A ghrelin-growth hormone axis drives stress-induced vulnerability to enhanced fear
Open accessAbstract
Hormones in the hypothalamus-pituitary-adrenal (HPA) axis mediate many of the bodily responses to stressors, yet there is no clear relationship between the levels of these hormones and stress-associated mental illnesses such as posttraumatic stress disorder (PTSD). Therefore, other hormones are likely to be involved in this effect of stress. Here we used a rodent model of PTSD in which rats repeatedly exposed to a stressor display heightened fear learning following auditory Pavlovian fear conditioning. Our results show that stress-related increases in circulating ghrelin, a peptide hormone, are necessary and sufficient for stress-associated vulnerability to exacerbated fear learning and these actions of ghrelin occur in the amygdala. Importantly, these actions are also independent of the classic HPA stress axis. Repeated systemic administration of a ghrelin receptor agonist enhanced fear memory but did not increase either corticotropin-releasing factor (CRF) or corticosterone. Repeated intraamygdala infusion of a ghrelin receptor agonist produced a similar enhancement of fear memory. Ghrelin receptor antagonism during repeated stress abolished stress-related enhancement of fear memory without blunting stress-induced corticosterone release. We also examined links between ghrelin and growth hormone (GH), a major downstream effector of the ghrelin receptor. GH protein was upregulated in the amygdala following chronic stress, and its release from amygdala neurons was enhanced by ghrelin receptor stimulation. Virus-mediated overexpression of GH in the amygdala was also sufficient to increase fear. Finally, virus-mediated overexpression of a GH receptor antagonist was sufficient to block the fear-enhancing effects of repeated ghrelin receptor stimulation. Thus, ghrelin requires GH in the amygdala to exert fear-enhancing effects. These results suggest that ghrelin mediates a novel branch of the stress response and highlight a previously unrecognized role for ghrelin and growth hormone in maladaptive changes following prolonged stress.
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Repeated injection of GHS receptor agonists into amygdala increases stressor-inducing fear memory formation in mice.
“repeated injection of GHS receptor agonists into the amygdala increases stressor-inducing fear memory formation”
From Anxiety, depression, and the microbiome: A role for gut peptides (2018) · cites this paper as [315]
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Anxiety, depression, and the microbiome: A role for gut peptides
Lach, G., Schellekens, H., Dinan, T. G., & Cryan, J. F. (2018) · Neurotherapeutics · doi:10.1007/s13311-017-0585-0 · Cited by 573 · see citing works
Diet, Stress and Mental Health
Bremner, J. D., Moazzami, K., Wittbrodt, M. T., Nye, J. A., Lima, B. B., Gillespie, C. F., Rapaport, M. H., Pearce, B. D., Shah, A. J., & Vaccarino, V. (2020) · Nutrients · doi:10.3390/nu12082428 · Cited by 394 · see citing works
Amygdala inputs to prefrontal cortex guide behavior amid conflicting cues of reward and punishment
Burgos-Robles, A., Kimchi, E. Y., Izadmehr, E. M., Porzenheim, M. J., Ramos-Guasp, W. A., Nieh, E. H., Felix-Ortiz, A. C., Namburi, P., Leppla, C. A., Presbrey, K. N., et al. (2017) · Nature Neuroscience · doi:10.1038/nn.4553 · Cited by 318 · see citing works
Self-citationThe Homeostatic Force of Ghrelin
Yanagi, S., Sato, T., Kangawa, K., & Nakazato, M. (2018) · Cell Metabolism · doi:10.1016/j.cmet.2018.02.008 · Cited by 324 · see citing works
Gut liver brain axis in diseases: the implications for therapeutic interventions
Yan, M., Man, S., Sun, B., Ma, L., Guo, L., Huang, L., & Gao, W. (2023) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-023-01673-4 · Cited by 301 · see citing works
Michopoulos, V., Norrholm, S. D., & Jovanovic, T. (2015) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.01.005 · Cited by 206 · see citing works
Depression as a Glial-Based Synaptic Dysfunction
Rial, D., Lemos, C., Pinheiro, H., Duarte, J. M., Gonçalves, F. Q., Real, J. I., Prediger, R. D., Gonçalves, N., Gomes, C. A., Canas, P. M., et al. (2016) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00521 · Cited by 182 · see citing works
Bacterial Metabolites of Human Gut Microbiota Correlating with Depression
Averina, O. V., Zorkina, Y., Yunes, R. А., Kovtun, A. S., Ushakova, V. M., Morozova, A. Y., Kostyuk, G. P., Даниленко, В. Н., & Chekhonin, V. P. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21239234 · Cited by 166 · see citing works
Walker, A. K., Rivera, P. D., Wang, Q., Chuang, J.-C., Tran, S., Osborne-Lawrence, S., Estill, S. J., Starwalt, R., Huntington, P., Morlock, L., et al. (2015) · Molecular Psychiatry · doi:10.1038/mp.2014.34 · Cited by 161 · see citing works
Posttraumatic stress disorder: A metabolic disorder in disguise?
