Multiple representation in primate SI: A view from a window on the brain

This chapter summarizes recent findings regarding the functional organization of primary somatosensory cortex (SI) in primates when viewed through ‘windows’ on the brain with optical imaging methodologies. These views have confirmed previous knowledge regarding topographic organization in SI. They have also revealed the presence of functional domains for the processing of different sensory tactile modalities (pressure, flutter, and vibration domains). Surprisingly, the representation of these tactile modalities is quite distinct in organization from that of visual modalities (form, color, and depth) in visual cortex. Rather, tactile modality maps appear similar to visual orientation maps in primate visual cortex. Implications of these findings for the relationship of cortical organization to the sensory scene are discussed. List of Abbreviations: SI, primary somatosensory cortex; SII, second somatosensory area; PV, parietal ventral area; SA, slowly adapting; RA, rapidly adapting; PC, pacinian; VPL, ventral posterior lateral; VPI, ventroposterior inferior; CCD, charge coupled device; V1, primary visual cortex; V2, second visual area; V4, fourth visual area; IT, inferotemporal cortex 1 Functional Representation in Primary Somatosensory Cortex (SI) 1.1 Multiple Topographic Maps in SI Primate primary somatosensory cortex (SI) in the postcentral gyrus contains four complete topographic maps of the body surface that fall within the architectonically defined Brodmann’s Areas 3a, 3b, 1, and 2 (e.g., Woolsey et al., 1942; Powell and Mountcastle, 1959; Kaas et al., 1979; Nelson et al., 1980; Sur et al., 1982; Pons et al., 1985, 1987) > Figure 1‐1. Areas 3b and 1 receive input primarily from cutaneous afferents where areas 3a and 2 receive input from deep afferents (muscle spindles and joints) (e.g., Tanji and Wise, 1981). Other parietal areas, such as Areas 5 and 7, also process somatosensory information (Murray and Mishkin, 1984; Dong et al., 1994; Burton et al., 1997; Duhamel et al., 1998; Debowy et al., 2001). Somatotopic maps are also found laterally in second somatosensory area (SII) and the adjacent parietal ventral area (PV) (Burton and Fabri, 1995; Krubitzer et al., 1995) and there are other somatosensory areas in insular cortex that receive cutaneous and visceral information (Robinson and Burton, 1980; Schneider et al., 1993; Craig, 2003). 1.2 Hierarchical Relationship between Areas 3b and 1 Numerous studies suggest a hierarchical relationship between Area 3b and Area 1. Ablations of Area 3a and 3b leave Area 1 unresponsive, consistent with anatomy studies that show that Area 1 receives the bulk of its input from Area 3b. These findings suggest that direct thalamic inputs to Area 1 play either a weak or a modulatory role in cutaneous information processing (Garraghty et al., 1990). In comparison with cells of Area 1, response properties of cells in Area 3b can be described as relatively simple or closer to the physical aspects of the stimulus. Area 3b neurons (and layer 4 neurons in Area 1) have receptive fields confined to single‐digit tips; in contrast, Area 1 neurons recorded in supra‐ or infragranular layers integrate over larger areas of skin, often spanning multiple‐digit tips (Mountcastle and Powell, 1959; Hyvarinen and Poranen, 1978; Costanzo and Gardner, 1980; Iwamura et al., 1983; Sur et al., 1980, 1985). In concert with a greater degree of integration in Area 1, intrinsic connections within Area 1 are more extensive than those in Area 3b (Burton and Fabri, 1995). Both SA (slowly adapting) and RA (rapidly adapting) responsive cells are commonly found in Area 3b, whereas Area 1 is characterized by a predominance of RA cells and cells responsive to motion and orientation (Warren et al., 1986; Nelson et al., 1991). Although both mechareceptors and RA cells are responsive to textured surfaces, the firing patterns of slowly-adapting type I mechanoreceptors cells are more closely tied with roughness and texture features (Connor and Johnson, 1992; Blake et al., 1997). These findings could suggest a stronger role of Area 3b in fine spatial pattern 2 1 Multiple representation in primate SI: A view from a window on the brain