Independent neural coding of reward and movement by pedunculopontine tegmental nucleus neurons in freely navigating rats

Abstract

Phasic firing of dopamine (DA) neurons in the ventral tegmental area (VTA) and substantia nigra (SN) is likely to be crucial for reward processing that guides learning. One of the key structures implicated in the regulation of this DA burst firing is the pedunculopontine tegmental nucleus (PPTg), which projects to both the VTA and SN. Different literatures suggest that the PPTg serves as a sensory‐gating area for DA cells or it regulates voluntary movement. This study recorded PPTg single‐unit activity as rats perform a spatial navigation task to examine the potential for both reward and movement contributions. PPTg cells showed significant changes in firing relative to reward acquisition, the velocity of movement across the maze and turning behaviors of the rats. Reward, but not movement, correlates were impacted by changes in context, and neither correlate type was affected by reward manipulations (e.g. changing the expected location of a reward). This suggests that the PPTg conjunctively codes both reward and behavioral information, and that the reward information is processed in a context‐dependent manner. The distinct anatomical distribution of reward and movement cells emphasizes different models of synaptic control by PPTg of DA burst firing in the VTA and SN. Relevant to both VTA and SN learning systems, however, PPTg appears to serve as a sensory gating mechanism to facilitate reinforcement learning, while at the same time provides reinforcement‐based guidance of ongoing goal‐directed behaviors.