Non-bursting non-rhythmic neurons of the ventral pallidum form cell assemblies and respond to reward and punishment during Pavlovian conditioning

Abstract The ventral pallidum (VP) is a major hub interfacing striatopallidal and limbic circuits, conveying information about salience and valence crucial to adjusting behavior. However, how neuron populations of the VP with different firing properties represent these variables is not fully understood. Therefore, we trained mice on auditory Pavlovian conditioning and recorded the activity of VP neurons while mice were performing the task. Many VP neurons responded to punishment (51%) and reward (44%), either by firing rate increase or decrease. Additionally, 20% of cells responded to outcome-predicting auditory stimuli, showing larger responses to reward-predicting cues compared to those that signaled likely punishment. We found that a large subset of VP neurons showed burst firing based on their auto-correlograms, while a small population exhibited fast rhythmic discharge in the beta/gamma frequency range. Some bursting neurons exhibited distinct response properties of their bursts and single spikes, suggesting a multiplexed coding scheme in the VP. However, non-bursting, non-rhythmic neurons were the most sensitive to reward and punishment. Finally, we demonstrate the presence of synchronously firing neuron assemblies in the VP. Neurons participating in such assemblies were particularly responsive to reinforcing stimuli. This suggests that a synchronous, non-bursting, non-rhythmic neuron population of the VP is responsible for the lion’s share of ventral pallidal salience representation, likely important for reinforcement learning. Significance statement The ventral pallidum (VP) is a subcortical brain area that participates in regulating motion and emotion by processing information related to appetitive and aversive stimuli. However, how these stimuli are represented by VP neural circuits is not well understood. Therefore, we investigated how VP neuron populations defined by their firing properties respond to reward and punishment during Pavlovian conditioning. We found that a distinct, non-bursting-non-rhythmic group of neurons was responsible for most responses to reward and punishment in the VP. Neurons of this group formed co-active cell assemblies and multiplexed different types of information via different firing patterns, revealing flexible and plastic neuronal representation strategies in the VP during associative learning.