Prefrontal synaptic activation during hippocampal memory reactivation

Yuya Nishimura,Yuji Ikegaya,Takuya Sasaki

doi:10.1016/j.celrep.2021.108885

Abstract

Cooperative reactivation of hippocampal and prefrontal neurons is considered crucial for mnemonic processes. To directly record synaptic substances supporting the interregional interactions, we develop concurrent spike recordings of hippocampal neuronal ensembles and whole-cell patch-clamp recordings of medial prefrontal neurons in awake rats. We find that medial prefrontal neurons depolarize when hippocampal neurons synchronize. The depolarization in medial prefrontal neurons is larger when hippocampal place cells that encoded overlapping place fields and place cells that encoded a novel environment are synchronously reactivated. Our results suggest a functional circuit-synapse association that enables prefrontal neurons to read out specific memory traces from the hippocampus.

Highlights

A functional information transfer from the hippocampus (HPC) to the prefrontal cortex (PFC), via direct and indirect synaptic projections (Cenquizca and Swanson, 2007; Hoover and Vertes, 2007; Spellman et al, 2015), is pivotal to declarative memories (Eichenbaum, 2017; Tang and Jadhav, 2019)
A possible neurophysiological substrate for the HPC-PFC communication is the reactivation of HPC neuronal ensembles that encoded previously experienced behavioral trajectories (Joo and Frank, 2018; Lee and Wilson, 2002; Wilson and McNaughton, 1994), typically associated with sharp-wave ripples (SWRs), a high-frequency oscillation event (150–250 Hz) in local field potential (LFP) signals (Buzsaki, 2015)
For PFC neurons to efficiently read out information contents arising from the HPC, synchronized HPC cell ensemble patterns need to be properly transformed into synaptic inputs onto PFC neurons

Summary

Introduction

A functional information transfer from the hippocampus (HPC) to the prefrontal cortex (PFC), via direct and indirect synaptic projections (Cenquizca and Swanson, 2007; Hoover and Vertes, 2007; Spellman et al, 2015), is pivotal to declarative memories (Eichenbaum, 2017; Tang and Jadhav, 2019). The selective depolarization in a subset of PFC neurons determines whether they participate in HPCPFC coordinated activity Such neuronal inputs at a subthreshold level have not been directly measured, primarily owing to a lack of methodologies. To address this question, we simultaneously measured spike patterns of a HPC cell ensemble and a membrane potential of a medial PFC (mPFC) neuron from an awake rat by an integrated technique. While the ventral and intermediate HPC have been reported to more strongly project to the mPFC (Cenquizca and Swanson, 2007; Hoover and Vertes, 2007; Jay and Witter, 1991; Spellman et al, 2015) compared with the dorsal HPC, we recorded dorsal HPC neurons due to a technical limitation of recordings of sufficient numbers of HPC neuronal ensembles from the ventral and

Methods

Results

Discussion

Conclusion