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

Abstract

Memory retrieval refers to the fundamental ability of organisms to make use of acquired, sometimes inconsistent, information about the world. While memory acquisition has been studied extensively, the neurobiological mechanisms underlying memory retrieval remain largely unknown. 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 aversive taste memory retrieval promotes cell-type-specific activation in the aIC. Aversive, but not appetitive taste memory retrieval, relies on specific changes in activity and connectivity at parvalbumin (PV) inhibitory synapses onto aIC pyramidal neurons projecting to the basolateral amygdala. PV aIC interneurons, coordinate aversive taste memory retrieval, and are necessary for its dominance when conflicting internal representations are encountered. This newly described interaction of PV and subset of excitatory neurons can explain the coherency of aversive memory retrieval, an evolutionary pre-requisite for animal survival in nature.

The Engram’s Dark Horse: How Interneurons Regulate State-Dependent Memory Processing and Plasticity

“…CFM consolidation relies on activity of D1/5 dopamine receptors, and downstream activation of cAMP and ERK, in hippocampal PV+ interneurons in the hours following CFC ( Karunakaran et al, 2016 ). PV+ interneurons in various brain structures, including the insular cortex, medial septum, and nucleus accumbens also play critical roles during memory recall–coordinating activity within limbic structures during recall of appetitive and aversive associations ( Trouche et al, 2019 ; Sans-Dublanc et al, 2020 ; Yiannakas et al, 2021 ). Altogether, these data highlight the importance of PV+ interneurons for memory processing, and underscore that the connectivity between PV+ interneurons and the principal cells they target is crucial for engram formation.…”