LTD at amygdalocortical synapses as a novel mechanism for hedonic learning

Haley, Melissa S.; Bruno, Stephen; Fontanini, Alfredo; Maffei, Arianna

doi:10.7554/elife.55175

Cited by 21 publications

(22 citation statements)

References 63 publications

(107 reference statements)

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“…Figure 4D-E, p=0.0002). Our results are consistent with other recent studies, suggesting that suppression of excitatory activity at the aIC during CTA retrieval reflects learning-dependent hedonic shifts in the cortical representation of tastants 12 .…”

Section: Resultssupporting

confidence: 93%

“…Through the use of the RAM/CRAM activity monitoring system we demonstrate that internal representations recruited at the aIC remain plastic in relation to past knowledge, and obey topography rules that reflect their perceived valence. Consistent with recent studies 12 , we found that the size of the recruited ensemble at the aIC is restricted in response to CTA taste memory retrieval or reinstatement (Figures 5 & 7). Conversely, aIC RAM responses were significantly enhanced in mice expressing preference for the same taste, regardless of familiarity or prior experience (Suppl.…”

Section: Discussionsupporting

confidence: 91%

“…By using in vivo calcium imaging during CTA retrieval, we have previously demonstrated increased recruitment of aIC-BLA projecting neurons in a valence-, but not stimulus-specific manner 10 , and that activation of this projection is necessary for CTA acquisition, as well as retrieval 11 . More recent evidence would suggest that memory retrieval relies on fine-tuning of activity in excitatory aIC circuits, that is driven by learning-induced changes in connectivity and plasticity 12 . Such learning-induced reconfigurations are thought to be supported by plasticity in inhibitory synapses 13 .…”

Section: Introductionmentioning

confidence: 99%

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

Yiannakas

Chandran²,

Kayyal³

et al. 2021

Preprint

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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.

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Section: Resultssupporting

confidence: 93%

Section: Discussionsupporting

confidence: 91%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

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

Yiannakas

Chandran²,

Kayyal³

et al. 2021

Preprint

View full text Add to dashboard Cite

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“…Here we directly examined how synaptic scaling shapes memory specificity in conditioned taste aversion (CTA) learning, a form of associative learning that relies on Hebbian plasticity within the gustatory cortex (GC) 19,20,21,22,23 . We found that following CTA conditioning, animals transitioned from a generalized to a taste-specific aversion over a timescale of ∼24 hours.…”

Section: Introductionmentioning

confidence: 99%

Homeostatic Synaptic Scaling Establishes the Specificity of an Associative Memory

Ramos

Katz

et al. 2020

Preprint

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Accurate memory formation has been hypothesized to depend on both rapid Hebbian plasticity for initial encoding, and slower homeostatic mechanisms that prevent runaway excitation and subsequent loss of memory specificity. Here, we tested the role of synaptic scaling in shaping the specificity of conditioned taste aversion (CTA) memory, a Hebbian plasticity-dependent form of associative learning. We found that CTA memory initially generalized to non-conditioned tastants (generalized aversion), becoming specific to the conditioned tastant only over the course of many hours. Blocking synaptic scaling in the gustatory cortex (GC) prolonged the duration of the initial generalized aversion and enhanced the persistence of synaptic strength increases observed after CTA. Taken together, these findings demonstrate that synaptic scaling is important for sculpting the specificity of an associative memory and suggest that the relative strengths of Hebbian and homeostatic plasticity can modulate the balance between stable memory formation and generalization.

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“…Given that in vitro slice recordings (e.g., Haley Fontanini et al 2016;Haley Bruno et al 2020) have shown BLA projection neurons to synapse onto both pyramidal cells (PCs) and interneurons (INs), it was important to ask whether the effect of BLAGCx was cell-type dependent. Our in vivo electrophysiology does not permit definitive determination of cell type, but we were able to distinguish putative PCs from putative INs based on the shape of the spike waveforms (cf.…”

Section: Both Enhancement and Inhibition Of Gc Taste Response Firing Are Wrought By Optogenetic Perturbation Of Blagc Axonsmentioning

confidence: 99%

Perturbation of amygdala-cortical projections reduces ensemble coherence of palatability coding in gustatory cortex

Lin

Mukherjee

Bernstein

et al. 2020

Preprint

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Taste palatability is centrally involved in consumption decisions—we ingest foods that taste good and reject those that don’t. Gustatory cortex (GC) and basolateral amygdala (BLA) almost certainly work together to mediate palatability-driven behavior, but the precise nature of their interplay during taste decision-making is still unknown. Here, we take a step toward filling this gap in our knowledge, by investigating the specific role that activity in the BLA→GC pathway plays in the emergence of palatability-related firing in GC response dynamics (which influence consumption decisions). We implanted electrode/optical-fiber probes in virally-prepared female Long-Evans rats, such that we could optogenetically hyperpolarize BLA→GC axons, perturbing activity in these axons without affecting BLA and GC somas, while recording GC neural responses to intra-oral presentations of a diverse taste battery. This inter-regional axonal perturbation strongly altered GC taste responses, but despite the laser illumination being tonic for the first 2s that the taste was on the tongue, the alterations were far from monolithic: rather than changing all moments of the response equally, or causing a simple exponential decay of changes, the perturbation was most strongly felt at the onset times of previously-described response epochs; furthermore, the effect was epoch-specific—perturbations had little impact on the amount of taste identity information in the “middle epoch” of the responses, but reduced evidence of palatability-related activity in the “late-epoch.” Finally, BLA→GC axon inhibition affected the nature of the epochal dynamics themselves, such that the normal abruptness of the behaviorally-relevant ensemble transitions into the palatability-related epoch was greatly diminished. These results suggest that BLA “organizes” behavior-related GC taste dynamics.

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LTD at amygdalocortical synapses as a novel mechanism for hedonic learning

Cited by 21 publications

References 63 publications

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

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

Homeostatic Synaptic Scaling Establishes the Specificity of an Associative Memory

Perturbation of amygdala-cortical projections reduces ensemble coherence of palatability coding in gustatory cortex

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