Rodent model of infant attachment learning and stress
Open accessAbstract
Here we review the neurobiology of infant odor learning in rats, and discuss the unique role of the stress hormone corticosterone (CORT) in the learning necessary for the developing rat. During the first 9 postnatal (PN) days, infants readily learn odor preferences, while aversion and fear learning are attenuated. Such restricted learning may ensure that pups only approach their mother. This sensitive period of preference learning overlaps with the stress hyporesponsive period (SHRP, PN4–14) when pups have a reduced CORT response to most stressors. Neural underpinnings responsible for sensitive‐period learning include increased activity within the olfactory bulb and piriform “olfactory” cortex due to heightened release of norepinephrine from the locus coeruleus. After PN10 and with the decline of the SHRP, stress‐induced CORT release permits amygdala activation and facilitates learned odor aversions and fear. Remarkably, odor preference and attenuated fear learning can be reestablished in PN10–15 pups if the mother is present, an effect due to her ability to suppress pups' CORT and amygdala activity. Together, these data indicate that functional changes in infant learning are modified by a unique interaction between the developing CORT system, the amygdala, and maternal presence, providing a learning system that becomes more flexible as pups mature. © 2010 Wiley Periodicals, Inc. Dev Psychobiol 52: 651–660, 2010.
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Maternal separation in rodent pups is associated with greater LHPA axis reactivity.
“Maternal separation in rodent pups is associated with greater LHPA axis reactivity (Moriceau et al., 2010), accelerated amygdala development (Moriceau and Sullivan, 2006, Ono et al., 2008), increased anxiety-like behaviors (Romeo et al., 2003), and more social instability in adulthood (Kikusui and Mori, 2009).”
From The impact of developmental timing for stress and recovery (2015) · cites this paper as Moriceau et al., 2010
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Hostinar, C. E., Sullivan, R. M., & Gunnar, M. R. (2014) · Psychological Bulletin · doi:10.1037/a0032671 · Cited by 739 · see citing works
Self-citationGee, D. G., Gabard-Durnam, L., Telzer, E. H., Humphreys, K. L., Goff, B., Shapiro, M., Flannery, J., Lumian, D. S., Fareri, D. S., Caldera, C., et al. (2014) · Psychological Science · doi:10.1177/0956797614550878 · Cited by 363 · see citing works
The impact of developmental timing for stress and recovery
Gee, D. G., & Casey, B. J. (2015) · Neurobiology of Stress · doi:10.1016/j.ynstr.2015.02.001 · Cited by 245 · see citing works
“Maternal separation in rodent pups is associated with greater LHPA axis reactivity (Moriceau et al., 2010), accelerated amygdala development (Moriceau and Sullivan, 2006; Ono et al., 2008), increased anxiety-like behaviors (Romeo et al., 2003), and more social instability in adulthood (Kikusui and…”
BackgroundBradley, B., Westen, D., Mercer, K. B., Binder, E. B., Jovanovic, T., Crain, D., Wingo, A., & Heim, C. (2011) · Development and Psychopathology · doi:10.1017/s0954579411000162 · Cited by 213 · see citing works
Gunnar, M. R., Hostinar, C. E., Sanchez, M. M., Tottenham, N., & Sullivan, R. M. (2015) · Social Neuroscience · doi:10.1080/17470919.2015.1070198 · Cited by 158 · see citing works
Self-citationHuman amygdala development in the absence of species‐expected caregiving
Tottenham, N. (2012) · Developmental Psychobiology · doi:10.1002/dev.20531 · Cited by 149 · see citing works
Implications of newborn amygdala connectivity for fear and cognitive development at 6-months-of-age
Graham, A. M., Buss, C., Rasmussen, J. M., Rudolph, M. D., Demeter, D. V., Gilmore, J. H., Styner, M., Entringer, S., Wadhwa, P. D., & Fair, D. A. (2016) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2015.09.006 · Cited by 122 · see citing works
Asok, A., Bernard, K., Roth, T. L., Rosen, J. B., & Dozier, M. (2013) · Development and Psychopathology · doi:10.1017/s0954579413000011 · Cited by 128 · see citing works
Self-citationCallaghan, B. L., Sullivan, R. M., Howell, B., & Tottenham, N. (2014) · Developmental Psychobiology · doi:10.1002/dev.21260 · Cited by 115 · see citing works
Early life stress is associated with default system integrity and emotionality during infancy
Graham, A. M., Pfeifer, J. H., Fisher, P. A., Carpenter, S., & Fair, D. A. (2015) · Journal of Child Psychology and Psychiatry · doi:10.1111/jcpp.12409 · Cited by 84 · see citing works
Rickenbacher, E., Perry, R. E., Sullivan, R. M., & Moita, M. A. (2017) · eLife · doi:10.7554/elife.24080 · Cited by 81 · see citing works
Self-citationNorepinephrine, neurodevelopment and behavior
Saboory, E., Ghasemi, M., & Mehranfard, N. (2020) · Neurochemistry International · doi:10.1016/j.neuint.2020.104706 · Cited by 75 · see citing works
Kentner, A. C., Cryan, J. F., & Brummelte, S. (2019) · Developmental Psychobiology · doi:10.1002/dev.21775 · Cited by 64 · see citing works
Maternal regulation of infant brain state
Sarro, E. C., Wilson, D. A., & Sullivan, R. M. (2014) · Current Biology · doi:10.1016/j.cub.2014.06.017 · Cited by 61 · see citing works
Self-citation
- Authors
- Moriceau, S., Roth, T. L., & Sullivan, R. M.
- Affiliations
- University of Alabama at Birmingham (US)
- Nathan Kline Institute for Psychiatric Research (US)
- Venue
- Developmental Psychobiology
- Publisher
- Wiley
- Published
- 2010-08-20
- Volume
- 52
- Issue
- 7
- Pages
- 651-660
- ISSN
- 0012-1630 (ISSN-L)
- 1098-2302
- PMC
- PMC4334117
- OpenAlex
- W2137060882
- Cited by
- 119
- References
- 110
- Citations by year
- 2026: 2 · 2025: 1 · 2024: 7 · 2023: 5 · 2022: 5 · 2021: 6 · 2020: 9 · 2019: 5 · 2018: 5 · 2017: 8 · 2016: 10 · 2015: 7 · 2014: 12 · 2013: 12 · 2012: 12
- FWCI
- 1.05
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Developmental Psychobiology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute on Deafness and Other Communication Disorders (DC-009910, R01DC009910)
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Keywords
- infant attachment, corticosterone, stress hyporesponsive period, maternal presence, amygdala, olfactory bulb, piriform cortex, norepinephrine, locus coeruleus, fear learning, aversion learning, sensitive period, postnatal development
- MeSH terms
- Aging, Amygdala, Animals, Animals, Newborn, Association Learning, Corticosterone, Fear, Locus Coeruleus, Maternal Behavior, Motor Activity, Norepinephrine, Object Attachment, Odorants, Olfactory Bulb, Stress, Psychological, Rats
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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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