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Differential recruitment of ventral pallidal e-types by behaviorally salient stimuli during Pavlovian conditioning.

ABSTRACT: The ventral pallidum (VP) is interfacing striatopallidal and limbic circuits, conveying information about salience and valence crucial to adjusting behavior. However, how VP neuron populations with distinct electrophysiological properties (e-types) represent these variables is not fully understood. Therefore, we trained mice on probabilistic Pavlovian conditioning while recording the activity of VP neurons. Many VP neurons responded to punishment (54%), reward (48%), and outcome-predicting auditory stimuli (32%), increasingly differentiating distinct outcome probabilities through learning. We identified e-types based on the presence of bursts or fast rhythmic discharges and found that non-bursting, non-rhythmic neurons were the most sensitive to reward and punishment. Some neurons exhibited distinct responses of their bursts and single spikes, suggesting a multiplexed coding scheme in the VP. Finally, we demonstrate synchronously firing neuron assemblies, particularly responsive to reinforcing stimuli. These results suggest that electrophysiologically defined e-types of the VP differentially participate in transmitting reinforcement signals during learning.

SUBMITTER: Hegedus P

PROVIDER: S-EPMC8066429 | biostudies-literature | 2021 Apr

REPOSITORIES: biostudies-literature

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Differential recruitment of ventral pallidal e-types by behaviorally salient stimuli during Pavlovian conditioning.

Hegedüs Panna P Heckenast Julia J Hangya Balázs B

iScience 20210331 4

The ventral pallidum (VP) is interfacing striatopallidal and limbic circuits, conveying information about salience and valence crucial to adjusting behavior. However, how VP neuron populations with distinct electrophysiological properties (e-types) represent these variables is not fully understood. Therefore, we trained mice on probabilistic Pavlovian conditioning while recording the activity of VP neurons. Many VP neurons responded to punishment (54%), reward (48%), and outcome-predicting audit ...[more]

PMID: 33912818

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Project description:The ventral pallidum (VP) mediates motivated behaviors largely via the action of VP GABA and glutamatergic neurons. In addition to these neuronal subtypes, there is a population of cholinergic projection neurons in the VP, whose functional significance remains unclear. To understand the functional role of VP cholinergic neurons, we first examined behavioral responses to an appetitive (APP) odor that elicited approach, and an aversive (AV) odor that led to avoidance. To examine how VP cholinergic neurons were engaged in APP vs. AV responses, we used an immediate early gene marker and in-vivo fiber photometry, examining the activation profile of VP cholinergic neurons in response to each odor. Exposure to each odor led to an increase in the number of cFos counts and increased calcium signaling of VP cholinergic neurons. Activity and cre-dependent viral vectors were designed to label engaged VP cholinergic neurons in two distinct contexts: (1) exposure to the APP odor, (2) followed by subsequent exposure to the AV odor, and vice versa. These studies revealed two distinct, non-overlapping subpopulations of VP cholinergic neurons: one activated in response to the APP odor, and a second distinct population activated in response to the AV odor. These two subpopulations of VP cholinergic neurons are spatially intermingled within the VP, but show differences in electrophysiological properties, neuronal morphology, and projections to the basolateral amygdala. Although VP cholinergic neurons are engaged in behavioral responses to each odor, VP cholinergic signaling is only required for approach behavior. Indeed, inhibition of VP cholinergic neurons not only blocks approach to the APP odor, but reverses the behavior, leading to active avoidance. Our results highlight the functional heterogeneity of cholinergic projection neurons within the VP. These two subpopulations of VP cholinergic neurons differentially encode valence of olfactory stimuli and play unique roles in approach and avoidance behaviors.

Project description:The interconnected nuclei of the ventral basal ganglia have long been identified as key regulators of motivated behavior, and dysfunction of this circuit is strongly implicated in mood and substance use disorders. The ventral pallidum (VP) is a central node of the ventral basal ganglia, and recent studies have revealed complex VP cellular heterogeneity and cell- and circuit-specific regulation of reward, aversion, motivation, and drug-seeking behaviors. Although the VP is canonically considered a relay and output structure for this circuit, emerging data indicate that the VP is a central hub in an extensive network for reward processing and the regulation of motivation that extends beyond classically defined basal ganglia borders. VP neurons respond temporally faster and show more advanced reward coding and prediction error processing than neurons in the upstream nucleus accumbens, and regulate the activity of the ventral mesencephalon dopamine system. This review will summarize recent findings in the literature and provide an update on the complex cellular heterogeneity and cell- and circuit-specific regulation of motivated behaviors and reinforcement by the VP with a specific focus on mood and substance use disorders. In addition, we will discuss mechanisms by which stress and drug exposure alter the functioning of the VP and produce susceptibility to neuropsychiatric disorders. Lastly, we will outline unanswered questions and identify future directions for studies necessary to further clarify the central role of VP neurons in the regulation of motivated behaviors. Significance: Research in the last decade has revealed a complex cell- and circuit-specific role for the VP in reward processing and the regulation of motivated behaviors. Novel insights obtained using cell- and circuit-specific interrogation strategies have led to a major shift in our understanding of this region. Here, we provide a comprehensive review of the VP in which we integrate novel findings with the existing literature and highlight the emerging role of the VP as a linchpin of the neural systems that regulate motivation, reward, and aversion. In addition, we discuss the dysfunction of the VP in animal models of neuropsychiatric disorders.

Dataset Information

Differential recruitment of ventral pallidal e-types by behaviorally salient stimuli during Pavlovian conditioning.

Publications

Differential recruitment of ventral pallidal e-types by behaviorally salient stimuli during Pavlovian conditioning.

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