Altered Neuronal Activity in the Central Nucleus of the Amygdala Induced by Restraint Water-Immersion Stress in Rats
Open accessAbstract
Restraint water-immersion stress (RWIS), a compound stress model, has been widely used to induce acute gastric ulceration in rats. A wealth of evidence suggests that the central nucleus of the amygdala (CEA) is a focal region for mediating the biological response to stress. Different stressors induce distinct alterations of neuronal activity in the CEA; however, few studies have reported the characteristics of CEA neuronal activity induced by RWIS. Therefore, we explored this issue using immunohistochemistry and in vivo extracellular single-unit recording. Our results showed that RWIS and restraint stress (RS) differentially changed the c-Fos expression and firing properties of neurons in the medial CEA. In addition, RWIS, but not RS, induced the activation of corticotropin-releasing hormone neurons in the CEA. These findings suggested that specific neuronal activation in the CEA is involved in the formation of RWIS-induced gastric ulcers. This study also provides a possible theoretical explanation for the different gastric dysfunctions induced by different stressors.
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Stress increases CeA activity.
“Elevated CeA→DMS activity following stress is consistent with evidence that stress increases CeA activity63–65.”
From A dual-pathway architecture for stress to disrupt agency and promote habit (2025) · cites this paper as [64]
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Cites
The rat brain in stereotaxic coordinates
Palkovits, M. (1983) · Neuropeptides · doi:10.1016/0143-4179(83)90049-5 · Cited by 28,959 · see citing works
The Rat Brain in Stereotaxic Coordinates
Paxinos, G., & Watson, C. (1983) · Elsevier eBooks · doi:10.1016/c2009-0-63235-9 · Cited by 28,585 · see citing works
Neural regulation of endocrine and autonomic stress responses
Ulrich-Lai, Y. M., & Herman, J. P. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2647 · Cited by 3,318 · see citing works
Stress, memory and the amygdala
Roozendaal, B., McEwen, B. S., & Chattarji, S. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2651 · Cited by 1,760 · see citing works
Stressor specificity of central neuroendocrine responses: implications for stress-related disorders
Pacák, K., & Palkovits, M. (2001) · Endocrine Reviews · doi:10.1210/edrv.22.4.0436 · Cited by 926 · see citing works
Amygdala inhibitory circuits and the control of fear memory
Ehrlich, I., Humeau, Y., Grenier, F., Ciocchi, S., Herry, C., & Lüthi, A. (2009) · Neuron · doi:10.1016/j.neuron.2009.05.026 · Cited by 878 · see citing works
Kim, M. J., Loucks, R. A., Palmer, A. L., Brown, A. C., Solomon, K. M., Marchante, A. N., & Whalen, P. J. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.04.025 · Cited by 838 · see citing works
Vasopressin and Oxytocin Excite Distinct Neuronal Populations in the Central Amygdala
Huber, D., Veinante, P., & Stoop, R. (2005) · Science · doi:10.1126/science.1105636 · Cited by 804 · see citing works
The neurobiology of stress and gastrointestinal disease
MAYER, E. A. (2000) · Gut · doi:10.1136/gut.47.6.861 · Cited by 666 · see citing works
Brainstem circuits regulating gastric function
Travagli, R. A., Hermann, G. E., Browning, K. N., & Rogers, R. C. (2006) · Annual Review of Physiology · doi:10.1146/annurev.physiol.68.040504.094635 · Cited by 498 · see citing works
Brain–gut connections in functional GI disorders: Anatomic and physiologic relationships
Jones, M. P., Dilley, J. B., Drossman, D., & Crowell, M. D. (2006) · Neurogastroenterology & Motility · doi:10.1111/j.1365-2982.2005.00730.x · Cited by 358 · see citing works
Cassell, M. D., Gray, T. S., & Kiss, J. Z. (1986) · Journal of Comparative Neurology · doi:10.1002/cne.902460406 · Cited by 297 · see citing works
Pacák, K., Palkovits, M., Yadid, G., Květňanský, R., Kopin, I. J., & Goldstein, D. S. (1998) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1998.275.4.r1247 · Cited by 292 · see citing works
Stress-induced expression of immediate early genes in the brain and peripheral organs of the rat
Senba, E., & Ueyama, T. (1997) · Neuroscience Research · doi:10.1016/s0168-0102(97)00095-3 · Cited by 249 · see citing works
Anatomical Markers of Activity in Neuroendocrine Systems: Are we all ‘Fos‐ed out’?
