Influence of attentive behavior on neuronal responses to vibration in primary somatosensory cortex of the monkey

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Abstract
The influence of systematic variation in attentive behavior on cellular responses to cutaneous vibratory stimuli was studied in the postcentral somatosensory area I [SI] of 3 stump-tailed monkeys (Macaca speciosa). The monkeys performed a task in which identical vibratory stimuli were presented on the receptive fields of cortical neurons under 2 different conditions. In the relevant condition the monkey could expect a juice reward for correct detection of the end of the vibration period, and in the irrelevant condition the monkey was never rewarded and thus did not respond to the stimulus. Extracellular microelectrode recordings were made during the monkey''s performance of the task with glass-coated platinum-iridium or tungsten electrodes using the transdural recording technique. A sample of 160 single neurons, including rapidly adapting skin neurons, Pacinian neurons, neurons activated from skin and muscle, and nonspecific neurons, were selected for this study. A histological reconstruction was done to localize each cell in the cytoarchitectural regions and in the cortical laminage of SI. The recordings were analyzed with a computer constructing peristimulus time (PST) histograms and cycle histograms of the action-potential responses evoked by vibration. The responses of most of the neurons studied did not vary with respect to the irrelevant and the relevant stimulus condition. In area 3b92% of the neurons studied showed no difference in the 2 conditions, whereas in area 1 the percentage was 78. A lack of sensitivity to changes in behavioral conditions appears to be a rule for most cells in SI and particularly in area 3b where the thalamic input is the most direct. The responses of 16% of the neurons studied were clearly affected by attentive behavior. The effect was always on augmentation of the relevant response in comparison with the irrelevant and it was observable mainly as an increase in the response level (impulses/s) in the PST histograms, but in some cells also as a greater degree of phase-locking to the stimulus since wave as revealed in the cycle histograms. A laminar analysis of the location of the cells studied showed that the effect of attentive behavior was fairly common in the few elements recorded at the junction of cortical layers I and II and in layer II (50 and 25% of the cells studied), very rare in the middle layers, and more common again in layer VI (22%). This distribution of the effect of attention in the layers is similar to the distribution of nonspecific afferents, noradrenergic terminals and nicotinic cholinergic receptors in the cortex. The dense fiber network in the superficial cortical layers appears to mediate generalized effects of attention into the cortical modules, which can be aroused simultaneously in great numbers through this route.