Effects of a Cross-Modal Manipulation of Attention on Somatosensory Cortical Neuronal Responses to Tactile Stimuli in the Monkey

Abstract

The role of attention in modulating tactile sensitivity in primary (SI) and secondary somatosensory cortex (SII) was addressed using a cross-modal manipulation of attention, somatosensory versus visual. Two adult monkeys (Macaca mulatta) were trained to perform two tasks: tactile discrimination of a change in the texture of a surface presented to digits 3 and 4 and visual discrimination of a change in the intensity of a light. In each trial, standard texture (2 mm spatial period, SP) and visual stimuli were presented. These were followed by an increase in SP and/or luminance. Each trial was preceded by an instruction cue (colored light) that directed the animal to attend and respond to the change in one modality while ignoring any change in the other modality. The two tasks were interleaved during the recording, on a trial-by-trial basis. Extracellular recordings were made from 178 neurons (SI, 102; SII, 76), all with a cutaneous receptive field on the stimulated digit tips. Discharge was quantified in both tasks during the instruction, the standard-stimuli, and the texture-change periods. The results showed that selective attention to tactile stimuli had qualitatively and quantitatively greater and earlier effects in SII than SI. Twenty-four of 102 SI cells showed a significant change in discharge with the direction of attention. For almost all cells (20/24), discharge was enhanced when attention was directed toward the tactile stimuli; the effects were most frequent in the analysis interval that encompassed the change in SP (16/24). A significantly higher proportion of SII cells were attention-sensitive (47/76). The effects were concentrated in the texture-change period (39/47) but also included earlier periods in the trial (instruction period, n = 15; standard-stimuli period, n = 32). Attention-related modulation that spanned all three intervals (n = 11) likely reflected baseline changes in discharge. For the texture-sensitive cells (43 in SI, 37 in SII), the mean change in discharge frequency (post texture change - pre-texture change) in each task was significantly increased in SII but not SI with selective attention. The results are consistent with a two-stage modulation of parietal cortical discharge, an initial stage (SI) in which there is some enhancement of sensory responses to the salient feature, the texture change, and a second stage (SII) in which baseline changes occur, along with further feature selection. These controls may be independently exerted on SI and SII, or they may reflect top-down controls from SII to SI.

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