Michopoulos, V., Vester, A., & Neigh, G. (2016) · Experimental Neurology · doi:10.1016/j.expneurol.2016.05.038 · Cited by 152 · see citing works
Gut hormones in microbiota-gut-brain cross-talk
Sun, L.-J., Li, J.-N., & Nie, Y.-Z. (2020) · Chinese Medical Journal · doi:10.1097/cm9.0000000000000706 · Cited by 145 · see citing works
Cholinesterases and the fine line between poison and remedy
Pope, C., & Brimijoin, S. (2018) · Biochemical Pharmacology · doi:10.1016/j.bcp.2018.01.044 · Cited by 138 · see citing works
Neuroendocrine Regulation of Growth Hormone Secretion
Steyn, F. J., Tolle, V., Chen, C., & Epelbaum, J. (2016) · Comprehensive physiology · doi:10.1002/cphy.c150002 · Cited by 166 · see citing works
Hammack, S. E., & May, V. (2014) · Biological Psychiatry · doi:10.1016/j.biopsych.2014.12.003 · Cited by 127 · see citing works
Spencer, S. J., Emmerzaal, T. L., Kozicz, T., & Andrews, Z. B. (2015) · Biological Psychiatry · doi:10.1016/j.biopsych.2014.10.021 · Cited by 129 · see citing works
Xing, S., Li, Q., Xiong, B., Chen, Y., Feng, F., Liu, W., & Sun, H. (2020) · Medicinal Research Reviews · doi:10.1002/med.21745 · Cited by 126 · see citing works
Farokhnia, M., Grodin, E. N., Lee, M. R., Oot, E. N., Blackburn, A. N., Stangl, B. L., Schwandt, M. L., Farinelli, L. A., Momenan, R., Ramchandani, V. A., et al. (2017) · Molecular Psychiatry · doi:10.1038/mp.2017.226 · Cited by 120 · see citing works
Plasma butyrylcholinesterase regulates ghrelin to control aggression
Chen, V. P., Gao, Y., Geng, L., Parks, R. J., Pang, Y., & Brimijoin, S. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1421536112 · Cited by 110 · see citing works
Physiological roles for butyrylcholinesterase: A BChE-ghrelin axis
Brimijoin, S., Chen, V. P., Pang, Y., Geng, L., & Gao, Y. (2016) · Chemico-Biological Interactions · doi:10.1016/j.cbi.2016.02.013 · Cited by 110 · see citing works
Ghrelin in psychiatric disorders – A review
Wittekind, D. A., & Kluge, M. (2014) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2014.11.013 · Cited by 107 · see citing works
Sampling Blood from the Lateral Tail Vein of the Rat
Lee, G. L., & Goosens, K. A. (2015) · Journal of Visualized Experiments · doi:10.3791/52766 · Cited by 99 · see citing works
Self-citationThe Role of the Ghrelin System in Drug Addiction
Zallar, L. J., Farokhnia, M., Tunstall, B. J., Vendruscolo, L. F., & Leggio, L. (2017) · International review of neurobiology · doi:10.1016/bs.irn.2017.08.002 · Cited by 87 · see citing works
Central Regulation of Metabolism by Growth Hormone
Donato, J., Wasinski, F., Furigo, I. C., Metzger, M., & Frazão, R. (2021) · Cells · doi:10.3390/cells10010129 · Cited by 87 · see citing works
The Impact of Ghrelin in Metabolic Diseases: An Immune Perspective
Pereira, J. A. D. S., Corrêa‐da‐Silva, F., & Moraes‐Vieira, P. M. (2017) · Journal of Diabetes Research · doi:10.1155/2017/4527980 · Cited by 89 · see citing works
Harris, B. N. (2019) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2019.113355 · Cited by 76 · see citing works
Hypothalamus and Post-Traumatic Stress Disorder: A Review
Raise‐Abdullahi, P., Meamar, M., Vafaei, A. A., Alizadeh, M., Dadkhah, M., Shafia, S., Ghalandari-Shamami, M., Naderian, R., Samaei, A., & Rashidy‐Pour, A. (2023) · Brain Sciences · doi:10.3390/brainsci13071010 · Cited by 80 · see citing works
Linking Stress and Infertility: A Novel Role for Ghrelin
Sominsky, L., Hodgson, D. M., McLaughlin, E. A., Smith, R., Wall, H. M., & Spencer, S. J. (2017) · Endocrine Reviews · doi:10.1210/er.2016-1133 · Cited by 77 · see citing works
Circadian Rhythms of Perineuronal Net Composition
Pantazopoulos, H., Gisabella, B., Rexrode, L., Benefield, D., Yıldız, E., Seltzer, P., Valeri, J., Chelini, G., Reich, A., Ardelt, M., et al. (2020) · eNeuro · doi:10.1523/eneuro.0034-19.2020 · Cited by 73 · see citing works
