Abstract
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.
Highlights
The pedunculopontine tegmental nucleus (PPTN) is the major source of cholinergic projections in the midbrain, and contains glutamatergic, gamma aminobutyric acid (GABA)ergic, dopaminergic, and noradrenergic neurons (Mesulam et al, 1983; Rye et al, 1987; Clements and Grant, 1990; Jones, 1991; Spann and Grofova, 1992; Ford et al, 1995; Takakusaki et al, 1996; Wang and Morales, 2009)
Many PPTN neurons increase their tonic activity around the time of the initial target appearance, which was sustained until the end of the trial, and some of these neurons show predicted reward-related activity modulation (Okada et al, 2009)
We found that most PPTN neurons showed a tonic increase or decrease in activity during the task execution period, and the sign of tonic activity modulation was correlated with their response magnitude to large/small reward cues
Summary
The pedunculopontine tegmental nucleus (PPTN) is the major source of cholinergic projections in the midbrain, and contains glutamatergic, gamma aminobutyric acid (GABA)ergic, dopaminergic, and noradrenergic neurons (Mesulam et al, 1983; Rye et al, 1987; Clements and Grant, 1990; Jones, 1991; Spann and Grofova, 1992; Ford et al, 1995; Takakusaki et al, 1996; Wang and Morales, 2009). There are numerous studies showing that another neuromodulation system, i.e., dopaminergic neurons located in the substantia nigra pars compacta and ventral tegmental area, play an essential role in the regulation of motivated behavior by encoding a reward prediction error signal for reinforcement learning (Schultz, 1998; Bromberg-Martin et al, 2010b). Dopaminergic neurons exhibit phasic burst firing in response to external stimuli and rewards, and their response magnitude alters throughout the course of learning to match the reward prediction error signal (Hollerman and Schultz, 1998). It is possible that neurons in the PPTN encode the reward-related signals that are necessary for the computation of the reward prediction error signal by dopaminergic neurons
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