Functional properties of primate putamen neurons during the categorization of tactile stimuli

We used psychometric techniques and neurophysiological recordings to study the role of the putamen in somesthetic perception. Four monkeys were trained to categorize the speed of moving tactile stimuli. Animals performed a task in which one of two target switches had to be pressed with the right hand to indicate whether the speed of probe movement across the glabrous skin of the left, restrained hand was low or high. During the task we recorded the activity of neurons in the putamen contralateral (right) and ipsilateral (left) to the stimulated hand. We found different types of neuronal responses, all present in the right and left putamen. Some neurons responded during the stimulus period, others responded during the hand-arm movement used to indicate categorization, and others responded during both of these periods. The responses of many neurons did not vary either with the speed of the stimuli or in relation to the categorization process. In contrast, neurons of a particular type responded differentially: their activity reflected whether stimulus speed was low or high. These differential responses occurred during the stimulus and hand-arm motion periods. A number of the nondifferential and differential neurons were studied when the same stimuli used in the categorization task were delivered passively. Few neurons with nondifferential discharges, and none of the differential neurons, responded in this condition. In a visually cued control task we studied the possibility that the differential responses were associated with the intention to press or with the trajectory of the hand to one of the target switches. In this condition, a light turned on instructed the animal which target switch to press for a reward. Very few neurons in both hemispheres maintained the differential responses observed during the categorization task. Those neurons that discharged selectively for low or high speeds were analyzed quantitatively to produce a measure comparable with the psychometric function. The thresholds of the resulting neurometric curves for the neuronal populations were very similar to the psychometric thresholds. The activity of a large fraction of these neurons could be used to accurately predict whether the stimulus speed was low or high. The results indicate that the putamen, both contralateral and ipsilateral to the stimulated hand, contains neurons that discharge in response to the somesthetic stimuli during the categorization task. Those neurons that respond irrespective of the stimulus speed appear to be involved in the general sensorimotor behavior of the animal during the execution of the task. The results suggest that the putamen may play a role in bimanual tasks. The recording of neurons in the right and left putamen whose activities correlate with the speed categories suggests that this region of the basal ganglia, in addition to its role in motor functions, is also involved in the animal's decision process.