Dopamine neurons of the monkey midbrain: contingencies of responses to active touch during self-initiated arm movements

Abstract

1. Previous studies have shown that midbrain dopamine (DA) neurons in monkeys respond to external stimuli that are used to initiate behavioral reactions. In the present study, we investigated to what extent changes in neuronal activity would occur when behavioral acts are generated internally or whether they would depend solely on external stimuli. 2. Monkeys performed self-initiated arm movements from a resting key into a covered, food-containing box at a self-chosen moment and without external preparatory or triggering signals. In a second task, the arm movement was triggered by rapid opening of the door of the food box. This stimulus was either audible and visible or only audible to the animal. Impulses of DA neurons were recorded with movable microelectrodes from the pars compacta of substantia nigra (area A9) and areas A8 and A10 and were discriminated from those of other neurons by their long duration (1.5-5.0 ms) and low spontaneous frequency (0.5-8.5 imp/s). 3. The activity of 12% of 104 DA neurons increased slowly and moderately up to 1,500 ms before the onset of individual self-initiated arm movements. Median increases amounted to 91% over background discharge rate. A further 16% of DA neurons were activated together with the onset of muscle activity and during the movement. 4. During self-initiated movements, a nonhabituating, phasic burst of impulses occurred when the monkey's hand touched a morsel of food inside the box. This response was seen in 84% of 154 neurons on the contralateral side, with median onset latency of 65 ms and duration of 160 ms. A comparable percentage of neurons responded to ipsilateral touch with similar latency and duration. 5. The touch response during self-initiated movements was absent, both on the contra- and ipsilateral sides, when the animal's hand touched the bare wire normally holding the food, when touching nonfood objects, or during tactile exploration of the empty interior of the food box. Thus responses appeared to be related to the appetitive properties of the object being touched rather than the object itself. 6. In the task employing stimulus-triggered movements, 77% of 86 DA neurons discharged a burst of impulses in response to door opening but entirely failed to respond to the touch of food in the box. The response to door opening in this task was similar to the touch response during self-initiated movements in the same neurons in terms of latency, duration, and magnitude.(ABSTRACT TRUNCATED AT 400 WORDS)