it was probably poorly differentiated from VP.

Another source of information to the somatosensory thalamus was from second-order neurons that form the spinothalamic tract for the body and the functionally equivalent part of the trigeminothalamic tract for the face and mouth. Much of the information relayed in this pathway is nociceptive and thermoreceptive, but tactile and proprioceptive information is included as well (Dostrovsky & Craig, 2008). These thalamic inputs, representing the contralateral half of the body, terminated in and around the ventroposterior nucleus. In primates, they largely terminate in the ventroposterior inferior nucleus (VPI) and cell-poor septa that extend from this nucleus well into the ventroposterior nucleus to isolate subnuclei. However, VPI has not been distinguished in most mammals, although a VPI is well developed in raccoons, and it can be identified in cats and a few other mammals. Here a VPI nucleus is shown for early mammals (Fig. 10.2), although it may not have been histologically distinct from VP. Probably, most mammals have a spinothalamic pathway that terminates largely on small neurons on the ventral margin of VP and scattered within VP. These small cells in VPI and VP appear to project to the superficial layers of S1, S2, PV, and the rostral and caudal somatosensory belt areas (e.g., Penny et al., 1982). Their major role may be to modulate neurons in these areas and signal stimulus intensity. Other neurons in this spinothalamic pathway terminated in poorly defined groups of cells ventral and caudal to VP, sometimes called the posterior group, where information about temperature and pain is relayed to cortex caudal to S2 and PV in insular cortex. In addition, somatosensory visceral information in spinothalamic pathways was relayed via a basal ventromedial thalamic nucleus to part of insular cortex, and from the parafasciculus nucleus to the striatum (Craig, 2002; Dostrovsky & Craig, 2008).

Taste

The gustatory sense is mediated by a specialized part of the somatosensory system. As in present-day mammals, primary taste afferents from the taste buds on the tongue terminated in the nucleus of the solitary tract, a nucleus that receives various viscerosensory inputs over its long extent through most of the medulla. One of the functions of the nucleus is to project to neurons in the adjacent reticular formation, where neurons in turn project to motor nuclei involved in reflexes concerned with the acceptance (licking) or rejection (tongue protrusion) of palatable or aversive tastes. The nucleus of the solitary tract also projected rostrally to the parabrachial nucleus that in turn relayed to the lateral hypothalamus and amygdala. The parabrachial nucleus also provided taste, tactile, and viscerosensory information to the gustatory nucleus of the somatosensory thalamus, the parvocellular ventroposterior medial nucleus (VPMpc). This nucleus projected to cortex just ventral to the mouth and face representations of S1, possibly including both the granular cortex belonging to the S1 tongue representation and the dysgranular cortex corresponding to a representation of taste and tactile inputs just ventral to the S1 tongue representation and dorsal to the rhinal fissure (Kosar et al., 1986; Norgren & Wolf, 1975). Thus, there may have been at least two targets of VPMpc in early mammals, one in the tongue representation in primary somatosensory cortex (see Remple et al., 2003) and one in adjacent insular cortex. However, the representation of the tongue in S1 is usually not considered to be part of gustatory cortex. Gustatory cortex of insular cortex is thought to project directly or indirectly to a higher-order multisensory processing zone in orbitofrontal cortex (Pritchard & Norgren, 2004).

Pain and Temperature

A number of ascending systems that carry nociceptive and temperature information have been described in mammals (see for review Dostrovsky & Craig, 2008; Lima, 2008). For our purposes here, the relevant pathways are those that reach the dorsal thalamus and are (p.182) relayed to cortex, as the cortex is thought to be necessary for consciously appreciating the nature of painful stimuli and temperature change. Modifications and elaborations of nociceptive and temperature systems at the thalamic and cortical levels in primates allowed these systems to become involved in more behaviors (Craig, 2007). Limited comparative evidence suggests that in all mammals, pain and temperature information is relayed from peripheral afferents by trigemino- and spinothalamic projections to and around the ventroposterior nucleus of the thalamus, the poorly defined posterior complex or nucleus, the intralaminar nuclei, and other targets, such as hypothalamus, amygdala, and septal nuclei. Much of the information is relayed from thalamic targets to insular cortex just ventral to somatosensory cortex (S1 and S2), somatosensory cortex, and anterior cingulate cortex. Craig (2007) proposes that the primordial role of insular cortex was to participate in the sensing of noxious and temperature stimuli and to modulate and control brainstem homeostatic integration sites, including those associated with the autonomic nervous system. Somatosensory cortex probably played a role in sensing these stimuli as well, but possibly in terms of the intensities of noxious stimuli, rather than the painful aspects. Inputs to cingulate cortex were probably indirect, but important in limbic motor functions.

The Auditory and Vestibular Systems

The auditory systems of mammals share a number of components that likely were retained from an early mammal ancestor (Carr & Edds-Walton, 2008; Kaas & Hackett, 2008). All depend on a peripheral auditory system that includes an external ear that is generally mobile and a short canal ending at the tympanic membrane. The presence in the middle ear of a chain of three small bones that transmit vibrations from the tympanic membrane to the sound window of the cochlea of the inner ear is a characteristic of mammals. The cochlea is a complicated organ that allows the hair cells to be stimulated and activate the afferents of the auditory nerve that terminate on the neurons of the cochlear nuclei. These neurons provide information about sound intensity and frequency. Disparities in the information relayed by the afferents from each cochlea allow central circuits to extract information about sound location. Auditory processing starts in the three divisions or “nuclei” of the cochlear nuclear complex, which relay to nuclei of higher levels in the brainstem of both sides. These include the nuclei of the superior olivary complex, the nuclei of the lateral lemniscus, and subdivisions of the inferior colliculus of the midbrain. The divisions of the inferior colliculus project to the medial geniculate complex, where neurons relay to auditory cortex. The ventral nucleus of the medial geniculate complex (MGv) projects to the auditory core of auditory cortex, the primary area or areas, while other divisions, the dorsal nucleus (MGd) and medial or magnocellular nucleus (MGm), project more broadly to secondary auditory and multisensory areas of cortex.

