Discharge properties of neurones in the hand area of primary somatosensory cortex in monkeys in relation to the performance of an active tactile discrimination task

Summary

The present experiments were designed to characterize the discharge patterns of single cortical neurones within the cutaneous representation of the hand in postcentral cortex (areas 3b and 1) in awake monkeys during the performance of an active tactile discrimination task. The task consisted of making a single scanning movement over a surface (first half smooth; second half smooth or rough); the texture encountered over the second half of the surface was indicated by the animal, respectively, pushing or pulling a lever. Unitary discharge was recorded from 118 cells receiving input from the hand or distal forearm of two monkeys. Units with cutaneous fields on the digit tips in contact with the surfaces to be discriminated showed an increase in discharge (58%), a decrease in discharge (11%) or no change (31%) during the task. Units with cutaneous fields not in contact with the discriminanda were much more likely to show decreased discharge during the task (25%), suggesting that there is some selection of cutaneous inputs in this task. Cutaneous units in areas 3b and 1 were equally likely to signal differences in texture (respectively, 18% and 26% of those with digital receptive fields (RFs)) and most of the texture-related units (78%) had a large RF, spanning several digits. The discharge patterns of single texture-related cells did not reliably signal whether or not the animal successfully discriminated the surfaces: unitary responses were occasionally absent even though the animal correctly identified the surface or they were present when an incorrect response was made. This observation suggested that information derived from a population of cells is required for the performance of the task, since no single cell's discharge contained sufficient information upon which the animal could base its behavioural response. A group of cells with digital RFs (24% of area 3b cells and 15 % of area 1 units) were classified as movement-related. Their discharge signalled precisely the onset and/or end of movement, and they were generally insensitive to the texture of the surfaces scanned. Such cells may serve as an independent source of information for primary somatosensory cortex related to the physical parameters of movement. Most cells with digital RFs were more responsive during active tactile discrimination than during passive movement of the digits over the surfaces (monkey no longer required to discriminate the surface texture). For area 3b units, peripheral factors (RF orientation, speed of movement) were likely responsible for this observation. For area 1 units, the situation was more complex: 26% of the area 1 units were only active during the active behavioural task, suggesting that such units may signal peripheral events, but in a context-dependent manner. This may be related to attention, although other factors were not ruled out in the present experiments. Finally, the depth of modulation in the task was almost always less than that produced by classical RF testing, suggesting that the tactile inputs generated during exploratory movements are subject to gating controls, as has been shown for other types of movements.