Activity of tonically active neurons in the monkey putamen during initiation and withholding of movement

Tonically active neurons (TANs) of the primate striatum are putative interneurons that respond to events of motivational significance, such as primary rewards, and to sensory stimuli that predict such events. Because TANs influence striatal projection neurons, TANs may play a role in the initiation and control of movement. To examine this issue, we recorded from putaminal TANs in macaque monkeys trained to make the same arm movement in two ways--in reaction to an external cue and also after a variable delay without an explicit instruction to move (self-timed movements). On other trials, the animals had to withhold movement following an external cue. The task design ensured that the three types of trials were effectively randomly interleaved, equally frequent, and similar in overall timing. Separately, we presented "playback" trials in which the same sequence of visual stimulation and reward was presented while the animals fixated without making the arm movement. We found that TAN responses were strongly affected by behavioral context. In particular, TAN responses were strikingly stronger when the animals actively withheld movements than on the corresponding playback trials, even though the stimulus sequence and reward timing were identical and no movement was made in either case. Many TANs also became active in the absence of a proximate sensory cue on self-timed movements, suggesting that TANs may reflect internal processes that are specific to self-timed movements. These results suggest that TANs may directly participate in, or monitor the motivational significance of, an animal's actions as well as external events.