Most investigated mammals have an auditory core of two to three primary or primary-like areas, one of which (but not always the same one) has been identified as primary auditory cortex, A1 (Fig. 10.1). The comparative evidence suggests that early mammals had a core of at least an anterior auditory field, AAF, and an A1, surrounded by a narrow belt of several secondary auditory fields. Each secondary field in turn involved, via connections, other regions of cortex in auditory and multisensory processing. Core areas were tonotopically organized, and AAF and A1 were distinguished by having mirror-image or reversed patterns of tonotopic organizations. In present-day mammals, the tonotopic organizations of secondary auditory cortex are less precise, when they are present, and often difficult to reveal.

The sense of balance is mediated by the vestibular system (see for review Graf, 2007), which is not well understood at thalamic and cortical levels of processing, partly because the system can be difficult to study and partly because we are largely unaware of its sensory functions in postural control, reflexes, and the perception of self-movement. The organ for balance is part of the inner ear, and it consists of semicircular (p.183) canals and otoliths of the labyrinth. Hair cells in the labyrinth are stimulated by the movement of fluid in the canals and in the otoliths. Afferents in the vestibular nerve innervate vestibular nuclei, which provide inputs to a number of control systems, such as those controlling eye movement reflexes. Vestibular information also is relayed to the thalamus, and then to cortex, but this network is poorly understood in most mammals. The thalamic and cortical levels of processing, which are largely multisensory, have been more investigated in primates.

Motor Systems

Judging from somewhat limited comparative evidence (see for review Beck et al., 1996; Nudo & Frost, 2007), early mammals did not have a region of motor cortex that was distinct from somatosensory cortex. While more studies are needed, motor cortex apparently did not emerge as a separate area or areas until eutherian mammals evolved some 140 million years ago (Kaas, 2007b). Judging from results from members of the other two major branches of mammalian evolution, the monotremes and the marsupials, primary somatosensory cortex of early mammals received both somatosensory information from the ventroposterior nucleus of the thalamus and motor-related information from the cerebellum via projections from the ventrolateral thalamic nucleus, which is considered part of the motor thalamus. This early somatosensory cortex influenced motor behavior via projections to the basal ganglia and other subcortical targets, but the corticospinal pathway was rather poorly developed (Nudo & Frost, 2007; Nudo & Masterton, 1988). Comparative studies of placental mammals, in contrast, indicate that most or all have at least one distinct motor area, primary motor cortex (M1), and likely a second motor area (M2), which may be homologous to either premotor cortex or the supplementary motor area of primates. In placental mammals, M1 (Fig. 10.1) and S1 are distinguished by inputs from the ventral lateral nucleus of the motor thalamus and the ventroposterior nucleus of the somatosensory thalamus, respectively. In addition, M1 has a more developed corticospinal projection system, and thereby has a more direct impact on motor behavior. Most of the evidence for a second motor area in placental mammals comes from rats, where there is evidence for a second forelimb representation rostral to M1 that has cortical and subcortical connections that differ from those of M1 and are more similar to those of premotor cortex and the supplementary motor area of monkeys (Rouiller et al., 1993). Tree shrews, which are one of the closest living relatives of primates, have a strip of cortex along the rostral border of M1 that can be either considered a second parallel motor representation, M2, or possibly part of M1 (Remple et al., 2006). Microstimulation of M2 required higher currents than M1 for evoked movements, and M2 had few corticospinal neurons, which were densely distributed across M1, area 3a, and S1. Connection patterns suggest that tree shrews also have a motor area on the medial wall of the cerebral hemisphere, possibly a cingulate motor area. Thus, tree shrews appear to resemble primates more closely than rats in motor cortex organization. Studies of other mammals would be useful in determining how motor cortex varies and is similar across mammalian taxa.

Olfactory System

Structures for processing olfactory information were proportionately large and important for early mammals. Olfactory receptor cells connect directly to the olfactory bulb, which in early mammals had a surface area as large as all of neocortex, as in tenrecs today (Fig. 10.1). The olfactory bulb, in turn, projected to a huge expanse of olfactory (piriform) cortex, which had connections to frontal cortex via the dorsal thalamus (Wilson, 2008). In proportion to the rest of the brain, the olfactory bulb and cortex are small in primates, especially in anthropoid primates, where vision has become so important for the recognition of conspecifics, other animals, and food, and smell has become less important, especially in humans. Mammals also have an accessory olfactory system with inputs from the vomeronasal organ that is (p.184) involved in pheromone detection and other chemosensory functions. In chimpanzees and humans, the vomeronasal organ and the rest of the accessory olfactory system are degenerate (Bhatnagar & Smith, 2007) and nonfunctional. Thus, males no longer sniff the urine of females to determine the state of their reproductive cycle.

Sensory and Motor Systems in Primates

The sensory and motor systems of early mammals have been modified and expanded in many ways in subsequent lines of mammalian evolution. The altered auditory cortex of echolocating bats serves as one well-known example. Yet, the greatest changes are likely to be found in the cortical components of sensory and motor systems in those mammals with large brains and greatly expanded cortex, and humans are exceptional in this regard. However, all primate brains are exceptional in that they have many more neurons than rodent brains of the same size (Herculano-Houzel et al., 2007). Primates, in addition, have a cortex that is subdivided into an unusually large number of cortical areas, and the number of areas appears to be greater in those anthropoid primates with larger brains. In addition, many of their cortical areas are involved in sensory processing and motor behavior.

Here, we consider sensory and motor systems, especially at the cortical level, in members of the major branches of the primate radiation, the prosimian primates, New and Old World monkeys, and apes and humans. The interesting tarsiers, with a highly differentiated and expanded visual system (Collins et al., 2005a), are not considered here, as little is known about their other sensory systems or their motor system. Tarsiers have evolved to be highly specialized as visual predators of insects and small vertebrates.

