Hypothalamic oxytocin mediates adaptation mechanism against chronic stress in rats
Open accessAbstract
Accumulation of continuous life stress (chronic stress) often causes gastric symptoms. Although central oxytocin has antistress effects, the role of central oxytocin in stress-induced gastric dysmotility remains unknown. Solid gastric emptying was measured in rats receiving acute restraint stress, 5 consecutive days of repeated restraint stress (chronic homotypic stress), and 7 consecutive days of varying types of stress (chronic heterotypic stress). Oxytocin and oxytocin receptor antagonist were administered intracerebroventricularly (icv). Expression of corticotropin-releasing factor (CRF) mRNA and oxytocin mRNA in the paraventricular nucleus (PVN) of the hypothalamus was evaluated by real-time RT-PCR. The changes of oxytocinergic neurons in the PVN were evaluated by immunohistochemistry. Acute stress delayed gastric emptying, and the delayed gastric emptying was completely restored after 5 consecutive days of chronic homotypic stress. In contrast, delayed gastric emptying persisted following chronic heterotypic stress. The restored gastric emptying following chronic homotypic stress was antagonized by icv injection of an oxytocin antagonist. Icv injection of oxytocin restored delayed gastric emptying induced by chronic heterotypic stress. CRF mRNA expression, which was significantly increased in response to acute stress and chronic heterotypic stress, returned to the basal levels following chronic homotypic stress. In contrast, oxytocin mRNA expression was significantly increased following chronic homotypic stress. The number of oxytocin-immunoreactive cells was increased following chronic homotypic stress at the magnocellular part of the PVN. Icv injection of oxytocin reduced CRF mRNA expression induced by acute stress and chronic heterotypic stress. It is suggested that the adaptation mechanism to chronic stress may involve the upregulation of oxytocin expression in the hypothalamus, which in turn attenuates CRF expression.
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Animal studies have demonstrated that oxytocin plays an important role in lowering the physiological stress and anxiety response by activating a negative feedback loop.
“Animal studies have demonstrated that oxytocin plays an important role in lowering the physiological stress and anxiety response by activating a negative feedback loop (Onaka et al., 2012;Zheng et al., 2010).”
From Meta-analytic review of the effects of a single dose of intranasal oxytocin on threat processing in humans (2018) · cites this paper as Zheng et al., 2010
Elevated oxytocin secretion from the paraventricular nucleus of the hypothalamus following a stressful event is believed to lead to increased availability of gamma-aminobutyric acid (GABA), which in turn is believed to inhibit the HPA axis and amygdala activation.
“Elevated oxytocin secretion from the paraventricular nucleus of the hypothalamus following a stressful event is believed to lead to increased availability of gamma-aminobutyric acid (GABA), which in turn is believed to inhibit the HPA axis and amygdala activation (Onaka et al., 2012;Zheng et al., 2010).”
From Meta-analytic review of the effects of a single dose of intranasal oxytocin on threat processing in humans (2018) · cites this paper as Zheng et al., 2010
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“…(Ditzen et al., 2009, Heinrichs et al., 2003, Linnen et al., 2012, Parker et al., 2005, Quirin et al., 2011), ICV (Bulbul et al., 2011, Lukas et al., 2011, Norman et al., 2010, Windle et al., 2004, Windle et al., 1997, Zheng et al., 2010), and intraPVN (Blume et al., 2008, Smith & Wang, 2014b)).”
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“Indeed, it is well accepted that central application of OXT has anxiolytic effects, attenuates activation of the hypothalamic-pituitary-adrenal axis in response to chronic stress and mediates adaptation to repeated restraint stress in mice (Windle et al. 2004; Neumann, 2008; Babygirija et al. 2010; Zheng et al. 2010).”
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BackgroundOxytocin Release during the Meditation of Altruism and Appreciation (Arigato-Zen)
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Takahashi, T. (2021) · Frontiers in Psychology · doi:10.3389/fpsyg.2020.588068 · Cited by 42 · see citing works
“Accelerated colonic transit and delayed gastric emptying induced by stress are attenuated by intracerebroventricular (icv)-injection of OT in rodents (Zheng et al., 2010; Yoshimoto et al., 2012).”
