Ventral tegmental area subcircuits process rewarding and aversive experiences

Bariselli, Sebastiano; Glangetas, Christelle; Tzanoulinou, Stamatina; Bellone, Camilla

doi:10.1111/jnc.13779

Cited by 43 publications

(35 citation statements)

References 89 publications

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“…The VTA dopaminergic neurons are the primary mediators of the behavioral response to a rewarding or aversive stimulus (16). They are not uniform in their activity or projection targets, and thus activation of one neuron may produce substantially different behavioral output than another.…”

Section: Neurocircuitry Of the Reward Systemmentioning

confidence: 99%

Hunger and Satiety Gauge Reward Sensitivity

Cassidy

Tong

2017

Front. Endocrinol.

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Many of the neurocircuits and hormones known to underlie the sensations of hunger and satiety also substantially alter the activity of the dopaminergic reward system. Much interest lies in the ways that hunger, satiety, and reward tie together, as the epidemic of obesity seems tied to the recent development and mass availability of highly palatable foods. In this review, we will first discuss the basic neurocircuitry of the midbrain and basal forebrain reward system. We will elaborate how several important mediators of hunger—the agouti-related protein neurons of the arcuate nucleus, the lateral hypothalamic nucleus, and ghrelin—enhance the sensitivity of the dopaminergic reward system. Then, we will elaborate how mediators of satiety—the nucleus tractus solitarius, pro-opiomelanocortin neurons of the arcuate nucleus, and its peripheral hormonal influences such as leptin—reduce the reward system sensitivity. We hope to provide a template by which future research may identify the ways in which highly rewarding foods bypass this balanced system to produce excessive food consumption.

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Section: Neurocircuitry Of the Reward Systemmentioning

confidence: 99%

Hunger and Satiety Gauge Reward Sensitivity

Cassidy

Tong

2017

Front. Endocrinol.

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“…Electrophysiological recordings from the VTA have pointed to the fact that DA neurons constitute a heterogeneous population in terms of intrinsic properties, projection specificity and neurotransmitter/neuromodulator release [73][74][75] . This diversity is thought to subserve the processing of reinforcing and aversive experiences in an input-output specific manner [76][77][78] . VTA DA neurons projecting to the nucleus accumbens (NAc), but not prefrontal cortex (PFC), control social interaction 19 while IPN-projecting DA neurons are involved in preference for social novelty expression 20 .…”

Section: Discussionmentioning

confidence: 99%

Neuronal signature of social novelty exploration in the VTA: implication for Autism Spectrum Disorder

Bariselli

Hörnberg

Prévost-Solié

et al. 2018

Preprint

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Novel stimuli attract our attention, promote exploratory behavior, and facilitate learning. Atypical habituation and aberrant novelty exploration have been related with the severity of Autism Spectrum Disorders (ASD) but the underlying neuronal circuits are unknown. Here, we report that dopamine (DA) neurons of the ventral tegmental area (VTA) promote the behavioral responses to novel social stimuli, support preference for social novelty, and mediate the reinforcing properties of novel social interaction. Social novelty exploration is associated with the insertion of calciumpermeable GluA2-lacking AMPA-type glutamate receptors at excitatory synapses on VTA DA neurons. These novelty-dependent synaptic adaptations only persist upon repeated exposure to social stimuli and sustain social interaction. Global or DA neuron-specific inactivation of the ASD risk gene Neuroligin3 alters both social novelty exploration and the reinforcing properties of social stimuli. These behavioral deficits are accompanied by an aberrant expression of non-canonical GluA2-lacking AMPA-receptors at excitatory synapses on VTA DA neurons and an occlusion of novelty-induced synaptic plasticity. Altogether, these findings causally link impaired novelty exploration in an ASD mouse model to VTA DA circuit dysfunction.All rights reserved. No reuse allowed without permission.

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“…However, a proposed role of DH-projecting VTA dopamine neurons in memory [21][22][23] , has recently been challenged because of the finding that dopaminergic projections from VTA to DH are scarce and that dopaminergic mechanisms of memory primarily involve projections from the locus coeruleus 24,25 . Apart from dopaminergic neuronal populations, VTA contains glutamatergic and GABAergic neurons [26][27][28] that could contribute to DG granule cell activity 29 . We therefore sought to determine the extent of DH innervation provided by these projections and their role in driving behaviors based on valenced memories.…”

mentioning

confidence: 99%

Excitatory VTA to DH projections provide a valence signal to memory circuits

et al. 2020

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The positive or negative value (valence) of past experiences is normally integrated into neuronal circuits that encode episodic memories and plays an important role in guiding behavior. Here, we show, using mouse behavioral models, that glutamatergic afferents from the ventral tegmental area to the dorsal hippocampus (VTA→DH) signal negative valence to memory circuits, leading to the formation of fear-inducing context memories and to contextspecific reinstatement of fear. To a lesser extent, these projections also contributed to opioidinduced place preference, suggesting a role in signaling positive valence as well, and thus a lack of dedicated polarity. Manipulations of VTA terminal activity were more effective in females and paralleled by sex differences in glutamatergic signaling. By prioritizing retrieval of negative and positive over neutral memories, the VTA→DH circuit can facilitate the selection of adaptive behaviors when current and past experiences are valence congruent.

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Ventral tegmental area subcircuits process rewarding and aversive experiences

Cited by 43 publications

References 89 publications

Hunger and Satiety Gauge Reward Sensitivity

Hunger and Satiety Gauge Reward Sensitivity

Neuronal signature of social novelty exploration in the VTA: implication for Autism Spectrum Disorder

Excitatory VTA to DH projections provide a valence signal to memory circuits

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