Different Pedunculopontine Tegmental Neurons Signal Predicted and Actual Task Rewards

Abstract

The dopamine system has been implicated in guiding behavior based on rewards. The pedunculopontine tegmental nucleus (PPTN) of the brainstem receives afferent inputs from reward-related structures, including the cerebral cortices and the basal ganglia, and in turn provides strong excitatory projections to dopamine neurons. This anatomical evidence predicts that PPTN neurons may carry reward information. To elucidate the functional role of the PPTN in reward-seeking behavior, we recorded single PPTN neurons while monkeys performed a visually guided saccade task in which the predicted reward value was informed by the shape of the fixation target. Two distinct groups of neurons, fixation target (FT) and reward delivery (RD) neurons, carried reward information. The activity of FT neurons persisted between FT onset and reward delivery, with the level of activity associated with the magnitude of the expected reward. RD neurons discharged phasically after reward delivery, with the levels of activity associated with the actual reward. These results suggest that separate populations of PPTN neurons signal predicted and actual reward values, both of which are necessary for the computation of reward prediction error as represented by dopamine neurons.

Reward Prediction Error Computation in the Pedunculopontine Tegmental Nucleus Neurons

“…Thus, the ROC analysis reinforced the idea that the fixation target neurons convey information about the magnitude of the predicted reward during the cue and working memory periods as well as up to and beyond the time of reward delivery and the reward delivery neurons convey information about the magnitude of the current reward only after it has been delivered. The free reward paradigm experiment also supports this view (Okada et al, 2009). …”

“…The excitatory transients impinge on the dopamine neurons in the absence of neuronal reward delivery signals, producing a sharp cue response, while upon reward delivery, the inhibitory transients are summed with the excitatory actual reward signals for computation of the reward prediction error, producing no response when the reward prediction matches with the actual one Fiorillo et al, 2008). In our recent study, the fixation target responses in the PPTN do not primarily explain this inhibitory omission response of the dopamine neurons, as the responses of the majority of the fixation target neurons were shutdown at the actual, rather than the expected, reward delivery timing in the temporal reward omission experiments (Okada et al, 2009). Therefore, they would feed the inhibitory transients to the dopamine neurons through the temporal difference mechanism, at the time of the actual rather than the expected reward.…”

“…In the PPTN, we observed transient reward responses for free reward and reward during the two-valued reward task (Okada et al, 2009). The reward delivery neurons may receive the actual reward signals from the lateral hypothalamus (Rolls et al, 1980;Fukuda et al, 1986;.…”

“…We hypothesized that the task performance-related neurons signal the reward prediction and the reward delivery-related neurons signal the reward outcome. This hypothesis was tested in monkeys by studying the activity of PPTN neurons during visually guided saccade tasks that were rewarded with different amonts of juice that were cued by the shape of the fixation target (Okada et al, 2009). 3. Responses of PPTN neurons to different reward magnitude 3.1 Effect of reward prediction on behavior and neuronal activity of PPTN In this study, Japanese monkeys were trained on a visually guided saccade task that required them to maintain fixation on a central fixation target, and to make a horizontal saccade to a peripheral saccade target that was presented after the disappearance of the fixation target (Fig.…”

“…Figures were modified from our recent paper (Okada et al, 2009). drops of juice; the amount (large or small) being cued at the outset by the shape of the initial central fixation target (square or circle, respectively).…”