Offline orbitofrontal cortex reactivation depends on recency of place-reward changes and coheres with hippocampal replay
Silviu I. Rusu,
Jeroen J. Bos,
Pietro Marchesi,
Jan V. Lankelma,
Ildefonso Ferreira Pica,
Luc J. Gentet,
Marian Joëls,
Cyriel Pennartz
Affiliations
Silviu I. Rusu
Cognitive and Systems Neuroscience Group, SILS Center for Neuroscience, University of Amsterdam, Amsterdam, the Netherlands; Research Priority Program Brain and Cognition, University of Amsterdam, Amsterdam, the Netherlands; Department Translational Neuroscience, University Medical Center Utrecht, Utrecht, the Netherlands; School of Physiology, Pharmacology and Neuroscience, University of Bristol, Biomedical Sciences Building, University Walk, Bristol BS8 1TD, UK; Corresponding author
Jeroen J. Bos
Cognitive and Systems Neuroscience Group, SILS Center for Neuroscience, University of Amsterdam, Amsterdam, the Netherlands
Pietro Marchesi
Cognitive and Systems Neuroscience Group, SILS Center for Neuroscience, University of Amsterdam, Amsterdam, the Netherlands; Research Priority Program Brain and Cognition, University of Amsterdam, Amsterdam, the Netherlands
Jan V. Lankelma
Cognitive and Systems Neuroscience Group, SILS Center for Neuroscience, University of Amsterdam, Amsterdam, the Netherlands
Ildefonso Ferreira Pica
Cognitive and Systems Neuroscience Group, SILS Center for Neuroscience, University of Amsterdam, Amsterdam, the Netherlands
Luc J. Gentet
Cognitive and Systems Neuroscience Group, SILS Center for Neuroscience, University of Amsterdam, Amsterdam, the Netherlands
Marian Joëls
Department Translational Neuroscience, University Medical Center Utrecht, Utrecht, the Netherlands; University of Groningen, University Medical Center Groningen, 9713 GZ Groningen, the Netherlands
Cyriel Pennartz
Cognitive and Systems Neuroscience Group, SILS Center for Neuroscience, University of Amsterdam, Amsterdam, the Netherlands; Research Priority Program Brain and Cognition, University of Amsterdam, Amsterdam, the Netherlands; Corresponding author
Summary: The orbitofrontal cortex, one of the key neocortical areas in valuation and emotion, is critical for cognitive flexibility but its role in the consolidation of recently acquired information remains unclear. Here, we demonstrate orbitofrontal offline replay in the context of a place-reward association task on a maze with varying goal locations. When switches in place-reward coupling were applied, replay was enhanced relative to sessions with stable contingencies. Moreover, replay strength was positively correlated with the subsequent overnight change in behavioral performance. Interrogating relationships between orbitofrontal and hippocampal activity, we found that orbitofrontal and hippocampal replay could occur independently but became coordinated during a type of cortical state with strong spiking activity. These findings reveal a structured form of offline orbitofrontal ensemble activity that is correlated with cognitive flexibility required to adapt to changing task contingencies, and becomes associated with hippocampal replay only during a specific state of high cortical excitability.