BackgroundGołyszny, M. J., Obuchowicz, E., & Zielinski, M. W. (2021) · Neuropeptides · doi:10.1016/j.npep.2021.102216 · Cited by 41 · see citing works
Borrow, A. P., Bales, N. J., Stover, S. A., & Handa, R. J. (2018) · Endocrinology · doi:10.1210/en.2018-00217 · Cited by 39 · see citing works
Yee, J. R., Kenkel, W. M., Frijling, J. L., Dodhia, S., Onishi, K. G., Tovar, S., Saber, M. J., Lewis, G. F., Liu, W., Porges, S. W., et al. (2016) · Hormones and Behavior · doi:10.1016/j.yhbeh.2016.01.010 · Cited by 39 · see citing works
“…et al., 1999; Windle et al., 2004; Windle et al., 1997; Babygirija et al., 2012; Blume et al., 2008; Bülbül et al., 2011; Jurek et al., 2015; Zheng et al., 2010), mice made mutant for OXT (Amico et al., 2008), prairie voles (Smith et al., 2015; Smith and Wang, 2014), and humans (Heinrichs…”
BackgroundJiang, Y., & Travagli, R. A. (2020) · The Journal of Physiology · doi:10.1113/jp280023 · Cited by 38 · see citing works
“Previous studies (Zheng et al. 2010) have shown that exogenous administration of an OXT receptor antagonist prevented the restoration of the delayed gastric emptying observed following chronic homotypic”
BackgroundResultInfluentialYoshimoto, S., Babygirija, R., Dobner, A., Ludwig, K., & Takahashi, T. (2012) · Digestive Diseases and Sciences · doi:10.1007/s10620-012-2040-8 · Cited by 37 · see citing works
“The distinction between parvocellular and magnocellular subdivisions in the PVN was performed, as previously reported [9, 14].”
BackgroundMethodInfluentialBrowning, K. N., Babic, T., Toti, L., Holmes, G. M., Coleman, F. H., & Travagli, R. A. (2014) · The Journal of Physiology · doi:10.1113/jphysiol.2014.278192 · Cited by 37 · see citing works
“Hypothalamic OXT is important in the normalization and recovery of gastric and colonic motility following adaptation to stress (Babygirija et al. 2010a,b, 2011; Bulbul et al. 2010; Zheng et al. 2010).”
BackgroundInfluentialActivation of Brain Somatostatin Signaling Suppresses CRF Receptor-Mediated Stress Response
Stengel, A., & Taché, Y. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2017.00231 · Cited by 36 · see citing works
“Among them, the activation of brain neuropeptide Y1 and oxytocin receptors have been implicated in stress adaptation processes as recently reviewed (Zheng et al., 2010; Reichmann and Holzer, 2016).”
BackgroundOxytocin attenuates social and non-social avoidance: Re-thinking the social specificity of Oxytocin
Harari-Dahan, O., & Bernstein, A. (2017) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2017.04.005 · Cited by 34 · see citing works
“The GAAO is grounded in behavioral (e.g. De Dreu and Kret, 2016; De Dreu et al., 2014; Zheng et al., 2010), psychophysiological (e.g. Kubzansky et al., 2012), neurobiological (e.g. Huber et al., 2005), and neuroimaging (e.g. Kirsch et al., 2005) studies in animal and human research (see…”
InfluentialOxytocin and parenting behavior among impoverished mothers with low vs. high early life stress
Julian, M. M., Rosenblum, K. L., Doom, J. R., Leung, C. Y. Y., Lumeng, J. C., Cruz, M. G., Vázquez, D. M., & Miller, A. L. (2017) · Archives of Women s Mental Health · doi:10.1007/s00737-017-0798-6 · Cited by 34 · see citing works
“The early social context has been associated with individual differences in oxytocin release and its role in mediating or buffering distress (Bartz et al. 2011b; Neumann 2007; Uvnäs-Moberg 1998; Wismer Fries et al. 2005; Zheng et al. 2010).”
