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

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

doi:10.1016/j.neuron.2019.03.037

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

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

Research output: Contribution to journal › Article › peer-review

79 Scopus citations

Abstract

Food palatability is one of many factors that drives food consumption, and the hedonic drive to feed is a key contributor to obesity and binge eating. In this study, we identified a population of prepronociceptin-expressing cells in the central amygdala (Pnoc^CeA)that are activated by palatable food consumption. Ablation or chemogenetic inhibition of these cells reduces palatable food consumption. Additionally, ablation of Pnoc^CeA cells reduces high-fat-diet-driven increases in bodyweight and adiposity. Pnoc^CeA neurons project to the ventral bed nucleus of the stria terminalis (vBNST), parabrachial nucleus (PBN), and nucleus of the solitary tract (NTS), and activation of cell bodies in the central amygdala (CeA)or axons in the vBNST, PBN, and NTS produces reward behavior but did not promote feeding of palatable food. These data suggest that the Pnoc^CeA network is necessary for promoting the reinforcing and rewarding properties of palatable food, but activation of this network itself is not sufficient to promote feeding.

Original language	English
Pages (from-to)	1037-1052.e7
Journal	Neuron
Volume	102
Issue number	5
DOIs	https://doi.org/10.1016/j.neuron.2019.03.037
State	Published - 5 Jun 2019
Externally published	Yes

Keywords

binge eating
central amygdala
nociceptin
nucleus of the solitary tract
obesity
parabrachial nucleus
reward

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10.1016/j.neuron.2019.03.037

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Hardaway, J. A., Halladay, L. R., Mazzone, C. M., Pati, D., Bloodgood, D. W., Kim, M., Jensen, J., DiBerto, J. F., Boyt, K. M., Shiddapur, A., Erfani, A., Hon, O. J., Neira, S., Stanhope, C. M., Sugam, J. A., Saddoris, M. P., Tipton, G., McElligott, Z., Jhou, T. C., ... Kash, T. L. (2019). Central Amygdala Prepronociceptin-Expressing Neurons Mediate Palatable Food Consumption and Reward. Neuron, 102(5), 1037-1052.e7. https://doi.org/10.1016/j.neuron.2019.03.037

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title = "Central Amygdala Prepronociceptin-Expressing Neurons Mediate Palatable Food Consumption and Reward",

abstract = "Food palatability is one of many factors that drives food consumption, and the hedonic drive to feed is a key contributor to obesity and binge eating. In this study, we identified a population of prepronociceptin-expressing cells in the central amygdala (PnocCeA)that are activated by palatable food consumption. Ablation or chemogenetic inhibition of these cells reduces palatable food consumption. Additionally, ablation of PnocCeA cells reduces high-fat-diet-driven increases in bodyweight and adiposity. PnocCeA neurons project to the ventral bed nucleus of the stria terminalis (vBNST), parabrachial nucleus (PBN), and nucleus of the solitary tract (NTS), and activation of cell bodies in the central amygdala (CeA)or axons in the vBNST, PBN, and NTS produces reward behavior but did not promote feeding of palatable food. These data suggest that the PnocCeA network is necessary for promoting the reinforcing and rewarding properties of palatable food, but activation of this network itself is not sufficient to promote feeding.",

keywords = "binge eating, central amygdala, nociceptin, nucleus of the solitary tract, obesity, parabrachial nucleus, reward",

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

note = "Publisher Copyright: {\textcopyright} 2019 Elsevier Inc.",

year = "2019",

month = jun,

day = "5",

doi = "10.1016/j.neuron.2019.03.037",

language = "English",

volume = "102",

pages = "1037--1052.e7",

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Hardaway, JA, Halladay, LR, Mazzone, CM, Pati, D, Bloodgood, DW, Kim, M, Jensen, J, DiBerto, JF, Boyt, KM, Shiddapur, A, Erfani, A, Hon, OJ, Neira, S, Stanhope, CM, Sugam, JA, Saddoris, MP, Tipton, G, McElligott, Z, Jhou, TC, Stuber, GD, Bruchas, MR, Bulik, CM, Holmes, A & Kash, TL 2019, 'Central Amygdala Prepronociceptin-Expressing Neurons Mediate Palatable Food Consumption and Reward', Neuron, vol. 102, no. 5, pp. 1037-1052.e7. https://doi.org/10.1016/j.neuron.2019.03.037