Molecular Mechanisms and Health Benefits of Ghrelin: A Narrative Review
Jiao, Z., & Luo, Q. (2022) · Nutrients · doi:10.3390/nu14194191 · Cited by 79 · see citing works
Ghrelin is a persistent biomarker for chronic stress exposure in adolescent rats and humans
Yousufzai, M. I. U. A., Harmatz, E. S., Shah, M., Malik, M. O., & Goosens, K. A. (2018) · Translational Psychiatry · doi:10.1038/s41398-018-0135-5 · Cited by 73 · see citing works
Self-citationCabral, A., Portiansky, E. L., Sánchez‐Jaramillo, E., Zigman, J. M., & Perelló, M. (2016) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2016.01.027 · Cited by 70 · see citing works
Ghrelin-Derived Peptides: A Link between Appetite/Reward, GH Axis, and Psychiatric Disorders?
Labarthe, A., Fiquet, O., Hassouna, R., Zizzari, P., Lanfumey, L., Ramoz, N., Grouselle, D., Epelbaum, J., & Tolle, V. (2014) · Frontiers in Endocrinology · doi:10.3389/fendo.2014.00163 · Cited by 62 · see citing works
Anxiolytic-Like Effects of Increased Ghrelin Receptor Signaling in the Amygdala
Jensen, M. G., Ratner, C., Rudenko, O., Christiansen, S. H., Skov, L. J., Hundahl, C., Woldbye, D. P. D., & Holst, B. (2015) · The International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyv123 · Cited by 66 · see citing works
Stress Enables Reinforcement-Elicited Serotonergic Consolidation of Fear Memory
Baratta, M. V., Kodandaramaiah, S. B., Monahan, P. E., Yao, J., Weber, M. D., Lin, P.-A., Gisabella, B., Petrossian, N., Amat, J., Kim, K., et al. (2015) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.06.025 · Cited by 63 · see citing works
Self-citationCentral Ghrelin Resistance Permits the Overconsolidation of Fear Memory
Harmatz, E. S., Stone, L. A., Lim, S. H., Lee, G. L., McGrath, A. G., Gisabella, B., Peng, X., Kosoy, E., Yao, J., Liu, E. E., et al. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2016.11.009 · Cited by 61 · see citing works
Self-citationGhrelin as a Stress Hormone: Implications for Psychiatric Illness
Stone, L. A., Harmatz, E. S., & Goosens, K. A. (2020) · Biological Psychiatry · doi:10.1016/j.biopsych.2020.05.013 · Cited by 61 · see citing works
Self-citationLost in translation: How to upgrade fear memory research
Flores, Á., Fullana, M. À., Soriano-Mas, C., & Andero, R. (2018) · Molecular Psychiatry · doi:10.1038/s41380-017-0006-0 · Cited by 59 · see citing works
The Complex Signaling Pathways of the Ghrelin Receptor
Hedegaard, M. A., & Holst, B. (2020) · Endocrinology · doi:10.1210/endocr/bqaa020 · Cited by 57 · see citing works
Acylated but not des‐acyl ghrelin is neuroprotective in an MPTP mouse model of Parkinson's disease
Bayliss, J. A., Lemus, M. B., dos Santos, V. V., Deo, M., Elsworth, J. D., & Andrews, Z. B. (2016) · Journal of Neurochemistry · doi:10.1111/jnc.13576 · Cited by 56 · see citing works
Darling, J., Zhao, F., Loftus, R., Patton, L., Gibbs, R., & Hougland, J. L. (2015) · Biochemistry · doi:10.1021/bi5010359 · Cited by 55 · see citing works
Morin, V., Hozer, F., & Costemale-Lacoste, J.-F. (2018) · L Encéphale · doi:10.1016/j.encep.2017.10.012 · Cited by 55 · see citing works
Hippocampus ghrelin receptor signaling promotes socially-mediated learned food preference
Hsu, T. M., Noble, E. E., Reiner, D. J., Liu, C. M., Suarez, A. N., Konanur, V., Hayes, M. R., & Kanoski, S. E. (2017) · Neuropharmacology · doi:10.1016/j.neuropharm.2017.11.039 · Cited by 54 · see citing works
Is there a relationship between PTSD and complicated obesity? A review of the literature
Aaseth, J., Roer, G. E., Lien, L., & Bjørklund, G. (2019) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2019.108834 · Cited by 51 · see citing works