The Visual Systems of Primates

All primates are characterized by a well-developed visual system, including forward-facing eyes, a laminated lateral geniculate nucleus and a number of pulvinar nuclei in the visual thalamus, and a visual cortex with a large primary area and a number of additional visual areas (Kaas, 2003; Kaas & Collins, 2004; Kremers, 2005). Early primates were nocturnal, and many of the prosimian primates remain nocturnal, but the early anthropoid primates were diurnal, and all have remained diurnal except owl monkeys, which reverted to nocturnal life. Thus, all anthropoid primates, except owl monkeys, are specialized for diurnal vision. This includes an emphasis on cone- rather than rod-mediated vision, a fovea in the retina for detailed vision, and a great investment in the parvocellular pathway from the retina to the lateral geniculate nucleus, as this pathway is devoted to the detailed, color vision that is used in object recognition. In macaque monkeys, and probably most other anthropoid primates, 80% of the retinal ganglion cells are devoted to the parvocellular (P) pathway (Weller & Kaas, 1989). The retina of primates also has two other types of outputs that are named after the layers they project to in the lateral geniculate nucleus (LGN); the magnocellular or M-cell pathway and the koniocellular or K-cell pathway, each accounting for about 10% of the retina’s output. The M-cell subsystem is specialized for the detection of changes in contrast, such as that caused by a blinking light or a moving object. The koniocellular system is not well understood, but it contains information from the blue (S) cones and thereby is involved in color vision (Casagrande & Xu, 2004).

The LGN of all primates is divided into two pairs of parvocellular layers, one with inputs from the ipsilateral eye and one with inputs from the contralateral eye (Kaas et al., 1978). In anthropoid primates other than owl monkeys, these layers are thick and they are subdivided, producing four or more sublayers in the part of the nucleus devoted to central vision. The thinner magnocellular layers are also paired, one for each eye. The LGN of nocturnal prosimian primates has two well-developed koniocellular layers, one for each eye, but the small cells of this system are not so distinct in (p.185) anthropoid primates, and they are generally considered to be between layers (interlaminar cells) rather than forming layers. However, in nocturnal owl monkeys, a thick koniocellular region is found. Thus, the koniocellular pathway seems to be more important in nocturnal primates. Unlike some mammals, such as cats and other carnivores, the LGN of primates projects almost exclusively (but not completely so) to a large primary visual area, V1.

The retinal K and M cells (but not the P cells in anthropoid primates) also project to the superior colliculus, which in turn projects to the LGN and parts of the visual pulvinar (Kaas & Huerta, 1988). The superior colliculus of all primates is specialized for frontal, binocular vision, and unlike other mammals, each colliculus represents only the contralateral visual hemifield, rather than the whole visual field of the contralateral eye (Fig. 10.3). This remarkable modification of the visual system appears to be related to an emphasis on frontal vision, but the implication of this change for the behavior in early primates is not completely clear. Another major modification is the huge projection to the superior colliculus from the many visual areas of cortex (Collins et al., 2005b).

Chapter 10 Chapter 10 Sensory and Motor Systems in Primates

Figure 10.3 The unique type of retinotopic organization of the superior colliculus that is shared by all primates but differs from all studied nonprimates. The circles at the top represent the two eyes, while the large circle below represents a surface view of the left superior colliculus (SC). Arrows on the back of the eye indicate the temporal part of the retina that projects to the ipsilateral SC in mammals (white arrows). In primates, this projection is largely overlapped by a projection from the larger nasal retina from the contralateral eye (black arrow). The line of decussation (LD) marks the dividing point for these two projections. The LD runs vertically through the fovea. In nonprimates both the temporal segment of the retina of the contralateral eye (longer black arrow) and the temporal retina (short black arrow) project to the contralateral superior colliculus, creating a representation of the complete retina. This extended representation may aid in the detection of movement and predators from all parts of the visual field, while the primate SC is more devoted to frontal vision.

The pulvinar of primates contains inferior, lateral, and medial divisions (Kaas & Huerta, 1988). The medial division has mixed functions, judging from its cortical connections, but the lateral division of two nuclei and the inferior division of four nuclei are all visual (Kaas & Lyon, 2007). The superior colliculus provides K-cell and M-cell information to the pulvinar and K-cell information to the LGN. Most of the other activating inputs to pulvinar nuclei are from visual cortex. Thus, the pulvinar complex (p.186) relays superior colliculus information to visual cortex, and distributes visual cortex information back to visual cortex. Some of the possible functions of such cortical-thalamic-cortical loops are discussed by Sherman and Guillery (2005). The larger nuclei of the pulvinar complex project to early visual areas in the cortical processing hierarchy, those with mixed visual functions or an emphasis on object vision, while a cluster of inferior pulvinar nuclei, including those with dense superior colliculus inputs, project to a cluster of temporal lobe visual areas concerned with visual motion and using vision for guiding motor behavior (Kaas & Lyon, 2007).

All primates have a greatly expanded cortical visual system. This elaboration is greater in anthropoid primates than in prosimians. However, many of the cortical visual areas that characterize anthropoid primates are present in prosimian galagos (Fig. 10.4), indicating that these visual areas emerged early in primate or preprimate evolution. Tree shrews, which are the closest living relative of primates that have been studied, also devote much of their cortex to visual processing (see Remple et al., 2006), suggesting that some of the specializations of visual cortex in primates predate primates and are shared by tree shrews. All primates have a large primary visual area, V1, that has an orderly internal organization so that cells are grouped by the particular orientation of visual stimuli, such as lines, that best activate them. V1 is divided into a number of pinwheels of such clusters of cells, which together represent a given region of visual space and all orientations. Tree shrews and carnivores also have such pinwheels of orientation selective cells, but rodents do not (Van Hooser et al., 2005), suggesting that tree shrews and primates shared an ancestor with orientation pinwheels, while carnivores evolved them independently. The main outputs of V1 are to the second visual area, V2, which is divided into a series of repeats of three types of band-like clusters of cells, two of which are devoted to different aspects of object vision and the third part of a processing stream for visual guidance of motor control (Casagrande & Kaas, 1994; Roe, 2003). This specialization of V2 is apparently unique to primates. Most of the other outputs of V1 are to a third visual area, V3, and the middle temporal visual area, MT.

