title: Physiological expression of olfactory discrimination rule learning balances whole-population modulation and circuit stability in the piriform cortex network.
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.
authors.affiliation: Sagol department of Neurobiology, Faculty of Natural Sciences, University of Haifa, Haifa, Israel.
authors.forename: Luna
authors.initials: L
authors.lastname: Jammal
authors.affiliation: School of Chemistry, Food & Nutritional Sciences and Pharmacy, The University of Reading, Reading, UK.
authors.forename: Ben
authors.initials: B
authors.lastname: Whalley
authors.affiliation: Sagol department of Neurobiology, Faculty of Natural Sciences, University of Haifa, Haifa, Israel.
authors.forename: Sourav
authors.initials: S
authors.lastname: Ghosh
authors.affiliation: Sagol department of Neurobiology, Faculty of Natural Sciences, University of Haifa, Haifa, Israel.
authors.forename: Raphael
authors.initials: R
authors.lastname: Lamrecht
authors.affiliation: Sagol department of Neurobiology, Faculty of Natural Sciences, University of Haifa, Haifa, Israel ebarkai@research.haifa.ac.il.
authors.forename: Edi
authors.initials: E
authors.lastname: Barkai
mesh_terms: D000818:Animals; D001522:Behavior, Animal; D004192:Discrimination, Psychological; D019706:Excitatory Postsynaptic Potentials; D066298:In Vitro Techniques; D053444:Inhibitory Postsynaptic Potentials; D007858:Learning; D008297:Male; D055369:Miniature Postsynaptic Potentials; D009434:Neural Pathways / Q000166:cytology / Q000502:physiology; D009473:Neuronal Plasticity; D055696:Olfactory Perception; D066195:Piriform Cortex / Q000166:cytology / Q000502:physiology*; D017966:Pyramidal Cells / Q000502:physiology*; D017207:Rats, Sprague-Dawley; D012903:Smell; D009435:Synaptic Transmission; D013997:Time Factors
keywords: Brain slices; brain slices; lomg‐term memory; piriofm cortex; synaptic plasticity