Hoffman, G. E., & Lyo, D. (2002) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2002.00775.x · Cited by 242 · see citing works
Role of stress, corticotrophin releasing factor (CRF) and amygdala plasticity in chronic anxiety
Shekhar, A., Truitt, W., Rainnie, D., & Sajdyk, T. (2005) · Stress · doi:10.1080/10253890500504557 · Cited by 237 · see citing works
Neural Regulation of the Stress Response: The Many Faces of Feedback
Myers, B., McKlveen, J. M., & Herman, J. P. (2012) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-012-9801-y · Cited by 175 · see citing works
Makino, S., Shibasaki, T., Yamauchi, N., Nishioka, T., Mimoto, T., Wakabayashi, I., Gold, P. W., & Hashimoto, K. (1999) · Brain Research · doi:10.1016/s0006-8993(99)02114-9 · Cited by 168 · see citing works
Hsu, D. T., Chen, F.-L., Takahashi, L. K., & Kalin, N. H. (1998) · Brain Research · doi:10.1016/s0006-8993(98)00032-8 · Cited by 154 · see citing works
Induction and adaptation of Fos expression in the rat brain by two types of acute restraint stress
Mohammad, G., Chowdhury, I., Fujioka, T., & Nakamura, S. (2000) · Brain Research Bulletin · doi:10.1016/s0361-9230(00)00231-8 · Cited by 153 · see citing works
Stretch activates heparin-binding EGF-like growth factor expression in bladder smooth muscle cells
Park, J. M., Borer, J. G., Freeman, M. R., et al. (1998) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1998.275.5.c1247 · Cited by 140 · see citing works
Marchant, N. J., Densmore, V. S., & Osborne, P. B. (2007) · The Journal of Comparative Neurology · doi:10.1002/cne.21464 · Cited by 123 · see citing works
Pitts, M. W., Todorovic, C., Blank, T., & Takahashi, L. K. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.0740-09.2009 · Cited by 90 · see citing works
Gastric acid secretion and lesion formation in rats under water-immersion stress
Hayase, M., & Takeuchi, K. (1986) · Digestive Diseases and Sciences · doi:10.1007/bf01300703 · Cited by 75 · see citing works
Wang, S.-S., Xue-bo, Y., Hofman, M. A., Swaab, D. F., & Zhou, J. (2010) · Neuroscience Bulletin · doi:10.1007/s12264-010-0329-1 · Cited by 73 · see citing works
Corticotropin releasing factor in neuroplasticity
Regev, L., & Baram, T. Z. (2013) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2013.10.001 · Cited by 71 · see citing works
Role of Anxiety in the Pathophysiology of Irritable Bowel Syndrome: Importance of the Amygdala
Myers, B., & Meerveld, B. G. (2009) · Frontiers in Neuroscience · doi:10.3389/neuro.21.002.2009 · Cited by 70 · see citing works
Furlong, T. M., McDowall, L. M., Horiuchi, J., Polson, J. W., & Dampney, R. A. L. (2014) · European Journal of Neuroscience · doi:10.1111/ejn.12521 · Cited by 68 · see citing works
Cruz, M. T., Murphy, E. C., Sahibzada, N., et al. (2006) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00863.2005 · Cited by 62 · see citing works
Current concepts in gastric microcirculatory pathophysiology.
Ph, G. (1994) · PubMed · Cited by 59 · see citing works
Zhou, S.-Y., Lu, Y.-X., Yao, H., & Owyang, C. (2008) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00309.2006 · Cited by 53 · see citing works
Gastric mucosal ulceration associated with electrochemical stimulation of the limbic brain
Innes, D. L., & Tansy, M. F. (1980) · Brain Research Bulletin · doi:10.1016/0361-9230(80)90300-7 · Cited by 52 · see citing works
Recent studies of the central nucleus of the amygdala and stress ulcers
Henke, P. G. (1988) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(88)80006-x · Cited by 49 · see citing works
Henke, P. G., Ray, A., & Sullivan, R. M. (1991) · Digestive Diseases and Sciences · doi:10.1007/bf01296409 · Cited by 48 · see citing works
Analysis of the cold-water restraint procedure in gastric ulceration and body temperature
Landeira-Fernández, J. (2004) · Physiology & Behavior · doi:10.1016/j.physbeh.2004.06.016 · Cited by 44 · see citing works
Su, J., Tanaka, Y., Muratsubaki, T., Kano, M., Kanazawa, M., & Fukudo, S. (2014) · Neurogastroenterology & Motility · doi:10.1111/nmo.12462 · Cited by 44 · see citing works
Lyubashina, O. A., Jolkkonen, E., & Pitkänen, A. (2000) · Neuroscience Letters · doi:10.1016/s0304-3940(00)01392-6 · Cited by 43 · see citing works
Niedringhaus, M. S., Jackson, P. G., Evans, S. R. T., Verbalis, J. G., Gillis, R. A., & Sahibzada, N. (2007) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00391.2007 · Cited by 40 · see citing works
Zhang, X., Cui, J., Tan, Z. T., Jiang, C., & Fogel, R. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2003.045906 · Cited by 37 · see citing works
Ray, A., & Henke, P. G. (1990) · Behavioural Brain Research · doi:10.1016/0166-4328(90)90172-b · Cited by 33 · see citing works
Neurons in Primary Motor Cortex Encode Hand Orientation in a Reach-to-Grasp Task
Ma, C., Ma, X., Fan, J., et al. (2017) · Neuroscience Bulletin · doi:10.1007/s12264-017-0126-1 · Cited by 33 · see citing works
Zhao, D., & Hong-bin, A. (2011) · PLoS ONE · doi:10.1371/journal.pone.0023362 · Cited by 31 · see citing works
Helfferich, F., & Palkovits, M. (2003) · Brain Research · doi:10.1016/s0006-8993(03)02509-5 · Cited by 30 · see citing works
Geng, X., Xie, J., Wang, X., et al. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2016.02.026 · Cited by 30 · see citing works
Self-citationHenke, P. G., Sullivan, R. M., & Ray, A. (1988) · Neuroscience Letters · doi:10.1016/0304-3940(88)90255-8 · Cited by 28 · see citing works
How precise is the timing of action potentials?