Chapter 10 Chapter 10 Sensory and Motor Systems in Primates

Figure 10.4 A dorsolateral view of the brain of a prosimian galago with major sensory and motor areas indicated. Visual areas include primary (V1), secondary (V2), and third (V3) visual areas, as well as the dorsolateral (DL), middle temporal (MT), fundal superior temporal (FST), MT crescent (MTc), medial superior temporal (MST), and dorsomedial (DM) visual areas. Much of posterior parietal (PP) and inferior temporal (IT) cortex contains additional visual areas. Auditory cortex includes primary auditory cortex (A1), the rostral auditory area (R), areas of the auditory belt (AB), and areas of the parabelt (not shown). Somatosensory cortex includes primary somatosensory cortex (S1 or area 3b), adjoining somatosensory areas 1 and 3a, the second area (S2), and the parietal ventral area (PV). Motor areas include the primary area (M1), dorsal (PMD) and ventral (PMV) premotor areas, a frontal eye field (FEF), supplementary motor cortex (SMA), and rostral and caudal cingulate motor areas (CMAr and CMAc) that are not shown. Dots in V1 and bars in V2 signify types of modular organization (see text).

Two of the classes of cell bands (modules) in V2 project to the dorsolateral visual area (DL), also known as V4. DL/V4 is a critically important visual area in the so-called ventral stream of visual processing areas devoted to object vision (Ungerleider & Mishkin, 1982). DL/V4 projects in turn to inferior temporal cortex (IT), which consists of several visual areas. Parts of IT cortex feed into memory-related areas that connect with the hippocampus, and to the prefrontal cortex of the frontal lobe for “working memory” and other functions. Overall, a huge amount of cortex is devoted to this object vision cortical stream, even in prosimians (Fig. 10.4), but much more in anthropoid primates (Fig. 10.5).

Chapter 10 Chapter 10 Sensory and Motor Systems in Primates

Figure 10.5 A lateral view of the brain of an owl monkey showing subdivisions of sensory and motor cortex (below) and a view of the cortex after it has been removed and flattened. See Figure 10.4 and text for abbreviations. Plus and minus notations in visual areas indicate representations of upper (+) and lower (–) visual hemifields. Rostral (DLr) and caudal (DLc) divisions of DL (V4) are shown, as well as caudal (ITc), rostral (ITr), medial (ITm), and polar (ITp) divisions of inferior temporal cortex. Dashed lines indicate opened fissures. M, medial visual area; VPP, ventral posterior parietal area; RI, retroinsular cortex; CC, corpus callosum.

The third type of module in V2 projects to MT, as some classes of neurons in V1 do directly (Casagrande & Kaas, 1994). MT contains orderly arrangements of clusters of cells sensitive to stimulus orientation and direction of movement (see Xu et al., 2004). MT is one of a number of visual areas that appear to be unique to primates and collectively have the major role of further analyzing visual inputs to extract information about object and global motion, which is then sent to subdivisions of posterior parietal cortex (see Figs. 10.4 and 10.5). Thus, area MT is interconnected with bordering areas MST, MTc, and FST. FST has dorsal and ventral divisions with the dorsal division, FSTd, having interconnections with MT and the ventral division, FSTv, having connections with MTc (Kaas & Morel, 1993). These areas are also associated with band-like portions of V3, the caudal division of DL (DLc), and the dorsomedial area, DM. Areas MT, MST, and FSTd all project to portions of posterior parietal cortex. Together, these areas, including those in posterior parietal cortex, constitute most of the dorsal stream of visual processing that is concerned with visually guiding motor behavior. It is in posterior parietal cortex where transformations occur from analyzing sensory information to informing sensorimotor programs that induce ethologically relevant behaviors.

(p.187) Posterior Parietal Cortex and the Sensorimotor Transformation

Most mammals have very little cortex that can be called posterior parietal cortex (e.g., Fig. 10.1), but this region of the brain has greatly expanded in all primates (Figs. 10.4 and 10.5). The expansion may have preceded the emergence of primates, as tree shrews, close relatives of primates, have a strip of posterior parietal cortex that is somewhat enlarged, and has basic features of primate posterior parietal cortex (Remple et al., 2007). Thus, posterior parietal cortex in tree shrews receives both visual inputs from higher-order visual areas and somatosensory inputs from higher-order somatosensory areas, while projecting to motor cortex.

Prosimian primates have proportionately less posterior parietal cortex than anthropoid primates, but recent studies in prosimian galagos have revealed a lot about the organization of posterior parietal cortex (Fig. 10.6). Most notably, posterior parietal cortex is divided into rostral (PPr) and caudal (PPc) zones, with the rostral zone dominated by somatosensory inputs from higher-order somatosensory areas (S2, PV, area 1) and the caudal zone dominated by visual inputs from higher-order visual areas (V2, V3, DM, MT, MTc, MST, DLr). The caudal zone, PPc, projects to the rostral zone, PPr, so that both visual and somatosensory inputs reach PPr. Rostral PP is organized into a mediolateral series of functionally distinct sensorimotor zones that were revealed by electrical stimulation with microelectrodes. As described by Graziano and coworkers for motor cortex and even part of posterior parietal cortex in macaque monkeys (p.188) (see Graziano, 2006; Graziano, this volume), half-second trains of electrical pulses, which are longer than those typically used for cortical stimulation, can evoke complex movements. In galagos, such half-second trains of brief electrical pulses evoked hindlimb and forelimb movements when medial sites in PPr were stimulated (hindlimb and forelimb in Fig. 10.6C). These movements, evoked in anesthetized galagos, resembled climbing movements. More laterally in PPr, defensive forelimb movements, reaching movements, and hand-to-mouth movements could be evoked from separate regions of cortex. Finally, in the most lateral portion of posterior parietal cortex, eye movements, defensive face movements, and aggressive face movements were evoked from separate cortical territories (Stepniewska et al., 2005). The existence of these different subregions for different complex, ethologically relevant movements suggests that a number of cortical networks exist for specific types of functionally important movements. As similar movements can be evoked from motor and premotor cortex, it appears that posterior parietal modules contain circuits that use visual and somatosensory information to activate and modulate outputs. These modules dictate specific categories of (p.189) useful movements, which are then mediated via projections to motor and premotor cortex, where the movement patterns are likely adjusted and refined. Aspects of the final movement patterns would also depend on motor nuclei circuits in the brainstem and spinal cord. In support of this proposal, our ongoing experiments in galagos and New World monkeys indicate that any block of neural activity in primary motor cortex, M1, abolishes the motor behavior evoked from PPr.