Fritz, E. M., Singewald, N., & Bundel, D. D. (2020) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2020.594484 · Cited by 42 · see citing works
Effects of growth hormone in the central nervous system
Wasinski, F., Frazão, R., & Donato, J. (2019) · Archives of Endocrinology and Metabolism · doi:10.20945/2359-3997000000184 · Cited by 42 · see citing works
Börchers, S., Krieger, J.-P., Marić, I., Carl, J., Abraham, M., Longo, F., Asker, M., Richard, J. E., & Skibicka, K. P. (2022) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.901669 · Cited by 38 · see citing works
Sampling Blood from the Lateral Tail Vein of the Rat
Lee, G. L., & Goosens, K. A. (2015) · Journal of Visualized Experiments · doi:10.3791/52766-v · Cited by 40 · see citing works
Self-citationThe best-laid plans go oft awry: synaptogenic growth factor signaling in neuropsychiatric disease
Williams, A. J., & Umemori, H. (2014) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2014.00004 · Cited by 37 · see citing works
Gupta, D., Chuang, J.-C., Mani, B. K., Shankar, K., Rodriguez, J. A., Osborne-Lawrence, S. L., Metzger, N. P., & Zigman, J. M. (2019) · Neuropsychopharmacology · doi:10.1038/s41386-019-0334-7 · Cited by 37 · see citing works
Liu, W., Wang, H., Wang, Y., Li, H., & Liu, J. (2015) · Psychiatry Research · doi:10.1016/j.psychres.2015.05.102 · Cited by 36 · see citing works
The potential of epigenetics in stress-enhanced fear learning models of PTSDPreprint
Blouin, A. M., Sillivan, S. E., Joseph, N. F., & Miller, C. A. (2016) · Learning & Memory · doi:10.1101/lm.040485.115 · Cited by 36 · see citing works
Méquinion, M., Foldi, C. J., & Andrews, Z. B. (2020) · Frontiers in Nutrition · doi:10.3389/fnut.2019.00190 · Cited by 34 · see citing works
Davis, T. R., Pierce, M. R., Novak, S. X., & Hougland, J. L. (2021) · Open Biology · doi:10.1098/rsob.210080 · Cited by 33 · see citing works
GHS-R1a Deficiency Alleviates Depression-Related Behaviors After Chronic Social Defeat Stress
Guo, L., Niu, M., Yang, J., Li, L., Liu, S., Sun, Y., Zhou, Z., & Zhou, Y. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.00364 · Cited by 33 · see citing works
Huang, C., Chou, D., Yeh, C.-M., & Hsu, K. (2015) · Neuropharmacology · doi:10.1016/j.neuropharm.2015.09.018 · Cited by 32 · see citing works
Takeoka, A., Tayama, J., Kobayashi, M., Sagara, I., Ogawa, S., Saigo, T., Hayashida, M., Yamasaki, H., Fukudo, S., & Shirabe, S. (2017) · Helicobacter · doi:10.1111/hel.12445 · Cited by 31 · see citing works
Hougland, J. L. (2019) · Biochemical Society Transactions · doi:10.1042/bst20180436 · Cited by 29 · see citing works
Distribution of growth hormone-responsive cells in the brain of rats and mice
Wasinski, F., Klein, M., Bittencourt, J. C., Metzger, M., & Donato, J. (2020) · Brain Research · doi:10.1016/j.brainres.2020.147189 · Cited by 30 · see citing works
New findings on brain actions of growth hormone and potential clinical implications
Donato, J., & Kopchick, J. J. (2023) · Reviews in Endocrine and Metabolic Disorders · doi:10.1007/s11154-023-09861-x · Cited by 31 · see citing works
Dyshomeostasis, obesity, addiction and chronic stress
Marks, D. F. (2016) · Health Psychology Open · doi:10.1177/2055102916636907 · Cited by 28 · see citing works
Advances in the Development of Nonpeptide Small Molecules Targeting Ghrelin Receptor
Giorgioni, G., Bello, F. D., Quaglia, W., Botticelli, L., Cifani, C., Bonaventura, E. M. D., Bonaventura, M. D. D., & Piergentili, A. (2022) · Journal of Medicinal Chemistry · doi:10.1021/acs.jmedchem.1c02191 · Cited by 23 · see citing works
Growth hormone biases amygdala network activation after fear learning
