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

AbstractMemory 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 a subset of excitatory neurons can explain the coherency of aversive memory retrieval, an evolutionary pre-requisite for animal survival.Graphical AbstractRetrieval of Conditioned Taste Aversion (CTA) memories at the anterior insular cortex 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 the amplitude and frequency of synaptic inhibition onto aIC-BLA projecting neurons, that is dependent on activity in aIC PV interneurons.Activation of aIC PV interneurons is necessary for the expression of learned taste avoidance, in both sexes, regardless of stimulus identity.Extinction of aversive taste memories suppresses the frequency, but not the amplitude of synaptic inhibition on aIC-BLA projecting neurons.The reinstatement of aversive taste memories following extinction is dependent upon activation of aIC PV interneurons and increases in the frequency of inhibition on aIC-BLA projecting neurons.

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

Current Biology ◽

10.1016/j.cub.2021.04.010 ◽

2021 ◽

Author(s):

Adonis Yiannakas ◽

Sailendrakumar Kolatt Chandran ◽

Haneen Kayyal ◽

Nathaniel Gould ◽

Mohammad Khamaisy ◽

...

Keyword(s):

Memory Retrieval ◽

Basolateral Amygdala ◽

Anterior Insula ◽

Aversive Taste ◽

Parvalbumin Interneuron

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The anterior insular cortex associates temporally discontiguous stimuli during threat learning

10.1101/2021.10.19.465048 ◽

2021 ◽

Author(s):

Ho Namkung ◽

Sedona Lockhart ◽

Josephine de Chabot ◽

Lauren Guttman ◽

Imad Isehak ◽

...

Keyword(s):

Animal Studies ◽

Basolateral Amygdala ◽

Pyramidal Neurons ◽

Insular Cortex ◽

D1 Receptor ◽

Time Interval ◽

Essential Information ◽

Anterior Insular Cortex ◽

Dopamine Signaling ◽

Mouse Study

Learning about potential threats in the environment is indispensable for survival. Deficits in threat learning constitute a key dimension of multiple brain disorders, which include posttraumatic stress disorder and anxiety disorder. While human brain imaging studies have highlighted a reliable engagement of the anterior insular cortex (AIC) in threat learning, its precise role remains elusive partly due to the lack of animal studies that can address causality and mechanistic questions. Filling in this gap, the present mouse study proposes a novel AICmediated mechanism underlying the association of temporally discontiguous stimuli during threat learning. We identified that activity of AIC layer 5 (L5) pyramidal neurons is required for associating temporally discontiguous stimuli, specifically during a time interval between them. Notably, the AIC is not required for associating temporally contiguous stimuli during threat learning. The AIC not only sends the essential information, via its L5 pyramidal neurons, to the basolateral amygdala (BLA) during the time interval, but also receives from the BLA. We also identified a modulatory role of AIC dopamine D1 receptor (D1R)-mediated dopamine signaling in associating temporally discontiguous stimuli during the time interval.

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Muscarinic activation of a non-selective cationic conductance in pyramidal neurons in rat basolateral amygdala

Neuroscience ◽

10.1016/s0306-4522(98)00210-3 ◽

1999 ◽

Vol 88 (1) ◽

pp. 159-167 ◽

Cited By ~ 17

Author(s):

J Yajeya ◽

A de la Fuente Juan ◽

V.M Bajo ◽

A.S Riolobos ◽

M Heredia ◽

...

Keyword(s):

Basolateral Amygdala ◽

Pyramidal Neurons

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Nicotinic activity depresses synaptic potentiation in layer V pyramidal neurons of mouse insular cortex

Neuroscience ◽

10.1016/j.neuroscience.2017.06.031 ◽

2017 ◽

Vol 358 ◽

pp. 13-27 ◽

Cited By ~ 13

Author(s):

Hajime Sato ◽

Tsutomu Kawano ◽

Dong Xu Yin ◽

Takafumi Kato ◽

Hiroki Toyoda

Keyword(s):

Pyramidal Neurons ◽

Insular Cortex ◽

Synaptic Potentiation ◽

Layer V

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VTA-IC dopaminergic inputs enhances the salience to consolidate aversive but not appetitive taste recognition memory via D1 receptors

10.1101/2021.11.19.469297 ◽

2021 ◽

Author(s):

Elvi Gil Lievana ◽

Gerardo Ramirez Mejia ◽

Oscar Urrego Morales ◽

Jorge Luis Islas ◽

Ranier Gutierrez ◽

...

Keyword(s):

Neural Network ◽

Recognition Memory ◽

Dopaminergic Neurons ◽

Insular Cortex ◽

Taste Stimulus ◽

D1 Receptors ◽

Hedonic Value ◽

The Neural Network ◽

Aversive Taste ◽

Dopaminergic Pathway

Taste memory involves storing information through plasticity changes in the neural network of taste, including the insular cortex (IC) and ventral tegmental area (VTA), a critical provider of dopamine. Although a VTA-IC dopaminergic pathway has been demonstrated, its role to consolidate taste recognition memory remains poorly understood. We found that photostimulation of dopaminergic neurons in the VTA or VTA-IC dopaminergic terminals of TH-Cre mice increases the salience to facilitate consolidation of a novel taste stimulus regardless of its hedonic value, without altering their taste palatability. Importantly, the inhibition of the D1-like receptor into the IC impairs the salience to facilitate consolidation of an aversive taste recognition memory. Finally, our results showed that VTA photostimulation improves the salience to facilitate consolidation of a conditioned taste aversion memory through the D1-like receptor into the IC. It is concluded that the dopamine activity from the VTA into IC is required to increase the salience to facilitate consolidation of a taste recognition memory. Notably, the D1-like receptor activity into the IC is required to consolidate both innate and learned aversive taste memories but not appetitive taste memory.