Social interaction attenuates stress responses following chronic stress in maternally separated rats
Babygirija, R., Yoshimoto, S., Gribovskaja‐Rupp, I., Bülbül, M., Ludwig, K., & Takahashi, T. (2012) · Brain Research · doi:10.1016/j.brainres.2012.06.007 · Cited by 32 · see citing works
Central apelin mediates stress-induced gastrointestinal motor dysfunction in rats
Bülbül, M., Izgut-Uysal, V. N., Sinen, O., Birsen, İ., & Tanrιöver, G. (2015) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00145.2015 · Cited by 31 · see citing works
Neuroprotective effects of melatonin administration against chronic immobilization stress in rats.
Gomaa, A. M. S., Galal, H. M., & Abou-Elgait, A. T. (2017) · PubMed Central · Cited by 31 · see citing works
Sustained Delayed Gastric Emptying During Repeated Restraint Stress in Oxytocin Knockout Mice
Babygirija, R., Zheng, J., Bülbül, M., Cerjak, D., Ludwig, K., & Takahashi, T. (2010) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2010.02069.x · Cited by 30 · see citing works
Gatta, E., Mairesse, J., Deruyter, L., Marrocco, J., Camp, G. V., Bouwalerh, H., Lo‐Guidice, J., Morley‐Fletcher, S., Nicoletti, F., & Maccari, S. (2018) · NeuroToxicology · doi:10.1016/j.neuro.2018.04.005 · Cited by 29 · see citing works
Mooney, S. J., & Holmes, M. M. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.11.014 · Cited by 27 · see citing works
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Minhas, S., Liu, C. M., Galdamez, J., So, V. M., & Romeo, R. D. (2016) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2016.03.014 · Cited by 26 · see citing works
“Conversely, oxytocin has been implicated in potentiating the effects of CRH on ACTH release from the anterior pituitary (Gibbs et al., 1984).”
BackgroundThe Psyche and Gastric Functions
Nardone, G., & Compare, D. (2014) · Digestive Diseases · doi:10.1159/000357851 · Cited by 28 · see citing works
Bülbül, M., Babygirija, R., Cerjak, D., Yoshimoto, S., Ludwig, K., & Takahashi, T. (2012) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00447.2011 · Cited by 26 · see citing works
“6 mm ventral to the brain surface), as previously reported (71).”
BackgroundMethodInfluentialBabygirija, R., Bülbül, M., Cerjak, D., Ludwig, K., & Takahashi, T. (2011) · Neuroscience Letters · doi:10.1016/j.neulet.2011.03.045 · Cited by 25 · see citing works
Hypothalamic circuit regulating colonic transit following chronic stress in rats
Yoshimoto, S., Cerjak, D., Babygirija, R., Bülbül, M., Ludwig, K., & Takahashi, T. (2011) · Stress · doi:10.3109/10253890.2011.614297 · Cited by 24 · see citing works
“5mg) completely reversed inhibitory effects of acute restraint stress on gastric emptying in rats (Zheng et al. 2010).”
BackgroundMethodInfluentialStress Adaptation Upregulates Oxytocin within Hypothalamo-Vagal Neurocircuits
Jiang, Y., Coleman, F. H., Doheny, K. K., & Travagli, R. A. (2018) · Neuroscience · doi:10.1016/j.neuroscience.2018.08.021 · Cited by 24 · see citing works
“In a series of brilliant experiments, Takahashi’s group correlated the GI adaptive changes observed upon chronic homotypic stress to increased levels of OXT-IR and OXT mRNA containing neurons in the PVN (Zheng et al., 2010; Babygirija et al., 2012).”