Chapter 10 Chapter 10 Sensory and Motor Systems in Primates

Figure 10.6 The organization of posterior parietal cortex in prosimian galagos. See Figure 10.4 and text for abbreviations. (A) A dorsolateral view of the brain with visual, somatosensory, motor, and posterior parietal areas outlined. (B) Arrows indicate visual areas projecting to the caudal half of posterior parietal cortex and somatosensory and motor areas projecting to the rostral half. (C) An enlarged view of posterior parietal cortex showing regions where electrical stimulation evoked different types of ethologically relevant complex movements. From Stepniewska, I., Fang, P. C., & Kaas, J. H. (2005). Microstimulation reveals specialized subregions for different complex movements in posterior parietal cortex of prosimian galagos. Proceedings of the National Academy of Sciences, 102, 4878–4883. Used with permission.

While posterior parietal cortex is unlikely to be organized in the same way in all primates, our experiments have produced results very similar to those from galagos in New World owl and squirrel monkeys. The arrangements of areas and functional subregions may be somewhat different in posterior parietal cortex of Old World macaque monkeys, where current proposals include a number of areas, defined by responses to sensory inputs, connection patterns, and cortical architecture, that do not closely reflect their organization described here for posterior parietal cortex of galagos and New World monkeys. While there is not complete agreement on areas and names for areas, macaque areas include ventral (VIP), medial (MIP), lateral (LIP), and anterior (AIP) areas of the intraparietal sulcus, as well as a number of other areas (see Lewis & Van Essen, 2000). Yet, when half-second trains of electrical pulses were applied to VIP, defensive movements were evoked (Cooke et al., 2003), and eye movements have been elicited by electrically stimulating LIP (Kurylo & Skavenski, 1991; Thier & Andersen, 1998). Other parts of posterior parietal cortex in macaques appear to be involved in reaching and grasping (Calton et al., 2002; Snyder et al., 2000). Thus, the organization of posterior parietal cortex in Old World macaque monkeys may not be so different than in New World monkeys and prosimians. Some (p.190) investigators, using functional magnetic resonance imaging, have results that suggest similarities between macaques and the more extensive posterior parietal cortex of humans (e.g., Swisher et al., 2007).

The Somatosensory System of Primates

While vision was obviously very important to early primates, most early primates were small and adapted to a nocturnal lifestyle that included feeding in the fine branches of bushes and trees on insects, small vertebrates, fruits, and leaves (Ross & Martin, 2007). This lifestyle required unusual sensorimotor abilities as these primates needed to hold on to moving branches while reaching for food. According to Whishaw (2003), visual guidance of hand movements is one of the most distinguishing features of primates. One of the reasons for reaching for food, rather than grasping it with their mouth, was to protect the large, forward-facing eyes. As an adaptation for greater hand use, primates have large concentrations of low-threshold mechanoreceptors in the glabrous skin of the hand, especially of the Meissner corpuscles, subserving the rapidly adapting type 1 afferents with small receptive fields and sensitivity to stimulus change (see for review Kaas, 2004). An enlarged representation of the glabrous skin of the hand is found in somatosensory nuclei and cortical areas of primates, especially Old World monkeys, apes, and humans.

In the thalamus, the ventroposterior complex of primates is well differentiated into a ventroposterior inferior nucleus (VPI) with spinothalamic inputs, a ventroposterior nuc-leus (VP) with inputs from cutaneous mechanoreceptors, and a ventroposterior superior nucleus (VPS) with inputs from muscle spindle receptors (Kaas, 2007). An anterior pulvinar (PA) can be identified, and it has connections with areas of somatosensory cortex. The nonprimary homolog of PA is not obvious, but PA possibly corresponds to the posterior nucleus of rodents.

Anterior parietal cortex organization varies across primates (Qi et al., 2008). In prosimian primates, three areas can be distinguished: a primary area, S1, which is clearly homologous with area 3b of anthropoid primates, and narrow strips of somatosensory cortex bordering S1 (3b) rostrally and caudally (Fig. 10.4). Area 3b gets inputs from VP in prosimians and all other primates. The more rostral somatosensory strip (SR) gets input from VPS, and is involved in proprioception in all primates and in at least some other mammals. This strip is clearly area 3a of anthropoid primates. The identity of the caudal somatosensory strip (SC) is less clear. It is in the position of area 1 of anthropoid primates, but unlike area 1, SC does not respond well to light touch on the skin. While area 1 gets dense projections from VP, the projections are sparse in SC. As a further difference, there is no evidence for an area 2 just caudal to SC, as an area 2 with inputs from VPS is caudal to area 1 in anthropoid primates. Possibly an area like SC differentiated into area 1 of anthropoid primates, or perhaps SC differentiated into both area 1 and area 2. Here we tentatively identify SC as area 1. Areas 3a, 3b, 1, and 2 of anthropoid primates (Fig. 10.5), including humans, contain parallel representations of the contralateral half of the body, from hindlimb to tongue in a mediolateral sequence. Together these fields interconnect with somatosensory areas of lateral (insular) parietal cortex, posterior parietal cortex, and motor cortex.

Lateral somatosensory of the upper bank of the lateral fissure and the insula contain additional somatosensory areas, including S2 and PV of other mammals, the ventral somatosensory area (VS), the parietal rostral area (PR), and likely others. The organization across primate taxa is not well understood, but differences are likely given the large extent of insular cortex in some anthropoid primates. Pathways through lateral parietal cortex are thought to be important in the recognition of objects by touch (Murray & Mishkin, 1984) and form the functional equivalent of the ventral visual stream of processing. Posterior parietal cortex, as discussed previously, also forms an important part of the somatosensory system, constituting much of the dorsal steam of somatosensory processing for guiding reaching and other actions.