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Astrocytic modulation of information processing by layer 5 pyramidal neurons of the mouse visual cortex

10.1101/2020.07.09.190777 ◽

2020 ◽

Cited By ~ 2

Author(s):

Dimitri Ryczko ◽

Maroua Hanini-Daoud ◽

Steven Condamine ◽

Benjamin J. B. Bréant ◽

Maxime Fougère ◽

...

Keyword(s):

Visual Cortex ◽

Cortical Neurons ◽

Calcium Binding ◽

Pyramidal Neurons ◽

Binding Protein ◽

Contextual Information ◽

Dendritic Tree ◽

Cortical Layer ◽

List Type ◽

Ionic Environment

AbstractThe most complex cerebral functions are performed by the cortex which most important output is carried out by its layer 5 pyramidal neurons. Their firing reflects integration of sensory and contextual information that they receive. There is evidence that astrocytes influence cortical neurons firing through the release of gliotransmitters such as ATP, glutamate or GABA. These effects were described at the network and at the synaptic levels, but it is still unclear how astrocytes influence neurons input-output transfer function at the cellular level. Here, we used optogenetic tools coupled with electrophysiological, imaging and anatomical approaches to test whether and how astrocytic activation affected processing and integration of distal inputs to layer 5 pyramidal neurons (L5PN). We show that optogenetic activation of astrocytes near L5PN cell body prolonged firing induced by distal inputs to L5PN and potentiated their ability to trigger spikes. The observed astrocytic effects on L5PN firing involved glutamatergic transmission to some extent but relied on release of S100β, an astrocytic Ca2+-binding protein that decreases extracellular Ca2+ once released. This astrocyte-evoked decrease of extracellular Ca2+ elicited firing mediated by activation of Nav1.6 channels. Our findings suggest that astrocytes contribute to the cortical fundamental computational operations by controlling the extracellular ionic environment.Key Points SummaryIntegration of inputs along the dendritic tree of layer 5 pyramidal neurons is an essential operation as these cells represent the most important output carrier of the cerebral cortex. However, the contribution of astrocytes, a type of glial cell to these operations is poorly documented.Here we found that optogenetic activation of astrocytes in the vicinity of layer 5 in the mouse primary visual cortex induce spiking in local pyramidal neurons through Nav1.6 ion channels and prolongs the responses elicited in these neurons by stimulation of their distal inputs in cortical layer 1.This effect partially involved glutamatergic signalling but relied mostly on the astrocytic calcium-binding protein S100β, which regulates the concentration of calcium in the extracellular space around neurons.These findings show that astrocytes contribute to the fundamental computational operations of the cortex by acting on the ionic environment of neurons.

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Reduced GluN1 in mouse dentate gyrus is associated with CA3 hyperactivity and psychosis-like behaviors

Molecular Psychiatry ◽

10.1038/s41380-018-0124-3 ◽

2018 ◽

Vol 25 (11) ◽

pp. 2832-2843 ◽

Cited By ~ 6

Author(s):

Amir Segev ◽

Masaya Yanagi ◽

Daniel Scott ◽

Sarah A. Southcott ◽

Jacob M. Lister ◽

...

Keyword(s):

Dentate Gyrus ◽

Basolateral Amygdala ◽

Pyramidal Neurons ◽

Mossy Fibers ◽

Model Systems ◽

Memory Processing ◽

Hippocampal Subfields ◽

Whole Cell Patch Clamp ◽

Hippocampal Activity

Abstract Recent findings from in vivo-imaging and human post-mortem tissue studies in schizophrenic psychosis (SzP), have demonstrated functional and molecular changes in hippocampal subfields that can be associated with hippocampal hyperexcitability. In this study, we used a subfield-specific GluN1 knockout mouse with a disease-like molecular perturbation expressed only in hippocampal dentate gyrus (DG) and assessed its association with hippocampal physiology and psychosis-like behaviors. First, we used whole-cell patch-clamp recordings to measure the physiological changes in hippocampal subfields and cFos immunohistochemistry to examine cellular excitability. DG-GluN1 KO mice show CA3 cellular hyperactivity, detected using two approaches: (1) increased excitatory glutamate transmission at mossy fibers (MF)-CA3 synapses, and (2) an increased number of cFos-activated pyramidal neurons in CA3, an outcome that appears to project downstream to CA1 and basolateral amygdala (BLA). Furthermore, we examined psychosis-like behaviors and pathological memory processing; these show an increase in fear conditioning (FC), a reduction in prepulse inhibition (PPI) in the KO animal, along with a deterioration in memory accuracy with Morris Water Maze (MWM) and reduced social memory (SM). Moreover, with DREADD vectors, we demonstrate a remarkably similar behavioral profile when we induce CA3 hyperactivity. These hippocampal subfield changes could provide the basis for the observed increase in human hippocampal activity in SzP, based on the shared DG-specific GluN1 reduction. With further characterization, these animal model systems may serve as targets to test psychosis mechanisms related to hippocampus and assess potential hippocampus-directed treatments.

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