Orbitofrontal Cortex Signals Expected Outcomes with Predictive Codes When Stable Contingencies Promote the Integration of Reward History

Abstract

Memory can inform goal-directed behavior by linking current opportunities to past outcomes. The orbitofrontal cortex (OFC) may guide value-based responses by integrating the history of stimulus-reward associations into expected outcomes, representations of predicted hedonic value and quality. Alternatively, the OFC may rapidly compute flexible "online" reward predictions by associating stimuli with the latest outcome. OFC neurons develop predictive codes when rats learn to associate arbitrary stimuli with outcomes, but the extent to which predictive coding depends on most recent events and the integrated history of rewards is unclear. To investigate how reward history modulates OFC activity, we recorded OFC ensembles as rats performed spatial discriminations that differed only in the number of rewarded trials between goal reversals. The firing rate of single OFC neurons distinguished identical behaviors guided by different goals. When Ͼ20 rewarded trials separated goal switches, OFC ensembles developed stable and anticorrelated population vectors that predicted overall choice accuracy and the goal selected in single trials. When Ͻ10 rewarded trials separated goal switches, OFC population vectors decorrelated rapidly after each switch, but did not develop anticorrelated firing patterns or predict choice accuracy. The results show that, whereas OFC signals respond rapidly to contingency changes, they predict choices only when reward history is relatively stable, suggesting that consecutive rewarded episodes are needed for OFC computations that integrate reward history into expected outcomes.

Sucrose intensity coding and decision-making in rat gustatory cortices

“…Lesioning the OFC disrupts performance in an allocentric foraging task (Corwin et al, 1994), and radial arm and Morris water maze (Kolb et al, 1983). Moreover, the OFC also encodes head angle, spatial trajectory and movement speed in a spatial discrimination and reversal task in a plus maze (Riceberg and Shapiro, 2017). The latter evidence agrees with the high proportion of OFC Direction-selective neurons that we identified ( Fig 6).…”

Medial Prefrontal Cortex Reduces Memory Interference by Modifying Hippocampal Encoding

“…However, calculation of the required N’s is difficult when true effect sizes are unknown, as was the case with these experiments. We selected N’s based on our previous experience using within-subjects behavioral (e.g., Rich and Shapiro, 2009; Young and Shapiro, 2009)) and recording studies (e.g., (Riceberg and Shapiro, 2017)).…”

Prospective Representations in Rat Orbitofrontal Ensembles

“…Meanwhile, the past sensory cues, rewards, spatial directions, and behavioral choices are also reported to be reflected in the OFC neural activities (Feierstein, Quirk, Uchida, Sosulski, & Mainen, 2006;Kennerley, Behrens, & Wallis, 2011;Nogueira et al, 2017;Riceberg & Shapiro, 2017;Saez, Saez, Paton, Lau, & Salzman, 2017;Young & Shapiro, 2011;Zhou, Jia, Feng, Bao, & Luo, 2015). Such findings have been taken as evidence that the OFC, together with contributions from other interconnected brain regions such as the hippocampus, might provide a neural mechanism with which animals could mentally travel through a task model in time and recall the past events and simulate future outcomes (Behrens et al, 2018;Wang, Schoenbaum, & Kahnt, 2020;Wikenheiser & Schoenbaum, 2016; R. C. Wilson, Takahashi, Schoenbaum, & Niv, 2014).…”