Abstract
Non-overlapping cell populations within dorsomedial prefrontal cortex (dmPFC), defined by gene expression or projection target, control dissociable aspects of reward seeking through unique activity patterns. However, even within these defined cell populations, considerable cell-to-cell variability is found, suggesting that greater resolution is needed to understand information processing in dmPFC. Here, we use two-photon calcium imaging in awake, behaving mice to monitor the activity of dmPFC excitatory neurons throughout Pavlovian reward conditioning. We characterize five unique neuronal ensembles that each encodes specialized information related to a sucrose reward, reward-predictive cues, and behavioral responses to those cues. The ensembles differentially emerge across daily training sessions - and stabilize after learning - in a manner that improves the predictive validity of dmPFC activity dynamics for deciphering variables related to behavioral conditioning. Our results characterize the complex dmPFC neuronal ensemble dynamics that stably predict reward availability and initiation of conditioned reward seeking following cue-reward learning.
Highlights
The dorsomedial prefrontal cortex has garnered considerable interest due to its dysregulation in diseases associated with disordered reward processing (Chen et al, 2018; Courchesne et al, 2011; Dienel and Lewis, 2019; Holmes et al, 2018; Koob and Volkow, 2010; Ye et al, 2012)
A two-way ANOVA revealed a significant cue by session interaction for conditioned licking behavior (D lick rate; F1,47 = 165.1; p-value < 0.001), and post hoc tests confirmed that mice licked significantly more during conditioned stimuli (CS)+ trials during late in learning sessions as compared with CS- trials during both sessions (p-values < 0.001) and CS+ trials during early in learning sessions (p-value < 0.001)
Excitatory neuronal ensembles in dorsomedial prefrontal cortex (dmPFC) display specialized coding during reward seeking We find that dmPFC excitatory neuronal ensembles display unique activity patterns after developing Pavlovian conditioned behavioral responses, and that the relative proportion of neurons in each ensemble (Clusters 3 and 5) can predict behavioral task performance
Summary
The dorsomedial prefrontal cortex (dmPFC) has garnered considerable interest due to its dysregulation in diseases associated with disordered reward processing (Chen et al, 2018; Courchesne et al, 2011; Dienel and Lewis, 2019; Holmes et al, 2018; Koob and Volkow, 2010; Ye et al, 2012). We observe five unique neuronal ensembles after task acquisition that encode specialized information related to the sucrose reward, reward-predictive cues, and behavioral responses to those cues These five ensembles differentially emerge across days during learning in a manner that improves the predictive validity of dmPFC population dynamics for deciphering reward delivery, cue presentation, and behavior. These adaptations were specific to a reward-predictive cue, but not another neutral cue, suggesting that the identified neuronal activity patterns are likely related to associative learning. Our results highlight the importance of ensemble-specific recording and manipulation strategies for understanding the function of dmPFC activity for reward processing
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