(p.191) Gustatory Cortex

The organization of the taste or gustatory system is not well understood in any mammals. Thus, modifications in primates are not clear. The standard view for primates is that the thalamic taste nucleus, VPMpc, projects to both the tongue representation of “S1” and to a large primary gustatory region in the cortex of the lateral sulcus (Fig. 10.7A). The gustatory area, G, in turn projects (apparently not directly) to orbitofrontal cortex, where hedonic or pleasurable aspects of taste are processed with other types of relevant information (see for review Kaas et al., 2006). More current evidence indicates that VPMpc projects to the tongue representation of area 3b, and possibly area 1, and that corticocortical connections implicate tongue representations in areas 3a and 1 in processing taste (Iyengar et al., 2007). While an area G may exist, another possibility is that the tongue portions of several areas of the cortex of the lateral sulcus are involved in taste (Fig. 10.7B).

Chapter 10 Chapter 10 Sensory and Motor Systems in Primates

Figure 10.7 Proposed locations of cortical taste areas shown on a lateral view of the brain of a squirrel monkey. (A) Early investigators did not consider the architectonic fields 3a, 3b, 1, and 2 of anterior parietal cortex to be separate fields, and grouped them together in S1, where the lateral part represents the tongue and gets input from the parvocellular ventral posterior medial nucleus (VPMpc). However, the main projections of VPMpc were thought to be to the gustatory area, G, at the rostral end of the central sulcus. Area G was thought to project to a hedonistic (H) taste region in orbitofrontal cortex (OBF). (B) A contemporary view of somatosensory cortex organization in monkeys. The region of G appears to contain parts of several somatosensory areas (also see Fig. 10.5), suggesting that tongue representations in several fields may contribute to the processing of taste information. Note that the tongue is represented twice in area 3b. c, contralateral. Modified from Kaas, J. H., Qi, H-X., & Iyengar, S. (2006). Cortical network for representing the teeth and tongue in primates. Anatomical Records Part A, 288A, 182–190. Used with permission.

Pain and Temperature

According to Craig (2003, 2007), primates differ from other mammals in having two specific regions of the thalamus that have differentiated as sites for the termination of nociceptive information from the spinal cord and brainstem, the posterior part of the ventral medial nucleus (VMpo) and the ventral caudal part of the medial dorsal nucleus (MDvc). VMpo provides projections in turn to a representation of painful stimuli in the dorsal portion of insular cortex, where other representations of body sensations, including temperature, may exist. Another projection is to part of area 3a for uncertain functions. MDvc projects to anterior cingulate cortex to motivate behavioral responses.

Auditory Cortex in Primates

Possibly due to limited study, the subcortical auditory system of primates is thought to be highly similar to those in other mammalian taxa. This cannot be quite true, as the greatly expanded cortical auditory system of primates would be reflected by changes in the thalamus, as cortical areas have thalamic interconnections and subcortical connections, such as those to the inferior colliculus. With this note of caution, present understandings of the organization of auditory cortex in primates are outlined.

All anthropoid primates appear to have a strip of auditory cortex that has the characteristics of a primary sensory field (Kaas & Hackett, 2008). This strip of cortex, generally called the auditory core, consists of three auditory areas, distinguished by their differing patterns of tonotopic organization (Fig. 10.5). The core has the well-differentiated layer 4 and other architectonic characteristics of primary sensory areas, as well as activating inputs from a thalamic relay nucleus, the ventral nucleus of the medial geniculate complex, MGv. Neurons in the core respond well to pure tones, and neurons in different locations across the three primary areas respond best, or at the lowest sound intensity, to tones of different frequencies. The auditory core in monkeys is in cortex of the lower bank of the lateral sulcus, where it forms an elongated caudorostral strip. The so-called primary area, A1, is the caudal-most area. The most caudal neurons in A1 respond to tones of the highest frequency, and neurons at progressively more rostral locations in A1 respond best to tones of progressively lower frequencies. Neurons in bands running perpendicular to this caudorostral frequency gradient respond best to tones of roughly the same frequency. These bands or rows of neurons constitute the lines of isorepresentation for tones in A1. The pattern of tonotopic representation in A1 reverses for the rostral auditory area, R, and again for the rostrotemporal auditory area, RT. The core has been histologically identified in a number of primates, including macaques, chimpanzees, and humans (Hackett et al., 2001). In prosimian galagos, only A1 and R of the core have been identified (Fig. 10.4). The three core areas seem very much alike, but a presumption is that they have at least somewhat different functional roles. One hypothesis is that they contribute differently to dorsal and ventral streams of auditory processing, with the dorsal stream more concerned with locating sounds in space and the ventral stream involved in deducing the meanings of the sounds (see Rauschecker & Tian, 2000). (p.192)

(p.193) The auditory core is surrounded by a “belt” of adjacent auditory areas that at least partly depend on inputs from the core for activation. The cortical connections of the core, at least in monkeys, are almost completely with the belt. The number of areas in the belt is somewhat uncertain; the proposed number is eight, with two areas on the caudal end of A1 and pairs of inner and outer areas on each side of A1, R, and RT. Presently, there is evidence that at least three of the auditory belt areas are tonotopically organized, although this is difficult to determine as neurons in the belt areas generally respond much better to complex sounds than tones (Rauschecker et al., 1995). One of the belt areas, the caudomedial area (CM), has many neurons that respond to light touch (Fu et al., 2003), while another area, the middle lateral belt (ML), is influenced by vision (Ghazanfar et al., 2005), demonstrating a surprising substrate for bisensory integration at a very early level of auditory processing (see Romanski & Ghazanfar, this volume). Auditory belt areas connect broadly to core areas, other belt areas, the adjacent parabelt region, and even more distant cortical regions, such as prefrontal cortex where neurons responsive to visual and auditory stimuli are found (Romanski & Goldman-Rakic, 2002). Thalamic inputs are from dorsal (MGd) and medial (MGm) divisions of the medial geniculate complex, and other thalamic nuclei, suggesting multisensory or broader auditory functions. The more rostral belt areas appear to be more involved in a ventral stream for sound identification, with the more caudal belt areas more concerned with sound localization.