BackgroundInfluentialElectro-acupuncture improves the social interaction behavior of rats
Zhang, H., Li, H.-X., Dai, Y., Xu, X., Han, S., Zhang, R., & Han, J. (2015) · Physiology & Behavior · doi:10.1016/j.physbeh.2015.08.014 · Cited by 24 · see citing works
“Additionally, it is well known that OXT/AVP systems could be affected by acute or chronic restraint stress [28] [29], as well as other types of stressors such as forced swimming [30], dehydration [31] or electric footshock [32].”
Ji, N., Kang, J., Hua, R., & Zhang, Y. (2018) · Neurological Research · doi:10.1080/01616412.2018.1460702 · Cited by 22 · see citing works
“Other studies have also demonstrated that the animal model of pain results in depression-like activity in behavioral tests [20,21].”
ResultEffects of atosiban on stress-related neuroendocrine factors
Babic, S., Pokusa, M., Danevova, V., Ding, S., & Ježová, D. (2015) · Journal of Endocrinology · doi:10.1530/joe-14-0560 · Cited by 22 · see citing works
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Hou, W., He, Z., Yang, Y., Yuan, W., Wang, L., Zhang, J., Zhang, X., Cai, W., Guo, Q., & Tai, F. (2020) · European Journal of Neuroscience · doi:10.1111/ejn.14691 · Cited by 21 · see citing works
“The administration of an OTR agonist or antagonist by icv. or local injection (in the PVN, central amygdala and prefrontal cortex) consistently produces an anxiolytic effect similar to that of synthetic or endogenous OT in male and female rodents, especially during periods of robust activation and increased central re…”
BackgroundInfluentialLi, J., Li, H.-X., Shou, X., Xu, X., Song, T.-J., Han, S., Zhang, R., & Han, J. (2016) · Neuropeptides · doi:10.1016/j.npep.2016.08.011 · Cited by 21 · see citing works
“For instance, a number of recent studies have shown that restraint stress induces c-fos expression in oxytocinergic neurons in PVN in rats (Miyata et al., 1995; Zheng et al., 2010; Yoshimoto et al., 2012).”
InfluentialOxytocin Signaling Acts as a Marker for Environmental Stressors in Zebrafish
Chuang, H.-J., Chang, C.-Y., Ho, H.-P., & Chou, M. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22147459 · Cited by 18 · see citing works
“Under chronic homotypic stress, the number of oxytocin neurons in the PVN also increased [65,66].”
BackgroundStengel, A., Goebel‐Stengel, M., Wang, L., et al. (2011) · Neurogastroenterology & Motility · doi:10.1111/j.1365-2982.2011.01706.x · Cited by 18 · see citing works
Yu, Y., Yu, H., Babygirija, R., et al. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.629003 · Cited by 17 · see citing works
Effects of Stresscopin on Rat Hypothalamic Paraventricular Nucleus Neurons In Vitro
Chu, C., Jin, W.-Z., Bing, Y.-H., Jin, Q.-H., Kannan, H., & Qiu, D. (2013) · PLoS ONE · doi:10.1371/journal.pone.0053863 · Cited by 17 · see citing works
“Intracerebroventricular injection of OT significantly attenuates the increase in CRF mRNA expression in the PVN induced by restraint stress [40].”
BackgroundFulenwider, H. D., Zhang, Y., & Ryabinin, A. E. (2023) · Hormones and Behavior · doi:10.1016/j.yhbeh.2023.105452 · Cited by 15 · see citing works
The Role of the Oxytocin/Arginine Vasopressin System in Animal Models of Autism Spectrum Disorder
Zhang, R., Xu, X., Zhang, H.-F., Han, S., & Han, J. (2017) · Advances in anatomy, embryology and cell biology · doi:10.1007/978-3-319-52498-6_8 · Cited by 16 · see citing works
Bülbül, M., Sinen, O., Gemici, B., & Izgut-Uysal, V. N. (2016) · Peptides · doi:10.1016/j.peptides.2016.11.001 · Cited by 14 · see citing works
Babygirija, R., Cerjak, D., Yoshimoto, S., Gribovskaja‐Rupp, I., Bülbül, M., Ludwig, K., & Takahashi, T. (2012) · Autonomic Neuroscience · doi:10.1016/j.autneu.2012.03.001 · Cited by 14 · see citing works
“To mimic complex stress exposure in humans, we utilized chronic stress models in rats (Choudhury et al., 2009; Zheng et al., 2010).”
