Reward prediction-related increases and decreases in tonic neuronal activity of the pedunculopontine tegmental nucleus

The neuromodulators serotonin, acetylcholine, and dopamine have been proposed to play important roles in the execution of movement, control of several forms of attentional behavior, and reinforcement learning. While the response pattern of midbrain dopaminergic neurons and its specific role in reinforcement learning have been revealed, the roles of the other neuromodulators remain elusive. Reportedly, neurons in the dorsal raphe nucleus, one major source of serotonin, continually track the state of expectation of future rewards by showing a correlated response to the start of a behavioral task, reward cue presentation, and reward delivery. Here, we show that neurons in the pedunculopontine tegmental nucleus (PPTN), one major source of acetylcholine, showed similar encoding of the expectation of future rewards by a systematic increase or decrease in tonic activity. We recorded and analyzed PPTN neuronal activity in monkeys during a reward conditioned visually guided saccade task. The firing patterns of many PPTN neurons were tonically increased or decreased throughout the task period. The tonic activity pattern of neurons was correlated with their encoding of the predicted reward value; neurons exhibiting an increase or decrease in tonic activity showed higher or lower activity in the large reward-predicted trials, respectively. Tonic activity and reward-related modulation ended around the time of reward delivery. Additionally, some tonic changes in activity started prior to the appearance of the initial stimulus, and were related to the anticipatory fixational behavior. A partially overlapping population of neurons showed both the initial anticipatory response and subsequent predicted reward value-dependent activity modulation by their systematic increase or decrease of tonic activity. These bi-directional reward- and anticipatory behavior-related modulation patterns are suitable for the presumed role of the PPTN in reward processing and motivational control.