The auditory parabelt constitutes a third level of auditory cortical processing in primates. The parabelt in monkeys occupies the part of the superior temporal gyrus that adjoins the lateral belt (Fig. 10.5). The parabelt region gets dense inputs from the auditory belt areas, but practically no input from the core. Connections from belt areas are most dense with nearer portions of the parabelt, suggesting that the parabelt has functional divisions. Hackett and colleagues (1998) divided the parabelt into rostral (RPB) and caudal (CPB) regions with most dense connections with rostral or caudal belt areas, respectively.

The parabelt projections are to regions of cortex that we define as the fourth level of cortical auditory processing. Areas of the fourth level are diverse and distributed across the temporal, parietal, and frontal lobes. One of these regions is cortex of the upper bank of the superior temporal cortex in monkeys. This appears to be a region where neurons respond to auditory and visual stimuli (see Cusick, 1997). Neurons in this and other bisensory fields may function to localize a sound to a visual object (the so-called ventriloquist effect) (see Romanski & Ghazanfar, this volume). Other projections are to rostroventral parts of the superior temporal cortex. This cortex relays auditory information to orbitofrontal cortex that is involved in evaluating the rewarding value of stimuli (Rolls, 2004). Projections of the parabelt to cortex of the temporal-parietal junction and adjoining parietal cortex are to multisensory regions (visual somatosensory, auditory) where neurons project to the frontal eye fields (Huerta et al., 1987), perhaps to help direct the eyes toward sounds of interest. Parietal lobe multisensory areas also project to premotor areas of the frontal lobe, where they help guide motor behavior. Finally, parabelt projections to prefrontal granular cortex (Romanski & Goldman-Rakic, 2002) may be involved in working memory for auditory signals. Auditory and visual parts of prefrontal cortex project to premotor areas of frontal cortex, thus providing another source of sensory guidance of motor behavior.

Humans, of course, differ from other primates in that the left cerebral hemisphere is usually specialized for language. However, an asymmetry between the extent and shape of the lateral sulcus between the left and right hemispheres has been described, not only in humans, but also, from skull endocasts, in the brains of our extinct ancestors, suggesting that left hemisphere auditory specialization preceded the emergence of language (Galaburda et al., 1978). In humans, a region of cortex near the auditory core is enlarged in the left hemisphere, and this region, as part of Wernicke’s area, appears to be important in language. In the frontal lobe, a premotor region is enlarged in the left (p.194) hemisphere, constituting the main part of Broca’s speech area (Foundas et al., 1996). These may be only some of the ways in which the human auditory system differs from that of monkeys. For further discussion on the issue of cerebral asymmetries, see Hopkins in this volume.

Vestibular Cortex

Multisensory integration in the vestibular system occurs as early as in the vestibular nuclei of the brainstem, and cortical areas with neurons sensitive to vestibular system activation are multisensory areas (Guldin & Grüsser, 1998). Probably the main cortical vestibular region in monkeys, the closest to a primary vestibular area, occupies the medial part of retroinsular cortex (Fig. 10.5). This region where half of the neurons respond to vestibular stimuli is called the parietal insular vestibular cortex (PIVC). A more posterior region of the cortex of the lateral fissure, the visual posterior sylvian area (VPS), is involved in visuomotor reflexes, and has neurons that are vestibularly activated or modulated. A third vestibular zone, the part of somatosensory area 3a where neck muscles are represented, also has neurons activated by vestibular stimulation. Parts of area 7 and area 2 have also been implicated in this extended, multisensory vestibular cortical system, and these vestibular cortical areas have a broader influence via connections with other cortical fields.

Cortical Motor Areas in Primates

Motor cortex has expanded and increased in number of areas in primates (Kaas, 2007b). Even prosimian galagos have an enlarged primary area (M1), a dorsal (PMD) and ventral (PMV) premotor area, a supplementary motor area (SMA), a presupplementary motor area (pre-SMA), a frontal eye field (FEF), and at least rostral (CMAr) and caudal (CMAc) cingulate motor areas (Figs. 10.4 and 10.6). These same areas are found in anthropoid primates (Fig. 10.5), where there is evidence for an increase in the number of premotor fields.

Primary motor cortex (M1) contains a mosaic of small regions, each devoted to a specific movement. These small regions are disbursed within a larger, gross somatotopic pattern that progresses from hindlimb, trunk, forelimb, and face to tongue in a mediolateral sequence across frontal cortex (Donoghue et al., 1992; Gould et al., 1986; Huang et al., 1988; Preuss et al., 1996). The gross pattern of somatotopic organization is similar across individuals of the same species, but the mosaic pattern varies in detail. M1 receives inputs from other frontal motor areas, including PMD, PMV, SMA, and cingulate areas; some of the somatosensory areas including areas 3a, 1, 2, S2, and PV; and posterior parietal cortex (see Fang et al., 2005; Stepniewska et al., 1993). Other important inputs are from the posterior ventrolateral nucleus (VLp) of the thalamus, which receives projections from the cerebellar nuclei (e.g., Stepniewska et al., 2003). M1 provides the majority of projections to brainstem and spinal cord motor circuits, and the projection to the upper spinal cord circuits that control the digits is enlarged in Old World monkeys and in the highly dexterous New World Cebus monkeys compared to most New World monkeys and prosimian primates (Nudo & Frost, 2007). Due to this more direct pathway, movements can be evoked at lower current levels from M1 than from other frontal motor areas, although stimulation thresholds from PMV can be nearly as low. Brief trains of electrical pulses in M1 have long been known to evoke simple movements, such as the extension of a digit. More recently, Graziano (this volume; Graziano et al., 2002) and coworkers have shown that larger, half-second trains of electrical pulses can evoke more complex, behaviorally relevant movements, such as hand-to-mouth movements, from M1 of macaque monkeys. In our unpublished studies led by Iwona Stepniewska, complex movements were evoked from M1 of galagos and squirrel monkeys. Complex movements have also been evoked from premotor cortex, as well as from posterior parietal cortex (see previous section), but inactivation of M1 abolishes or greatly modifies these movement patterns, suggesting that M1 is the final cortical (p.195) target in the circuits for such behaviors. However, the circuits addressed by the subcortical projections of M1 must be important in organizing aspects of the movement patterns.

