The Basic Somatosensory System

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The basic somatosensory system includes afferents from the peripheral receptors that terminate in the spinal cord or brain stem, a relay of second-order neurons from these structures to the thalamus, projections from the thalamus to different areas of neocortex, and a number of interconnected cortical somatosensory areas that project to motor cortex, other cortical areas, and subcortical structures. Afferents include those from several types of mechanoreceptors in the skin, muscle-spindle and joint receptors that signal movement and position, and afferents mediating temperature and pain. Here, our concern is with the parts of the system that are involved in tactile discriminations. Thus, we concentrate on the parts of the somatosensory system devoted to the inputs from mechanoreceptors in the skin for tactile information and to the muscle-spindle and joint receptors for information about position and movement, since tactile discriminations involve active exploration of surfaces and objects.

Afferents from the mechanoreceptors in the skin and muscle spindles terminate in a somatotopic pattern (for review, including humans and other primates, see Florence et al., 1989; Coq et al., 2000) in the dorsal column-trigeminal complex in the lower brain stem. Some of the muscle-spindle afferent terminations are segregated in separate subnuclei (the external cuneate "nucleus" for the forelimb). There is evidence from cats (Dykes et al., 1982) that the rapidly adapting (RA) and slowly adapting (SA) classes of afferents terminate in separate clusters of cells in the dorsal column nuclei. Glaborous skin has two types of slowly adapting afferents (SAI and SAII) associated with Merkel cell and Ruffini endings, respectively, and two types of rapidly adapting afferents (RAI and RAII), associated with Meissner corpuscles and Pacinian corpuscles, respectively. Hairy skin also has hair follicle receptors.

The mechanoreceptor and other afferents related to pain and temperature sensibilities also terminate in the dorsal horn of the spinal cord and the brain stem equivalent, where second-order neurons cross to form the ascending spinothalamic tract. The ascending spinothalamic information is clearly important, but after a thalamic relay, its role in the traditional areas of somatosensory cortex seems to be one of modulation rather than activation. After sectioning of the afferents in the dorsal columns of rats, the deprived areas of at least S1 are totally and persistently deactivated (Jain et al., 1995). Similarly, in monkeys, dorsal column section (Jain et al., 1997) abolishes all evoked activity in all four areas of the anterior parietal cortex (areas 3b or S1, 3a, 1, and 2). We conclude that only the dorsal column-medial lemniscus system is capable of independently activating primary and most-likely secondary areas of somatosensory cortex. While other afferents may have an important modulating role, and they are certainly critical in mediating pain and temperature sensations, dorsal column afferents are capable of mediating tactile discriminations by themselves.

The second-order neurons in the dorsal column-trigeminal complex cross and ascend to the contralateral ventroposterior nucleus (VP) in the thalamus. The RA and SA response classes are preserved in this relay, and these two types constitute the major inputs to VP, where they activate separate groups of neurons in cats (Dykes, 1982), monkeys (Dykes et al., 1981), and perhaps other mammals. Relay of the muscle-spindle, and possibly other, afferents terminate rostrodorsally just outside VP (Wiener et al., 1987) in a part of the thalamus that Dykes (1983) has distinguished as the ventroposterior oralis nucleus (VPO) while others included it in the posterior (PO) complex (see Gould et al., 1989). The thalamic nucleus for muscle spindles in primates has been called the ventroposterior superior nucleus (VPS). Possibly VPO, PO or part of it, and VPS are homologous nuclei.

In all investigated mammals, VP projects to the somatosensory koniocortex or primary somatosensory cortex (S1). Evidence from cats (e.g., Macchi et al., 1959) and a number of other species (see Garraghty et al., 1991) suggests that in the typical non-primate pattern some neurons in VP also project to the second somatosensory area, S2, and to a more recently described adjacent area, the parietal ventral area, PV (Krubitzer and Kaas, 1987). Some of the same neurons that project to S1 also project to S2 (see Spreafico et al., 1981). This means that S1 and S2 can be independently activated from the thalamus and that S2 does not depend on its inputs from S1 for activation. The capacity of S1 and S2 for parallel processing of VP outputs has been demonstrated in opossums (Coleman et al., 1999), rabbits (Murray et al., 1992), cats (Burton and Robinson, 1987), and tree shrews (Garraghty et al., 1991) by recording evoked responses in S2 after deactivating S1. In addition to VP, a medial posterior nucleus, Pom, also projects to both S1 and S2 (see Krubitzer and Kaas, 1987 for review).

The somatosensory cortex of many, and perhaps most, non-primate mammals appears to consist of five areas that are at least predominantly somatosensory in function. These areas are S1, S2, PV, and the cortical strips along the rostral and caudal borders of S1 (Figure 1.1). In opossums, we called these strips the caudal and rostral somatosensory areas, SC and SR (Beck et al., 1996). They have also been called the rostral (R) and posterior medial (PM) fields (Slutsky et al., 2000). In cats (Dykes, 1983; Felleman et al., 1983a), raccoons (Feldman and Johnson, 1988) and the flying fox (Krubitzer and Calford, 1992), a fruit bat, the rostral field has been called area 3a, because it resembles area 3a of primates in position, architecture, connections, and responsiveness to the stimulation of deep tissues (muscle-spindle receptors). In rats and squirrels, the rostrally bordering (and intruding into S1) area is known as dysgranular cortex (Chapin and Lin, 1984; Gould et al., 1989). The

FIGURE 1.1 Five somatosensory areas have been proposed for the North American opossum (Didelphis marsupialis): a primary somatosensory area (S1), a secondary area (S2), a parietal ventral area (PV), and caudal (SC) and rostral (SR) somatosensory areas bordering S1. For reference, primary (V1) and secondary (V2) visual areas and auditory cortex (Aud.) are shown. The olfactory bulb (OB) is on the left. Based on Beck et al., 1996. In some opossums, such as Monodelphis domestica, PV may not be apparent (Huffman et al., 1999; Catania et al., 2000; Frost et al., 2000).