Gisabella, B., Farah, S., Peng, X., Burgos-Robles, A., Lim, S. H., & Goosens, K. A. (2016) · Translational Psychiatry · doi:10.1038/tp.2016.203 · Cited by 28 · see citing works
Self-citationHsieh, S., Lin, H., Chen, C., Jhuo, C., Liao, K., Chen, W., & Tzen, J. T. C. (2019) · Chemico-Biological Interactions · doi:10.1016/j.cbi.2019.108893 · Cited by 27 · see citing works
An overview of ghrelinO-acyltransferase inhibitors: a literature and patent review for 2010-2019
Moose, J. E., Leets, K. A., Mate, N. A., Chisholm, J. D., & Hougland, J. L. (2020) · Expert Opinion on Therapeutic Patents · doi:10.1080/13543776.2020.1776263 · Cited by 26 · see citing works
Ribeiro, L. F., Catarino, T., de Carvalho, M. L., Cortes, L., Santos, S. D., Opazo, P., Ribeiro, L. R., Oliveiros, B., Choquet, D., Esteban, J. A., et al. (2021) · Science Signaling · doi:10.1126/scisignal.abb1953 · Cited by 25 · see citing works
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On making (and turning adaptive to) maladaptive aversive memories in laboratory rodents
Gazarini, L., Stern, C. A. J., & Bertoglio, L. J. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105101 · Cited by 25 · see citing works
Neuroendocrine Regulation of Growth Hormone Secretion
Steyn, F. J., Tolle, V., Chen, C., & Epelbaum, J. (2016) · Comprehensive physiology · doi:10.1002/j.2040-4603.2016.tb00692.x · Cited by 26 · see citing works
You, Z., Galaj, E., Alén, F., Wang, B., Bi, G., Moore, A. R., Buck, T. G., Crissman, M. E., Pari, S., Xi, Z., et al. (2021) · Neuropsychopharmacology · doi:10.1038/s41386-021-01249-2 · Cited by 25 · see citing works
Lu, Y.-C., Niu, M., Qiu, X., Cao, H.-S., Xing, B., Sun, Y.-X., Zhou, Z., & Zhou, Y. (2019) · Neuroscience · doi:10.1016/j.neuroscience.2019.05.067 · Cited by 23 · see citing works
The impact of early-life environment on absence epilepsy and neuropsychiatric comorbidities
Sarkisova, K. Y., & van Luijtelaar, G. (2022) · IBRO Neuroscience Reports · doi:10.1016/j.ibneur.2022.10.012 · Cited by 26 · see citing works
Acute Food Deprivation Rapidly Modifies Valence-Coding Microcircuits in the AmygdalaPreprint
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Brimijoin, S., Gao, Y., Geng, L., & Chen, V. P. (2018) · Frontiers in Pharmacology · doi:10.3389/fphar.2018.00112 · Cited by 23 · see citing works
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Beyond digestion: Exploring how the gut microbiota modulates human social behaviors
Abavisani, M., Faraji, N., Ebadpour, N., Kesharwani, P., & Sahebkar, A. (2024) · Neuroscience · doi:10.1016/j.neuroscience.2024.11.068 · Cited by 25 · see citing works
Li, N., Xiao, K., Mi, X., Li, N., Guo, L., Wang, X., Sun, Y.-X., Li, G.-D., & Zhou, Y. (2021) · Neuropharmacology · doi:10.1016/j.neuropharm.2021.108871 · Cited by 20 · see citing works
Associations of early life stress with leptin and ghrelin in healthy young adults
Daniels, T. E., Mathis, K. J., Gobin, A. P., Angeles, W. W. L.-D. L., Smith, E. M., Chanthrakumar, P., de la Monte, S. M., & Tyrka, A. R. (2022) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2022.106007 · Cited by 22 · see citing works
Growth Hormone Action in Somatostatin Neurons Regulates Anxiety and Fear Memory
dos Santos, W. O., Juliano, V. A. L., Chaves, F. M., Vieira, H. R., Frazão, R., List, E. O., Kopchick, J. J., Munhoz, C. D., & Donato, J. (2023) · Journal of Neuroscience · doi:10.1523/jneurosci.0254-23.2023 · Cited by 22 · see citing works
Ghrelin and aggressive behaviours—Evidence from preclinical and human genetic studies
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Neurotransmitter, neurohormonal, and neuropeptidal function in stress and PTSD
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Beyond Appetite: Acylated Ghrelin As A Learning, Memory and Fear Behavior-modulating Hormone.