Kirst, C. (2009) · Frontiers in Neuroscience · doi:10.3389/neuro.01.009.2009 · Cited by 26 · see citing works
The GABA/benzodiazepine receptor complex in the central amygdalar nucleus and stress ulcers in rats
Sullivan, R. M., Henke, P. G., Ray, A., Hebert, M. A., & Trimper, J. M. (1989) · Behavioral and Neural Biology · doi:10.1016/s0163-1047(89)90902-3 · Cited by 22 · see citing works
Zhang, Y.-Y., Zhu, W.-X., Cao, G.-H., et al. (2009) · The Journal of Physiological Sciences · doi:10.1007/s12576-009-0044-8 · Cited by 22 · see citing works
Sun, H., Zheng, S., Lu, K., et al. (2017) · World Journal of Gastroenterology · doi:10.3748/wjg.v23.i1.87 · Cited by 19 · see citing works
Wang, M., Qu, Q., He, T., Li, M., Song, Z., Chen, F., Zhang, X., Xie, J., Geng, X., Yang, M., et al. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2016.05.031 · Cited by 16 · see citing works
Self-citationGao, H.-R., Zhuang, Q., Zhang, Y.-X., Chen, Z., Li, B., Zhang, X., Zhong, Y.-T., Wang, J.-J., & Zhu, J. (2017) · Neuroscience Bulletin · doi:10.1007/s12264-017-0127-0 · Cited by 16 · see citing works
Amygdalofugal modulation of the vago-vagal gastric motor reflex in rat
Любашина, О. А., Bagaev, V. A., & Khotiantsev, S. (2002) · Neuroscience Letters · doi:10.1016/s0304-3940(02)00289-6 · Cited by 15 · see citing works
Sun, H., Liu, Z., & Ma, X. (2015) · Neuroreport · doi:10.1097/wnr.0000000000000515 · Cited by 13 · see citing works
Welkenhuysen, M., Gligorijević, I., Ameye, L., Prodanov, D., Huffel, S. V., & Nuttin, B. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.11.019 · Cited by 10 · see citing works
HE, F., & Ai, H. ‐. (2016) · Physiological Research · doi:10.33549/physiolres.933125 · Cited by 7 · see citing works
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A dual-pathway architecture for stress to disrupt agency and promote habit
Giovanniello, J. R., Paredes, N., Wiener, A., Ramírez-Armenta, K., Oragwam, C., Uwadia, H. O., Yu, A. L., Lim, K., Pimenta, J. S., Vilchez, G. E., et al. (2025) · Nature · doi:10.1038/s41586-024-08580-w · Cited by 30 · see citing works
- Authors
- He, F., Ai, H., Wang, M., Wang, X., & Geng, X.
- Affiliations
- Shandong Normal University (CN)
- Qilu University of Technology (CN)
- Corresponding author
- He, Feng
- ORCID
- Venue
- Neuroscience Bulletin
- Published
- 2018-08-31
- Volume
- 34
- Issue
- 6
- Pages
- 1067-1076
- ISSN
- 1995-8218 (ISSN-L)
- 1673-7067
- PMC
- PMC6246852
- OpenAlex
- W2889133039
- Cited by
- 15
- References
- 55
- Citations by year
- 2025: 3 · 2023: 1 · 2022: 2 · 2021: 1 · 2020: 5 · 2019: 3
- FWCI
- 1.30
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Neuroscience Bulletin (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, other-oa)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Funders
- National Natural Science Foundation of China (81501149, 31571104)
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Keywords
- restraint stress, central amygdala, gastric ulcer, Fos expression, corticotropin-releasing hormone neurons, neuronal firing properties
- MeSH terms
- Action Potentials, Analysis of Variance, Animals, Corticotropin-Releasing Hormone, Disease Models, Animal, Gastric Mucosa, Gene Expression Regulation, Neurons, Stress, Physiological, Stress, Psychological, Proto-Oncogene Proteins c-fos, Rats, Wistar, Patch-Clamp Techniques, Rats, Central Amygdaloid Nucleus
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