FIGURE 1.1 Five somatosensory areas have been proposed for the North American opossum (Didelphis marsupialis): a primary somatosensory area (S1), a secondary area (S2), a parietal ventral area (PV), and caudal (SC) and rostral (SR) somatosensory areas bordering S1. For reference, primary (V1) and secondary (V2) visual areas and auditory cortex (Aud.) are shown. The olfactory bulb (OB) is on the left. Based on Beck et al., 1996. In some opossums, such as Monodelphis domestica, PV may not be apparent (Huffman et al., 1999; Catania et al., 2000; Frost et al., 2000).

caudal area of the flying fox has been referred to as area 1/2 (Krubitzer and Calford, 1992) as it is in the same relative position as area 1 of primates and appears to be responsive to both cutaneous and deep receptors as area 2 of primates.

In all investigated mammals, S1 systematically represents the mechanoreceptors of the skin of the opposite side of the body (see Kaas, 1983). The body parts are usually represented from tail to tongue in a mediolateral sequence. The representations of different body parts often have a morphological counterpart in the cortex that can be visualized using appropriate histochemical techniques. These isomorphs of the body are best known for S1 of rats and mice, where an orderly arrangement of oval-like aggregates of neurons, one for each whisker on the side of the face, have long been described as the cortical barrels (Woolsey and Van Der Loos, 1970). Metabolic markers, cytochrome oxidase (CO), and succinic dehydrogenase have been used to reveal more of the isomorph including discrete cellular clusters for other whiskers and for the digits and pads of the forepaws and hindpaws (Dawson

Star-nosed mole

FIGURE 1.2 An example of isomorphs of body parts in primary somatosensory cortex S1. The star nose mole has 11 sensory rays on each half of its nose (A). These rays are represented in order in S1 and S2 of the contralateral cerebral hemisphere. In brain sections cut parallel to the cortical surface and processed for cytochrome oxidase (CO), the representation of each ray in S1 can be seen as a CO-dark stripe separated from neighbors by narrow CO-light septa, Numbered 1-11 in B corresponding to rays 1-11 in A. A second array of CO-dark stripes can be seen in S2 below S1 (unnumbered in A). The stripes are drawn in C. A and B are based on Catania and Kaas, 1995.

FIGURE 1.2 An example of isomorphs of body parts in primary somatosensory cortex S1. The star nose mole has 11 sensory rays on each half of its nose (A). These rays are represented in order in S1 and S2 of the contralateral cerebral hemisphere. In brain sections cut parallel to the cortical surface and processed for cytochrome oxidase (CO), the representation of each ray in S1 can be seen as a CO-dark stripe separated from neighbors by narrow CO-light septa, Numbered 1-11 in B corresponding to rays 1-11 in A. A second array of CO-dark stripes can be seen in S2 below S1 (unnumbered in A). The stripes are drawn in C. A and B are based on Catania and Kaas, 1995.

and Killackey, 1987; Li et al., 1990; Pearson et al., 1996). An isomorphic array of cortical bands, one for each of the 11 rays of the contralateral half of the nose, is especially prominent for the star-nosed mole (Figure 1.2; Catania and Kaas, 1995, 1996). Such isomorphs help identify S1, demonstrate existence of a single systematic representation in S1, and distinguish S1 from other representations. The star-nosed mole is unusual in that two other cortical representations, S2 and possibly PV, also have isomorphs of the rays of the nose. In addition, S2 also has a very prominent isomorph of the forepaw, while a comparable isomorph of the forepaw does not exist in S1 (Catania, 2000). This suggests a more pronounced or specialized role for S2 for forepaw afferents than for S1 in moles.

In a wide range of mammals, S1 projects directly to S2, PV, SR, and SC (see Beck et al., 1996). Thus, all of these areas are involved in further processing of information from S1, as well as processing inputs from the thalamus. S2 and PV receive VP inputs, while SR and SC receive most of their thalamic inputs from neurons just outside of VP (Pom and adjacent parts of the VP "shell"). Some of this thalamic relay may be of muscle-spindle information (see Gould et al., 1989), as it appears to be for area 3a of cats (see Felleman et al., 1983a). S2 has been described in a large range of mammalian species (see Nelson et al., 1979; Sur et al., 1981 for review) and it seems to be a universal or nearly universal (see Krubitzer et al., 1995) subdivision of the somatosensory cortex. S2 borders S1 laterally, with face representations adjoining. Other body parts are represented more distantly from the S1/S2 border, and the forepaw and hindpaw are represented along the rostral border of S2. Because of uncertainties about the organization of S2, some early investigators may have failed to distinguish S2 from the rostrally adjoining parietal ventral area, PV, and confounded observations from two areas. PV was first distinguished as a mirror image representation of S2 along the rostral border of S2 in squirrels (Krubitzer et al., 1986), and the area has now been identified in a range of mammalian species (see Beck et al., 1996). Both S2 and PV respond throughout to cutaneous stimuli. Both appear to be higher level processors of information from S1, but PV also receives feed forward projections from S2. Thus, PV is characterized by a convergence of thalamic VP and cortical S1 and S2 inputs. Projections from PV include an even more ventral and rostral cortical region that we have called parietal rostral, PR (Krubitzer et al., 1986). Thus, another area may be part of the basic array of somatosensory areas in mammals. PR may provide the major inputs to peripheral cortex, the relay to the hippocampus as way of creating somatosensory memories (Mishkin, 1979). S2 and PV also provide substantial inputs to primary motor cortex, M1 (Krubitzer et al., 1986).

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