Parvalbumin interneuron inhibition onto anterior insula neurons projecting to the basolateral amygdala drives aversive taste memory retrieval

Adonis Yiannakas, Sailendrakumar Kolatt Chandran, Haneen Kayyal, Nathaniel Gould, Mohammad Khamaisy, Kobi Rosenblum

Research output: Contribution to journalArticlepeer-review

Abstract

Memory retrieval refers to the fundamental ability of organisms to make use of acquired, sometimes inconsistent, information about the world. Although memory acquisition has been studied extensively, the neurobiological mechanisms underlying memory retrieval remain largely unknown. Conditioned taste aversion (CTA) is a robust associative paradigm, through which animals can be trained to express aversion toward innately appetitive tastants. The anterior insula (aIC) is indispensable in the ability of mammals to retrieve associative information regarding tastants that have been previously linked with gastric malaise. Here, we show that CTA memory retrieval promotes cell-type-specific activation in the aIC. Using chemogenetic tools in the aIC, we found that CTA memory acquisition requires activation of excitatory neurons and inhibition of inhibitory neurons, whereas retrieval necessitates activation of both excitatory and inhibitory aIC circuits. CTA memory retrieval at the aIC activates parvalbumin (PV) interneurons and increases synaptic inhibition onto activated pyramidal neurons projecting to the basolateral amygdala (aIC-BLA). Unlike innately appetitive taste memory retrieval, CTA retrieval increases synaptic inhibition onto aIC-BLA-projecting neurons that is dependent on activity in aIC PV interneurons. PV aIC interneurons coordinate CTA memory retrieval and are necessary for its dominance when conflicting internal representations are encountered over time. The reinstatement of CTA memories following extinction is also dependent on activation of aIC PV interneurons, which increase the frequency of inhibition onto aIC-BLA-projecting neurons. This newly described interaction of PV and a subset of excitatory neurons can explain the coherency of aversive memory retrieval, an evolutionary pre-requisite for animal survival.

Original languageEnglish
Pages (from-to)2770-2784.e6
JournalCurrent Biology
Volume31
Issue number13
DOIs
StatePublished - 12 Jul 2021

Bibliographical note

Funding Information:
The authors would like to thank all current members of the Rosenblum lab for their help and support. Special thanks to Dr. Hanoch Kaphzan, Federica Cruciani, Gaia Auerbach, and Gila Scherer for critical reading of the manuscript. This research was supported by a grant from the Israel Science Foundation (ISF), ISF 946/17 , ISF 258/20 , ISF-UGC 2311/15 , and TransNeuro ERANET JPND supported by the Israel Ministry of Health grant 3-14616 to K.R.

Publisher Copyright:
© 2021 Elsevier Inc.

Keywords

  • basolateral amygdala
  • conditioned taste aversion
  • insular cortex
  • memory retrieval
  • parvalbumin

ASJC Scopus subject areas

  • Neuroscience (all)
  • Biochemistry, Genetics and Molecular Biology (all)
  • Agricultural and Biological Sciences (all)

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