All primates have dorsal and ventral divisions of the classical premotor cortex. Mainly forelimb and mouth and face movements are evoked from PMV, while both forelimb and hindlimb movements are evoked from PMD. Thresholds for evoking movements in PMD are higher than those for M1, while those for PMV can be higher or similar (e.g., Preuss et al., 1996). Although both of these areas project to the spinal cord and brainstem, much of their influence on motor behavior may depend on their projections to M1. Both PMV and PMD receive inputs from frontal cortex, posterior parietal cortex, and higher-order somatosensory fields. PMD appears to be divided into two fields in New and Old World monkeys, and two or three divisions of PMV have been proposed for Old World monkeys (e.g., Matelli et al., 1985). Thus, the number of premotor areas appears to be greater in macaque monkeys, and this is likely the case for apes and humans, where even more premotor fields may exist. Broca’s area in the left cerebral hemisphere of humans may be an elaboration of one or more of the PMV fields (see Preuss et al., 1996).

The supplementary motor area, SMA, has been described in prosimian galagos (Fig. 10.4), New World monkeys (Fig. 10.5), Old World monkeys, and humans (see Tanji, 1994; Wu et al., 2000, for reviews). SMA is located just dorsal to the hindlimb representation in M1, and it represents the hindlimb, forelimb, and face in a caudorostral sequence (e.g., Gould et al., 1986). SMA has been implicated in generating movement sequences and in bimanual coordination of movements (Tanji, 1994). SMA has dense projections to M1, while having some projections to the spinal cord. Inputs include those from posterior parietal cortex, pre-SMA, and cingulate motor cortex (Luppino et al., 1993). In addition, SMA receives inputs from both the basal ganglia and the cerebellum relayed through the motor thalamus (Akkal et al., 2007). The more rostrally located pre-SMA differs from SMA, being densely connected with prefrontal cortex, being involved in nonmotor tasks, and having a lack of projections to the spinal cord. Connections with SMA are not dense and direct projections to M1 are sparse or absent (Luppino et al., 1993; see Akkal et al., 2007, for review).

The cingulate motor areas are in frontal cortex of the medial wall of the cerebral hemisphere (Fig. 10.4). In macaques, three cingulate motor areas have been proposed, on the dorsal (CMAr and CMAd) and ventral (CMAv) banks of the cingulate sulcus ( Picard & Strick, 1996, for review). These areas differ somewhat in connections, but collectively they include those with prefrontal cortex, M1, the spinal cord, and parietal cortex. Microstimulation of CMAd and CMAv evoke movements in patterns that suggest that these fields have somatotopic organizations. CMAv is less responsive to stimulation. CMAr is thought to not control movements directly, but signal errors, reinforcement, and conflict, and thereby be involved in supervisory control (Schall et al., 2002).

Finally, all primates appear to have a frontal eye field (FEF) and perhaps a supplementary eye field (SEF). Microstimulation of these areas produces eye movements, and both fields project to the deeper layers of the superior colliculus (Huerta & Kaas, 1990; Huerta et al., 1986). The FEF has cortical connections with SEF and the SMA, prefrontal cortex, visual areas of the temporal lobe, and posterior parietal visuomotor areas (Huerta et al., 1987). Neurons in FEF respond to visual stimuli or control eye movements in a decision-making process (Schall et al., 2002). The connections of the SEF are more extensive with cortical areas and subcortical structures related to prefrontal and skeletomotor functions (Huerta & Kaas, 1990).

Conclusions

This review outlines major features of the organizations of sensory and motor systems in primates in comparison with the likely organizations of these systems in the nonprimate ancestors of primates. The major premise of the review is that sensory and motor systems have changed in many ways with or before the emergence of early primates, and more variation (p.196) subsequently occurred in the different lines of primate evolution. In general, prosimian galagos seem to have changed the least, but the sensory and motor systems of all primates are distinctly different from those of other mammals.

Alterations of sensory systems have been revealed most extensively in neocortex, which of course has expanded greatly in all primates, but especially humans. Alterations have been of two main types: those within areas common to all or most mammals, and the addition of areas that seem to be unique to primates, and even to specific lines of primate evolution. This review gives a global overview of the evolution of sensory and motor areas in primates, but much has been left out, most notably the implications of the huge increases in brain and especially neocortex size in some primates, especially apes and humans. A larger brain could mean larger sensory and motor areas, and at least the more easily identified sensory areas, such as V1, S1, and the auditory core are larger in larger brains. Yet, cortex has expanded more in the larger ape and human brains than the primary sensory areas, indicating that the larger brains also likely have more cortical areas. In addition, the functions of cortical areas relate to their sizes (Kaas, 2000), in part because cortical neurons do not vary much in size so that large areas have more neurons but less widespread intrinsic connections. Thus, large sensory areas are not well suited for global integration of sensory inputs from across the receptor sheet. As primates with larger brains and larger cortical areas evolved, the internal organizations and functions of cortical areas changed as areas increased in size so that they were less involved in global integration. Other, smaller sensory areas evolved to take over roles in global integration. Thus, the other major change that seems to have occurred in the evolution of primate taxa with larger brains is an increase in the number of areas, including the number in sensory and motor systems. This potentially increases the steps in serial processing, and it is the repetition of the local processing within columns of cells from area to area that allows complex outcomes from computationally simple steps. Adding cortical areas also increases the potential for functionally distinct parallel pathways to emerge, thereby adding functions and abilities.

In brief, primate brains differ from other brains by maintaining a similar level of neuronal density as brains increase in size. Primate brains also differ from nonprimate brains in the ways their sensory and motor systems are organized. Finally, the organizations of these systems vary within and across the major branches of primate evolution, probably much more than in any other mammalian order.

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