Responses of striatal neurons in the behaving monkey. 1. Head of the caudate nucleus

Abstract The activity of 394 neurons in the head of the caudate nucleus and the most anterior part of the putamen was analyzed in 3 behaving rhesus monkeys in order to analyze the functions of this part of the striatum. Of these neurons, 64.2% responded in the tests used in relation to, for example, environmental events, movements made by the monkey, the performance of a visual discrimination, or during feeding. However, only relatively small proportions of these neurons had responses which were unconditionally related to visual (9.6%), auditory (3.5%), or gustatory (0.5%) stimuli, or to movements (4.1%). Instead, the majority of the responsive neurons had activity in relation to stimuli or movements which was conditional, in that the responses occurred in only some test situations, and were often dependent on the performance of a task by the monkeys. Thus, it was found in the visual discrimination task that 14.5% of the neurons responded during a 0.5 sec tone/light cue period which signalled the start of each trial; 31.1% responded in the period in which the discriminative visual stimuli were shown, with 24.3% of these responding more to either the visual stimulus which signified food reward or to that which signified punishment; and 6.2% responded in relation to lick responses. Yet these neurons typically did not respond in relation to the cue stimuli, to the visual stimuli, or to movements, when these occurred independently of the task, or when performance of the task was prevented. Comparably, of the neurons tested during feeding, 25.8% responded when the food was seen by the monkey, 6.2% when he tasted it, and 22.4% during a cue given by the experimenter that a food or non-food object was about to be presented. However, only few of these neurons had responses to the same stimuli presented in different situations. It is concluded that many neurons in the head of the caudate nucleus and the most anterior part of the putamen respond in relation to events which are used as cues to prepare for the performance of tasks, including feeding, in which movements must be initiated. Other neurons respond in relation to the stimuli used and the movements made in these tasks. However, the majority of these neurons do not have unconditional sensory or motor responses. It is therefore suggested that the anterior neostriatum contains neuronal mechanisms which are important in the process by which environmental cues are used in the preparation of behavioral responses, and in the initiation of particular behavioral responses made in particular situations to particular environmental stimuli. Deficits in the initiation of movements following damage to striatal pathways may arise in part because of interference with these functions of the anterior neostriatum.