Dynamics of prelimbic cortex activity encode the predictive value of reward-associated cues

QUAVE, C.B.; AQUINO-MIRANDA, G.; ALBERT, R.; CHIDOMERE, C.; BORA, E.; CATTANI, M.; FERNANDEZ LEON, JOSE A.; ENGELKE, D.S.; DO-MONTE, F.H.

Conferencia; 2021 SfN Neuroscience; 2021

Behavioral adaptation to shifts in food availability is critical for maintaining efficiency during foraging. Neurons in the prelimbic prefrontal cortex (PL) display changes in firing rates in response to food-associated cues. However, it is unknown whether PL activity encodes fast changes in food availability (e.g. reward omission). We hypothesized that PL neurons show modified responses to reward availability and associated cues according to variations in reward predictability. Male Long-Evans rats implanted with a single-unit electrode in PL were trained to press a lever to obtain a reward (single sucrose pellet) in a nearby dish. Reward availability was limited to the duration of 15-second audiovisual cues. Rats were then subjected to an intercalated omission session (20 rewarded and 20 omitted trials semi-randomly interspersed) followed by a repeated omission session (18 rewarded followed by 20 omitted trials) to compare the neuronal correlates of unexpected vs. expected reward omission, respectively. PL firing rates were analyzed during both the onset of cues and when the animal’s head entered the dish after cued lever presses. During unexpected reward omission, rats exhibited “frustrative behaviors” characterized by higher lever press rate, greater number of burst presses, and increased locomotion speed (ANY-Maze automated video tracking system). However, these behaviors were not observed when reward omission was expected. Recordings from PL neurons (n = 233 cells from 16 rats) revealed a subset of cells that altered their firing rates (16% excited, 14% inhibited) when rats detected the presence of reward in the dish. Interestingly, 58% of these cells did not respond when reward was omitted, suggesting that PL neurons encode loss of a previously available reward. During expected reward omission, a subset of cells emerged exhibiting increased firing rates exclusively upon repeated detection of reward omission (8%), indicating that some PL neurons are recruited when reward omission becomes predictable. In addition, 13% of PL cells showed reductions in firing rates upon repeated reward cue presentation, half of which did not respond to repeated omission cues. It is possible that this progressive loss of inhibition in PL neurons may encode the reduced predictive value of cues when reward omission becomes an expected outcome. Together, our findings suggest that separate populations of PL neurons signal immediate vs. persistent reward loss and that real-time updating of PL activity is associated with dynamic changes in the predictive value of reward cues.