RAPID COMMUNICATION Neuronal Encoding of Texture Changes in the Primary and the Secondary Somatosensory Cortical Areas of Monkeys During Passive Texture Discrimination

Jiang, Wan, François Tremblay, and C. Elaine Chapman. Neusmooth and rough surfaces (raised Braille dots) (Ageraniotironal encoding of texture changes in the primary and the secondary Bélanger and Chapman 1992; Chapman and Ageranioti-Bésomatosensory cortical areas of monkeys during passive texture langer 1991) or between varying degrees of roughness prodiscrimination. J. Neurophysiol. 77: 1656–1662, 1997. Two rhesus vided by periodic gratings with spatial periods (SPs) ranging monkeys were trained to discriminate, with the use of passive from 0.75 to 3.15 mm (Darian-Smith et al. 1982; Sinclair touch, a standard surface [rectangular arrays of raised dots with a and Burton 1991, 1993). In the studies of Sinclair and Burspatial period (SP) of 2 mm across the rows and columns] from ton, texture-related neurons in both SI and SII showed graded three modified surfaces in which the SP between rows was inchanges in mean discharge frequency in response to the creased to 3, 4, or 5 mm over the second half of the surface. After periodic gratings, suggesting that an intensive code, based the surface presentation (to digit tips 3 and 4 of one hand) the monkeys indicated the presence or absence of a change in texture on mean firing rate, might underlie the central representation by pulling or pushing a lever, respectively, with the opposite hand. of texture in both areas. Of 193 neurons recorded from primary somatosensory cortex (SI, We report here a novel difference in the texture sensitivity 3 hemispheres) and 94 neurons from secondary somatosensory of SI and SII neurons in monkeys trained to discriminate cortex (SII, 1 hemisphere) , all contralateral to the stimulated hand, the presence or absence of a change in surface roughness, the discharge of 51 SI and 19 SII neurons was classified as texture produced by incrementing the SP of rectangular arrays of related. Two types of texture-related responses were obtained. raised dots over one dimension (range: 2–5 mm). SI neurons Graded neurons showed a linear relationship between mean disshowed a graded change in discharge when SP was incharge frequency and SP; nongraded neurons showed a significant creased; in contrast, SII neurons showed a nongraded change change in discharge over the modified half of the surfaces but the in discharge, i.e., their discharge signaled the presence of a discharge did not distinguish between the three modified surfaces. The distribution of these texture responses was significantly differchange in texture, but not its magnitude. Preliminary results ent in SI and SII: whereas most of the texture-related neurons in have been published in abstract form (Chapman et al. 1995; SI (44 of 51, 86%) were graded, the majority of those in SII Jiang and Chapman 1994). (12 of 19, 63%) were nongraded. The results were interpreted as suggesting that the nongraded responses reflect feature extraction in SII, signaling the presence of a change in texture but not its M E T H O D S magnitude, and so support the notion that texture signals are proTwo adult monkeys (Macaca mulatta) (monkey F, 8.7 kg; moncessed sequentially, first in SI and then in SII. key H, 6.0 kg) were trained to perform a passive texture discrimination task. The animal preparation and the behavioral task have been described elsewhere (Tremblay et al. 1996). Briefly, the monI N T R O D U C T I O N key was seated in a primate chair with the behavioral apparatus Several parietal cortical areas, including the primary and mounted in front of the animal, at waist height, and firmly clamped the secondary somatosensory cortical areas (SI and SII, reto the chair. The monkey was trained to discriminate changes in spectively) , are known to play important roles in the ability the texture of nylon polymer surfaces mounted on a drum (tactile to appreciate surface texture with the use of touch. Texture stimulator) that was in turn rotated, under computer control, underneath the digit tips of the monkey (Fig. 1B) . The animal was discrimination in the monkey is seriously impaired after leconditioned to rest one hand on the surface of the apparatus, placing sions of areas 3b, 1, and SII (Carlson 1981; Murray and the third and fourth digit tips on the textured surface that formed Mishkin 1984; Randolph and Semmes 1974; Ridley and Etthe floor of a small aperture over the drum (1.8 1 1.8 cm) tlinger 1976). Texture discrimination thresholds are also (Fig. 1C) . elevated after area 2 lesions (Randolph and Semmes 1974). The surfaces were fabricated from photographically reduced In agreement with the results of lesion studies, single-unit computer graphics photoetched onto a flexible letterpress plate with recordings have shown that neurons in both SI, including the use of an ultraviolet polymerization technique. Four different areas 3b, 1 and 2, and SII of monkeys signal differences textured surfaces (dimensions 20 1 100 mm) were employed (Fig. in texture explored with the use of active touch. Neuronal 1D) . One half of each surface (50 mm) had a standard texture discharge in both SI and SII varies as a function of the consisting of a rectangular array of raised dots (0.8 mm diam, 1 mm high) with a center-to-center distance of 2 mm between the explored texture, signaling differences either between