Central Amygdala Prepronociceptin-Expressing Neurons Mediate Palatable Food Consumption and Reward

Hardaway, J. Andrew; Halladay, Lindsay R.; Mazzone, Christopher M.; Pati, Dipanwita; Bloodgood, Daniel W.; Kim, Michelle; Jensen, Jennifer; DiBerto, Jeffrey F.; Boyt, Kristen M.; Shiddapur, Ami; Erfani, Ava; Hon, Olivia J.; Neira, Sofia; Stanhope, Christina M; Sugam, Jonathan A.; Saddoris, Michael P.; Tipton, Greg; McElligott, Zoé A.; Jhou, Thomas C.; Stuber, Garret D.; Bruchas, Michael R.; Bulik, Cynthia M.; Holmes, Andrew B.; Kash, Thomas L.

doi:10.1016/j.neuron.2019.04.036

Cited by 53 publications

(63 citation statements)

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“…Because the CeA is composed of a heterogenous population of neurons expressing multiple neuropeptides/signaling molecules, projecting both within the nucleus and across the brain, we suggest that stimulation of the CeA as a whole may obscure the role of specific projections or genetically-defined subtypes, particularly if they have reciprocal inhibitory connections within the CeA. In addition to Kim et al, other work in CeAPBN projections from genetically-defined subtypes, such as Htr2a (serotonin 2a receptor) and Pnoc (prepronociceptin), have shown that stimulation can support nose-poking behavior (Douglass et al, 2017;Hardaway et al, 2019). Another explanation may be that most of the experiments examining genetically-defined CeA populations have been conducted in mice, whereas studies stimulating the CeA as a whole have largely been performed in rats (however see de Guglielmo et al, 2019).…”

Section: Cea Neurotensin Neurons Promote Positive Valence Behaviorsmentioning

confidence: 71%

“…The central nucleus of the amygdala (CeA) is a heterogeneous structure that plays an important role in the regulation of appetitive, aversive, and ethanol-mediated behaviors (Mahler and Berridge, 2009;Tye et al, 2011;Robinson et al, 2014;McCall et al, 2015;Warlow et al, 2017;Kim et al, 2017;Douglass et al, 2017;Hardaway et al, 2019;Salling et al, 2016). While some data have shed light on neuronal subpopulations influencing fear-and feeding-related behaviors in the CeA (Haubensak et al, 2010;Cai et al, 2014;Douglass et al, 2017), it remains unclear which CeA subpopulations and efferents influence ethanol consumption, particularly during early ethanol seeking (Gilpin et al, 2015;de Guglielmo et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

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Manipulations of central amygdala neurotensin neurons alter the consumption of ethanol and sweet fluids in mice

Torruella-Suárez

Vandenberg

Cogan

et al. 2018

Preprint

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The central nucleus of the amygdala plays a significant role in alcohol use and other affective disorders; however, the genetically-defined neuronal subtypes and their projections that govern these behaviors are not well known. Here we show that neurotensin neurons in the central nucleus of the amygdala of male mice are activated by in vivo ethanol consumption and that genetic ablation of these neurons decreases ethanol consumption and preference in non-ethanol dependent animals. This ablation did not impact preference for sucrose, saccharin, or quinine. We found that the most robust projection of the central amygdala neurotensin neurons was to the parabrachial nucleus, a brain region known to be important in feeding behaviors, conditioned taste aversion, and alarm. Optogenetic stimulation of projections from these neurons to the parabrachial nucleus is reinforcing, and increases ethanol drinking as well as consumption of sucrose and saccharin solutions. These data suggest that this central amygdala to parabrachial nucleus projection influences the expression of reward-related phenotypes and is a novel circuit promoting consumption of ethanol and palatable fluids.

