Physiological expression of olfactory discrimination rule learning balances whole-population modulation and circuit stability in the piriform cortex network

Luna Jammal, Ben Whalley, Sourav Ghosh, Raphael Lamrecht, Edi Barkai

Research output: Contribution to journalArticlepeer-review

Abstract

Once trained, rats are able to execute particularly difficult olfactory discrimination tasks with exceptional accuracy. Such skill acquisition, termed “rule learning”, is accompanied by a series of long-lasting modifications to three cellular properties which modulate pyramidal neuron activity in piriform cortex; intrinsic excitability, synaptic excitation, and synaptic inhibition. Here, we explore how these changes, which are seemingly contradictory at the single-cell level in terms of their effect on neuronal excitation, are manifested within the piriform cortical neuronal network to store the memory of the rule, while maintaining network stability. To this end, we monitored network activity via multisite extracellular recordings of field postsynaptic potentials (fPSPS) and with single-cell recordings of miniature inhibitory and excitatory synaptic events in piriform cortex slices. We show that although 5 days after rule learning the cortical network maintains its basic activity patterns, synaptic connectivity is strengthened specifically between spatially proximal cells. Moreover, while the enhancement of inhibitory and excitatory synaptic connectivity is nearly identical, strengthening of synaptic inhibition is equally distributed between neurons while synaptic excitation is particularly strengthened within a specific subgroup of cells. We suggest that memory for the acquired rule is stored mainly by strengthening excitatory synaptic connection between close pyramidal neurons and runaway synaptic activity arising from this change is prevented by a nonspecific enhancement of synaptic inhibition.

Original languageEnglish
Article numbere12830
JournalPhysiological Reports
Volume4
Issue number14
DOIs
StatePublished - 1 Jul 2016

Bibliographical note

Publisher Copyright:
© 2016 The Authors. Physiological Reports published by Wiley Periodicals, Inc. on behalf of the American Physiological Society and The Physiological Society.

Keywords

  • Brain slices
  • brain slices
  • lomg-term memory
  • piriofm cortex
  • synaptic plasticity

ASJC Scopus subject areas

  • Physiology (medical)
  • Physiology

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