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Early-Life Stress Disrupts Attachment Learning: The Role of Amygdala Corticosterone, Locus Ceruleus Corticotropin Releasing Hormone, and Olfactory Bulb Norepinephrine
Emotional Brain Institute, Nathan Kline Institute, Orangeburg, New York, USA, / Child and Adolescent Psychiatry, Child Study Center, New York University Langone Medical Center, New York, New York, USA, Department of Zoology, University of Oklahoma, Norman, Oklahoma, USA.
Department of Zoology, University of Oklahoma, Norman, Oklahoma, USA / Laboratory Neurosciences Sensorielles, Centre National de la Recherche Scientifique, Universite Lyon, 69007 Lyon, France.
Department of Zoology, University of Oklahoma, Norman, Oklahoma, USA / National Institutes of Health, Bethesda, Maryland, USA.
Emotional Brain Institute, Nathan Kline Institute, Orangeburg, New York, USA / Child and Adolescent Psychiatry, Child Study Center, New York University Langone Medical Center, New York, New York, USA / New York University Center for Neural Science, New York, New York, USA / Department of Zoology, University of Oklahoma, Norman, Oklahoma, USA.
2009 (English)In: Journal of Neuroscience, ISSN 0270-6474, E-ISSN 1529-2401, Vol. 29, no 50, p. 15745-15755Article in journal (Refereed) Published
Abstract [en]

Infant rats require maternal odor learning to guide pups’ proximity-seeking of the mother and nursing. Maternal odor learning occurs using a simple learning circuit including robust olfactory bulb norepinephrine (NE), release from the locus ceruleus (LC), and amygdala suppression by low corticosterone (CORT). Early-life stress increases NE but also CORT, and we questioned whether early-life stress disrupted attachment learning and its neural correlates [2-deoxyglucose (2-DG) autoradiography]. Neonatal rats were normally reared or stressed-reared during the first 6 d of life by providing the mother with insufficient bedding for nest building and were odor–0.5 mA shock conditioned at 7 d old. Normally reared paired pups exhibited typical odor approach learning and associated olfactory bulb enhanced 2-DG uptake. However, stressed-reared pups showed odor avoidance learning and both olfactory bulb and amygdala 2-DG uptake enhancement. Furthermore, stressed-reared pups had elevated CORT levels, and systemic CORT antagonist injection reestablished the age-appropriate odor-preference learning, enhanced olfactory bulb, and attenuated amygdala 2-DG. We also assessed the neural mechanism for stressed-reared pups’ abnormal behavior in a more controlled environment by injecting normally reared pups with CORT. This was sufficient to produce odor aversion, as well as dual amygdala and olfactory bulb enhanced 2-DG uptake. Moreover, we assessed a unique cascade of neural events for the aberrant effects of stress rearing: the amygdala–LC–olfactory bulb pathway. Intra-amygdala CORT or intra-LC corticotropin releasing hormone (CRH) infusion supported aversion learning with intra-LC CRH infusion associated with increased olfactory bulb NE (microdialysis). These results suggest that early-life stress disturbs attachment behavior via a unique cascade of events (amygdala–LC–olfactory bulb).

Place, publisher, year, edition, pages
Washington, United States: Society for Neuroscience , 2009. Vol. 29, no 50, p. 15745-15755
National Category
Neurosciences
Identifiers
URN: urn:nbn:se:liu:diva-150384DOI: 10.1523/JNEUROSCI.4106-09.2009ISI: 000272837000016PubMedID: 20016090Scopus ID: 2-s2.0-72449201112OAI: oai:DiVA.org:liu-150384DiVA, id: diva2:1240544
Note

This work was funded by National Institutes of Health Grants DC003906 and DC009910, National Science Foun-dation Grant IOB0850527, the Leon Levy Foundation, and the Hope for Depression Foundation (R.M.S.).

Available from: 2018-08-21 Created: 2018-08-21 Last updated: 2018-08-29Bibliographically approved

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Shionoya, Kiseko

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