Reward-Based Learning Drives Rapid Sensory Signals in Medial Prefrontal Cortex and Dorsal Hippocampus Necessary for Goal-Directed Behavior

Pierre Le Merre,Vahid Esmaeili,Eloïse Charrière,Katia Galan,Paul-A Salin,Carl C.H Petersen,Sylvain Crochet

doi:10.1016/j.neuron.2017.11.031

Pierre Le Merre, Vahid Esmaeili + Show 5 more

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https://doi.org/10.1016/j.neuron.2017.11.031

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Abstract

SummaryThe neural circuits underlying learning and execution of goal-directed behaviors remain to be determined. Here, through electrophysiological recordings, we investigated fast sensory processing across multiple cortical areas as mice learned to lick a reward spout in response to a brief deflection of a single whisker. Sensory-evoked signals were absent from medial prefrontal cortex and dorsal hippocampus in naive mice, but developed with task learning and correlated with behavioral performance in mice trained in the detection task. The sensory responses in medial prefrontal cortex and dorsal hippocampus occurred with short latencies of less than 50 ms after whisker deflection. Pharmacological and optogenetic inactivation of medial prefrontal cortex or dorsal hippocampus impaired behavioral performance. Neuronal activity in medial prefrontal cortex and dorsal hippocampus thus appears to contribute directly to task performance, perhaps providing top-down control of learned, context-dependent transformation of sensory input into goal-directed motor output.

Highlights

The neural circuits involved in transforming relevant sensory information into goal-directed motor output are poorly understood
Water-restricted mice were rewarded with a drop of water if they licked a spout within the 1 s reward window that immediately followed a brief single-whisker deflection
Comparing the sensory-evoked response at the beginning (D1) and after 5–10 days of neutral exposure (Exposed), we found no significant difference in the peak amplitude across the recorded areas, except for a slight, but significant, increase of the response in parietal area (PtA) (Wilcoxon signed-rank test, D1 versus Exposed: p = 0.047)

Summary

Introduction

The neural circuits involved in transforming relevant sensory information into goal-directed motor output are poorly understood. In the absence of engagement in a behavioral task or even under anesthesia, sensory stimuli drive neural activity in multiple brain areas through innate feedforward signaling pathways. This first level of cortical sensory processing occurs predominantly in primary and secondary sensory areas, and in related motor areas. The transformation of external sensory signals into learned motor output appears to occur across a large network of brain areas that include sensory and motor neocortex, as well as associative and higher-order areas (Romo and de Lafuente 2013; Guo et al, 2014; Siegel et al, 2015). Among the associative and higher-order areas, the associative parietal area (PtA), the medial prefrontal cortex (mPFC), and the dorsal CA1 region of the hippocampus (dCA1) have been found to be implicated in different goal-directed behaviors in rodents, including contextual and spatial memory (Benchenane et al, 2010; Harvey et al, 2012; Place et al, 2016), multisensory integration (Song et al, 2017; Aronov et al, 2017; Terada et al, 2017), and sensory detection (Pinto and Dan, 2015; Otis et al, 2017) or discrimination (Pereira et al, 2007; Itskov et al, 2011)

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