TY - JOUR

T1 - Central Amygdala Prepronociceptin-Expressing Neurons Mediate Palatable Food Consumption and Reward

AU - Hardaway, J. Andrew

AU - Halladay, Lindsay R.

AU - Mazzone, Christopher M.

AU - Pati, Dipanwita

AU - Bloodgood, Daniel W.

AU - Kim, Michelle

AU - Jensen, Jennifer

AU - DiBerto, Jeffrey F.

AU - Boyt, Kristen M.

AU - Shiddapur, Ami

AU - Erfani, Ava

AU - Hon, Olivia J.

AU - Neira, Sofia

AU - Stanhope, Christina M.

AU - Sugam, Jonathan A.

AU - Saddoris, Michael P.

AU - Tipton, Greg

AU - McElligott, Zoe

AU - Jhou, Thomas C.

AU - Stuber, Garret D.

AU - Bruchas, Michael R.

AU - Bulik, Cynthia M.

AU - Holmes, Andrew

AU - Kash, Thomas L.

PY - 2019/6/5

Y1 - 2019/6/5

N2 - Food palatability is one of many factors that drives food consumption, and the hedonic drive to feed is a key contributor to obesity and binge eating. In this study, we identified a population of prepronociceptin-expressing cells in the central amygdala (PnocCeA)that are activated by palatable food consumption. Ablation or chemogenetic inhibition of these cells reduces palatable food consumption. Additionally, ablation of PnocCeA cells reduces high-fat-diet-driven increases in bodyweight and adiposity. PnocCeA neurons project to the ventral bed nucleus of the stria terminalis (vBNST), parabrachial nucleus (PBN), and nucleus of the solitary tract (NTS), and activation of cell bodies in the central amygdala (CeA)or axons in the vBNST, PBN, and NTS produces reward behavior but did not promote feeding of palatable food. These data suggest that the PnocCeA network is necessary for promoting the reinforcing and rewarding properties of palatable food, but activation of this network itself is not sufficient to promote feeding.

AB - Food palatability is one of many factors that drives food consumption, and the hedonic drive to feed is a key contributor to obesity and binge eating. In this study, we identified a population of prepronociceptin-expressing cells in the central amygdala (PnocCeA)that are activated by palatable food consumption. Ablation or chemogenetic inhibition of these cells reduces palatable food consumption. Additionally, ablation of PnocCeA cells reduces high-fat-diet-driven increases in bodyweight and adiposity. PnocCeA neurons project to the ventral bed nucleus of the stria terminalis (vBNST), parabrachial nucleus (PBN), and nucleus of the solitary tract (NTS), and activation of cell bodies in the central amygdala (CeA)or axons in the vBNST, PBN, and NTS produces reward behavior but did not promote feeding of palatable food. These data suggest that the PnocCeA network is necessary for promoting the reinforcing and rewarding properties of palatable food, but activation of this network itself is not sufficient to promote feeding.

KW - binge eating

KW - central amygdala

KW - nociceptin

KW - nucleus of the solitary tract

KW - obesity

KW - parabrachial nucleus

KW - reward

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U2 - 10.1016/j.neuron.2019.03.037

DO - 10.1016/j.neuron.2019.03.037

M3 - Article

C2 - 31029403

AN - SCOPUS:85067376304

SN - 0896-6273

VL - 102

SP - 1037-1052.e7

JO - Neuron

JF - Neuron

IS - 5

ER -

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

Abstract

Keywords

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