Distinct neural codes in primate hippocampus and lateral prefrontal cortex during associative learning in virtual environments

Benjamin W Corrigan; Roberto A Gulli; Guillaume Doucet; Megan Roussy; Rogelio Luna; Kartik S Pradeepan; Adam J Sachs; Julio C Martinez-Trujillo

doi:10.1016/j.neuron.2022.04.016

Distinct neural codes in primate hippocampus and lateral prefrontal cortex during associative learning in virtual environments

Neuron. 2022 Jul 6;110(13):2155-2169.e4. doi: 10.1016/j.neuron.2022.04.016. Epub 2022 May 12.

Authors

Benjamin W Corrigan¹, Roberto A Gulli², Guillaume Doucet³, Megan Roussy¹, Rogelio Luna⁴, Kartik S Pradeepan¹, Adam J Sachs³, Julio C Martinez-Trujillo⁵

Affiliations

¹ Department of Physiology and Pharmacology, University of Western Ontario, London, ON, Canada; Robarts Research Institute, University of Western Ontario, London, ON, Canada; Brain and Mind Institute, University of Western Ontario, London, ON, Canada.
² Zuckerman Mind Brain Behavior Institute, Columbia University, New York, NY, USA; Center for Theoretical Neuroscience, Columbia University, New York, NY, USA.
³ The Ottawa Hospital, University of Ottawa, Ottawa, ON, Canada.
⁴ Department of Physiology and Pharmacology, University of Western Ontario, London, ON, Canada; Robarts Research Institute, University of Western Ontario, London, ON, Canada.
⁵ Department of Physiology and Pharmacology, University of Western Ontario, London, ON, Canada; Robarts Research Institute, University of Western Ontario, London, ON, Canada; Brain and Mind Institute, University of Western Ontario, London, ON, Canada; Lawson Health Research Institute, London, ON, Canada. Electronic address: julio.martinez@robarts.ca.

PMID: 35561675
DOI: 10.1016/j.neuron.2022.04.016

Abstract

The hippocampus (HPC) and the lateral prefrontal cortex (LPFC) are two cortical areas of the primate brain deemed essential to cognition. Here, we hypothesized that the codes mediating neuronal communication in the HPC and LPFC microcircuits have distinctively evolved to serve plasticity and memory function at different spatiotemporal scales. We used a virtual reality task in which animals selected one of the two targets in the arms of the maze, according to a learned context-color rule. Our results show that during associative learning, HPC principal cells concentrate spikes in bursts, enabling temporal summation and fast synaptic plasticity in small populations of neurons and ultimately facilitating rapid encoding of associative memories. On the other hand, layer II/III LPFC pyramidal cells fire spikes more sparsely distributed over time. The latter would facilitate broadcasting of signals loaded in short-term memory across neuronal populations without necessarily triggering fast synaptic plasticity.

Keywords: burst firing; hippocampus; long-term memory; neural code; prefrontal cortex; primate; short-term memory; working memory.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
Hippocampus* / physiology
Memory, Short-Term / physiology
Prefrontal Cortex* / physiology
Primates
Pyramidal Cells / physiology

Grants and funding

CIHR/Canada