BackgroundMethodResultInfluentialVagally mediated gastric effects of brain stem α2-adrenoceptor activation in stressed rats
Jiang, Y., Browning, K. N., Toti, L., & Travagli, R. A. (2018) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00382.2017 · Cited by 14 · see citing works
Can oxytocin inhibit stress-induced hyperalgesia?
Li, Y.-X., An, H. Y., Wen, Z., Tao, Z.-Y., & Cao, D. (2019) · Neuropeptides · doi:10.1016/j.npep.2019.101996 · Cited by 13 · see citing works
Yu, Y., Yu, H., Babygirija, R., Shi, B., Sun, W., Zheng, X., & Zheng, J. (2019) · Journal of Neurogastroenterology and Motility · doi:10.5056/jnm19065 · Cited by 12 · see citing works
“For CCS loading, the rats (n = 6-8) received different types of stressors for 7 consecutive days, as previously reported.(8) The stress paradigms used were fasten restraint stress (FRS), force swimming stress (FSS), cold restraint stress (CRS), and water avoidance stress (WAS).”
BackgroundMethodResultInfluentialKanada, Y., Katayama, A., Ikemoto, H., Takahashi, K., Tsukada, M., Nakamura, A., Ishino, S., Hisamitsu, T., & Sunagawa, M. (2018) · Neuropsychiatric Disease and Treatment · doi:10.2147/ndt.s156795 · Cited by 10 · see citing works
“These doses were determined by referring to a previous study.(24) It was reported that intraperitoneal administration of OT (500 pmol per rat) inhibited water-avoidance stress-induced colonic contraction in rats.”
BackgroundLuna, D., Calderón-Amor, J., González, C., Byrd, C. J., Palomo, R., Huenul, E., & Figueroa, J. (2024) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2024.106221 · Cited by 10 · see citing works
Dual autonomic inhibitory action of central Apelin on gastric motor functions in rats
Bülbül, M., & Sinen, O. (2018) · Autonomic Neuroscience · doi:10.1016/j.autneu.2018.03.005 · Cited by 10 · see citing works
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“Other experiments in rodents revealed that repeated defeat experiences increased the number of oxytocinergic neurons in the PVN as well as after chronic homotypic stress [107,108].”
BackgroundJovanović, P., Stefanović, B., Spasojević, N., Puškaš, N., & Dronjak, S. (2016) · Endocrine Research · doi:10.3109/07435800.2015.1094086 · Cited by 9 · see citing works
“The results of some other authors also suggest that oxytocin plays a pivotal role in mediating the adaptation mechanism in animals following chronic stress (37,38).”
ResultMagnetic Resonance Imaging of Gastric Motility in Conscious Rats
Wang, X., Alkaabi, F., Cornett, A. M., Choi, M., Scheven, U. M., Natale, M. R. D., Furness, J. B., & Liu, Z. (2024) · Neurogastroenterology & Motility · doi:10.1111/nmo.14982 · Cited by 6 · see citing works
“The acclimation involves repeatedly handling and restraining rats over multiple days, facilitating their adaptation [57, 58] and avoiding GI complications due to acute stress [59–63].”
Glucocorticoids and the Intestinal Environment
Ünsal, H., & Balkay, M. (2012) · InTech eBooks · doi:10.5772/51977 · Cited by 6 · see citing works
“Generally, intestinal ion secretion [40,59], macromolecular permeability [60,61], inflammation [40,59], visceral hypersensivity and colonic motility increased [40], while gastric motility decreased in various animal models of stress [62-64].”
BackgroundWhy is pharma so scared of psychiatric drug discovery?
