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Cited by 85Memory and Neural MechanismsNeuroendocrine regulation and behaviorStress Responses and Cortisol

Maternal attenuation of hypothalamic paraventricular nucleus norepinephrine switches avoidance learning to preference learning in preweanling rat pups

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Shionoya, Kiseko, Moriceau, Stephanie, Bradstock, Peter, Sullivan, Regina M.·2007·Hormones and Behavior
DOI 10.1016/j.yhbeh.2007.06.004PMC PMC2659450
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Abstract

Infant rats learn to prefer stimuli paired with pain, presumably due to the importance of learning to prefer the caregiver to receive protection and food. With maturity, a more 'adult-like' learning system emerges that includes the amygdala and avoidance/fear learning. The attachment and 'adult-like' systems appear to co-exist in older pups with maternal presence engaging the attachment system by lowering corticosterone (CORT). Specifically, odor-shock conditioning (11 odor-0.5 mA shock trials) in 12-day-old pups results in an odor aversion, although an odor preference is learned if the mother is present during conditioning. Here, we propose a mechanism to explain pups ability to 'switch' between the dual learning systems by exploring the effect of maternal presence on hypothalamic paraventricular nucleus (PVN) neural activity, norepinephrine (NE) levels and learning. Maternal presence attenuates both PVN neural activity and PVN NE levels during odor-shock conditioning. Intra-PVN NE receptor antagonist infusion blocked the odor aversion learning with maternal absence, while intra-PVN NE receptor agonist infusion permitted odor aversion learning with maternal presence. These data suggest maternal control over pup learning acts through attenuation of PVN NE to reduce the CORT required for pup odor aversion learning. Moreover, these data also represent pups' continued maternal dependence for nursing, while enabling aversion learning outside the nest to prepare for pups future independent living.

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  • In infant rodents, social buffering by the mother attenuates stress hormone release by the HPA axis at the PVN through suppression of NE afferents from medullary A1/A2 noradrenergic neurons.

    “It has been shown that in infant rodents, social buffering by the mother greatly attenuates stress hormone release by the HPA axis at the level of the hypothalamic paraventricular nucleus (PVN), through suppression of NE afferents from medullary A1/A2 noradrenergic neurons (Shionoya et al., 2007)–a system identified in adults (Ziegler and Herman, 2002).”

    From Early life adversity during the infant sensitive period for attachment: Programming of behavioral neurobiology of threat processing and social behavior (2017) · cites this paper as Shionoya et al., 2007

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Authors
Shionoya, K., Moriceau, S., Bradstock, P., & Sullivan, R. M.
Affiliations
University of Oklahoma (US)
Corresponding author
Sullivan, Regina M.
ORCID
Venue
Hormones and Behavior
Publisher
Elsevier BV
Published
2007-09
Volume
52
Issue
3
Pages
391-400
ISSN
0018-506X (ISSN-L)
DOI
10.1016/j.yhbeh.2007.06.004
PMC
PMC2659450
OpenAlex
W2086411151
Cited by
85
References
112
Citations by year
2026: 4 · 2025: 6 · 2024: 2 · 2023: 3 · 2022: 5 · 2021: 1 · 2020: 5 · 2019: 5 · 2018: 8 · 2017: 11 · 2016: 7 · 2015: 7 · 2014: 5 · 2013: 3 · 2012: 3
FWCI
1.50
Type
journal article
Language
en
Open access
Licence
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations
  • Hormones and Behavior (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • Oklahoma Center for the Advancement of Science and Technology
  • RIKEN
  • Eunice Kennedy Shriver National Institute of Child Health and Human Development (HD33402, R01HD033402)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
  • Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Keywords
maternal presence, hypothalamic paraventricular nucleus, norepinephrine, corticosterone, maternal deprivation, attachment, fear learning, avoidance learning, preweanling rats
MeSH terms
Analysis of Variance, Animals, Animals, Newborn, Arousal, Association Learning, Avoidance Learning, Corticosterone, Critical Period, Psychological, Female, Male, Maternal Behavior, Norepinephrine, Paraventricular Hypothalamic Nucleus, Receptors, Adrenergic, Smell, Social Environment, Stress, Psychological, Time Factors, Statistics, Nonparametric, Rats, Long-Evans, Rats

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