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Ghrelin, Neuroinflammation, Oxidative Stress, and Mood Disorders: What Are the Connections?
Mingardi, J., Meanti, R., Paoli, C., Cifani, C., Torsello, A., Popoli, M., & Musazzi, L. (2024) · Current Neuropharmacology · doi:10.2174/1570159x22999240722095039 · Cited by 16 · see citing works
The gut peptide neuropeptide Y and post-traumatic stress disorder
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Eldomiaty, M. A., Makarenko, O., Hassan, Z. A., Almasry, S. M., Petrov, P., & Elnaggar, A. M. (2020) · Folia Morphologica · doi:10.5603/fm.a2020.0007 · Cited by 16 · see citing works
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Self-citationEffects of Growth Hormone Receptor Ablation in Corticotropin-Releasing Hormone Cells
dos Santos, W. O., Gusmão, D. O., Wasinski, F., List, E. O., Kopchick, J. J., & Donato, J. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22189908 · Cited by 16 · see citing works
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The effect of obestatin on anxiety-like behaviour in mice
Szakács, J., Csabafi, K., Lipták, N., & Szabó, G. (2015) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.06.042 · Cited by 15 · see citing works
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- Authors
- Meyer, R. M., Burgos-Robles, A., Liu, E., Correia, S. S., & Goosens, K. A.
- Affiliations
- McGovern Institute for Brain Research (US)
- Venue
- Molecular Psychiatry
- Published
- 2013-10-15
- Volume
- 19
- Issue
- 12
- Pages
- 1284-1294
- ISSN
- 1359-4184 (ISSN-L)
- 1476-5578
- PMC
- PMC3988273
- OpenAlex
- W2064458835
- Cited by
- 169
- References
- 92
- Citations by year
- 2026: 3 · 2025: 8 · 2024: 12 · 2023: 14 · 2022: 18 · 2021: 11 · 2020: 22 · 2019: 15 · 2018: 11 · 2017: 14 · 2016: 19 · 2015: 14 · 2014: 8
- FWCI
- 7.39
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by-nc-nd
- www.springer.com/tdm (unspecified)
- Locations
- Molecular Psychiatry (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc-sa)
- PMC
- Funders
- Defense Advanced Research Projects Agency (W911NF-10-1-0059)
- Advanced Research Projects Agency
- National Institute of Mental Health (R01MH084966)
- National Institute of General Medical Sciences (T32GM007484)
- Army Research Office (W911NF-10-1-0059, W911NF)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Regulation of Appetite and Obesity
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Keywords
- ghrelin, growth hormone, growth hormone secretagogue receptor, amygdala, fear memory, post-traumatic stress disorder, chronic stress, fear conditioning, corticosterone, corticotropin-releasing factor, hypothalamic-pituitary-adrenal axis, stress response
- MeSH terms
- Amygdala, Animals, Chronic Disease, Corticosterone, Corticotropin-Releasing Hormone, Disease Models, Animal, Fear, Hypothalamo-Hypophyseal System, Male, Memory, Molecular Biology, Neurons, Pituitary-Adrenal System, Growth Hormone, Stress Disorders, Post-Traumatic, Stress, Psychological, Simplexvirus, Rats, Long-Evans, Ghrelin, Receptors, Ghrelin
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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