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Section: Cea Neurotensin Neurons Promote Positive Valence Behaviorsmentioning

confidence: 71%

Section: Introductionmentioning

confidence: 99%

Manipulations of central amygdala neurotensin neurons alter the consumption of ethanol and sweet fluids in mice

Torruella-Suárez

Vandenberg

Cogan

et al. 2018

Preprint

Self Cite

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“…Further, we found that Pnoc BNST neurons predominantly express the vesicular GABA transporter gene, Slc32a1, (Vgat) and not the vesicular glutamate transporter 2 gene, Slc17a6, (Vglut2; Figure 1B), indicating that Pnoc expression defines a subpopulation of GABAergic neurons within BNST. Pnoc-IRES-Cre mice (Hardaway et al, 2019;Parker et al, 2019) were then used for selective targeting of Pnoc + neurons in the adBNST in conjunction with cre-inducible viruses.…”

Section: Expression Of Prepronociceptin Defines a Subpopulation Of Gamentioning

confidence: 99%

“…Neuropeptide gene expression patterns have identified functionally distinct subpopulations of neurons in BNST (Kash et al, 2015). Recently, neurons that express the prepronociceptin gene (Pnoc, the genetic precursor to the nociception neuropeptide) within the central nucleus of the amygdala and the paranigral ventral tegmental area were shown to have a role in gating motivational states and reward seeking (Hardaway et al, 2019;Parker et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

Prepronociceptin expressing neurons in the extended amygdala encode and promote rapid arousal responses to motivationally salient stimuli

Rodríguez-Romaguera

Ung

Nomura

et al. 2020

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Motivational states are complex and consist of cognitive, emotional, and physiological components controlled by a network across multiple brain regions. An integral component of this neural circuitry is the bed nucleus of the stria terminalis (BNST). Here, we identified a subpopulation of neurons within BNST expressing the gene prepronociceptin (Pnoc BNST ), that can modulate the rapid changes in physiological arousal that occur upon exposure to stimuli with motivational salience. Using in vivo two-photon calcium imaging we found that excitatory responses from individual Pnoc BNST neurons directly corresponded with rapid increases in pupillary size and occurred upon exposure to both aversive and rewarding odors. Furthermore, optogenetic activation of these neurons increased pupillary size, but did not alter approach/avoidance or locomotor behaviors. These findings suggest that excitatory responses in Pnoc BNST neurons encode rapid arousal responses irrespective of tested behaviors. Further histological, electrophysiological, and single-cell RNA sequencing data revealed that Pnoc BNST neurons are composed of genetically and anatomically identifiable subpopulations that can be further investigated. Taken together, our findings demonstrate a key role for a Pnoc BNST neuronal ensemble in encoding the rapid arousal responses that are triggered by motivational stimuli.

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“…Neurons in the central nucleus of the amygdala (CeA) play an important role in controlling feeding, a behavior critical to our survival and health Douglass et al, 2017;Hardaway et al, 2019;Ip et al, 2019;Petrovich et al, 2009). However, how the CeA neurons control food intake at circuit level is still poorly understood.…”

Section: Introductionmentioning

confidence: 99%

Neural circuit mechanism underlying the feeding controlled by insula-central amygdala pathway

Zhang-Molina

Schmit

Cai

2019

Preprint

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SummaryCentral nucleus of amygdala (CeA) contains distinct populations of neurons that play opposing roles in feeding. The circuit mechanism of how CeA neurons process information sent from their upstream inputs to regulate feeding is still unclear. Here we show that activation of the neural pathway projecting from insular cortex neurons to CeA suppresses food intake. Surprisingly, we find that the inputs from insular cortex form excitatory connections with similar strength to all types of CeA neurons. To reconcile this puzzling result, and previous findings, we developed a conductance-based dynamical systems model for the CeA neuronal network. Computer simulations showed that both the intrinsic electrophysiological properties of individual CeA neurons and the overall synaptic organization of the CeA circuit play a functionally significant role in shaping the CeA neural dynamics. We successfully identified a specific CeA circuit structure that reproduces the desired circuit output consistent with existing experimentally observed feeding behaviors.

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Central Amygdala Prepronociceptin-Expressing Neurons Mediate Palatable Food Consumption and Reward

Cited by 53 publications

References 0 publications

Manipulations of central amygdala neurotensin neurons alter the consumption of ethanol and sweet fluids in mice

Manipulations of central amygdala neurotensin neurons alter the consumption of ethanol and sweet fluids in mice

Prepronociceptin expressing neurons in the extended amygdala encode and promote rapid arousal responses to motivationally salient stimuli

Neural circuit mechanism underlying the feeding controlled by insula-central amygdala pathway

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