Tricklebank, M. D., & Ajram, L. A. (2017) · doi:10.35841/neuroscience.1.1.1-4 · Cited by 6 · see citing works
“A study by Zhang et al, reasoned that it is the CRF receptors in a specific area of the hypothalamus (Para ventricular nucleus) which are markedly involved in controlling CRF secretion [24].”
BackgroundStress-induced neuroplasticity in the gastric response to brainstem oxytocin in male rats
Jiang, Y., Zimmerman, J. E., Browning, K. N., et al. (2022) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00347.2021 · Cited by 5 · see citing works
Xie, D., Yang, X., Cao, C.-Y., Wang, H., Li, Y., Qin, Y., Zhang, J., & Chang, X.-W. (2011) · Regulatory Peptides · doi:10.1016/j.regpep.2011.08.003 · Cited by 5 · see citing works
“Real time-PCR study showed that OT mRNA expression is upregulated in the paraventricular nucleus of the hypothalamus following chronic homotypic stress in rats [21].”
Oxytocin und die suchterhaltenden Mechanismen der Alkoholabhängigkeit
Faehrmann, T., Zernig, G., & Mechtcheriakov, S. (2017) · Neuropsychiatrie · doi:10.1007/s40211-017-0229-y · Cited by 5 · see citing works
“Hohe Oxytocinspiegel sind demnach mit erniedrigten CRFSpiegeln assoziiert [32].”
BackgroundInfluentialDelaCuesta-Barrutia, J., Hidema, S., Caldwell, H. K., Nishimori, K., Erdozain, A. M., & Peñagarikano, O. (2024) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2024.03.028 · Cited by 4 · see citing works
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“However, oxytocin can also restore gastric motility and reverse the delay in gastric emptying that is caused by stress (31, 66, 78).”
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“Delayed gastric emptying and accelerated colonic transit induced by acute restraint stress are abolished by intracerebroventricular (icv)-injection of OXT in rats([11,12]).”
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Malocclusion impairs cognitive behavior via AgRP signaling in adolescent mice
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“Although malocclusion is a stressor, no hypothalamic CRF mRNA upregulation was observed in the Malocclusion/powder group here.”
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The Neuroendocrine and Cardiovascular Responses to a Pup in Male Prairie Voles (M. ochrogaster)
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Oxytocin, Social Interactions and Coping: Implications for Depression
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- Authors
- Zheng, J., Babygirija, R., Bülbül, M., Cerjak, D., Ludwig, K., & Takahashi, T.
- Affiliations
- Medical College of Wisconsin (US)
- Corresponding author
- Takahashi, Toku
- Venue
- American Journal of Physiology-Gastrointestinal and Liver Physiology
- Publisher
- American Physiological Society
- Published
- 2010-10
- Volume
- 299
- Issue
- 4
- Pages
- G946-G953
- ISSN
- 0193-1857 (ISSN-L)
- 1522-1547
- PMC
- PMC2957337
- OpenAlex
- W2143119886
- Cited by
- 104
- References
- 53
- Citations by year
- 2026: 2 · 2024: 7 · 2023: 3 · 2022: 3 · 2021: 6 · 2020: 3 · 2019: 5 · 2018: 12 · 2017: 10 · 2016: 7 · 2015: 9 · 2014: 8 · 2013: 7 · 2012: 8
- FWCI
- 12.24
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- American Journal of Physiology-Gastrointestinal and Liver Physiology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Diabetes and Digestive and Kidney Diseases (R01 DK 62768, R01DK062768)
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Keywords
- chronic stress, stress adaptation, gastric emptying, corticotropin-releasing factor, paraventricular nucleus, hypothalamus, oxytocin receptor antagonist, magnocellular neurons, acute restraint stress
- MeSH terms
- Animals, Brain, Brain Chemistry, Chronic Disease, Gene Expression Regulation, Hypothalamus, Immunohistochemistry, Injections, Intraventricular, Male, Oxytocics, Oxytocin, Restraint, Physical, RNA, Messenger, Stress, Physiological, Rats, Sprague-Dawley, Receptors, Oxytocin, Rats
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