Unique neural circuitry for neonatal olfactory learning
Open accessAbstract
Imprinting ensures that the infant forms the caregiver attachment necessary for altricial species survival. In our mammalian model of imprinting, neonatal rats rapidly learn the odor-based maternal attachment. This rapid learning requires reward-evoked locus ceruleus (LC) release of copious amounts of norepinephrine (NE) into the olfactory bulb. This imprinting ends at postnatal day 10 (P10) and is associated with a dramatic reduction in reward-evoked LC NE release. Here we assess whether the functional emergence of LC alpha2 inhibitory autoreceptors and the downregulation of LC alpha1 excitatory autoreceptors underlie the dramatic reduction in NE release associated with termination of the sensitive period. Postsensitive period pups (P12) were implanted with either LC or olfactory bulb cannulas, classically conditioned with intracranial drug infusions (P14), and tested for an odor preference (P15). During conditioning, a novel odor was paired with either olfactory bulb infusion of abeta-receptor agonist (isoproterenol) to assess the target effects of NE or direct LC cholinergic stimulation combined with alpha2 antagonists and alpha1 agonists in a mixture to reinstate neonatal levels of LC autoreceptor activity to assess the source of NE. Pups learned an odor preference when the odor was paired with either olfactory bulb isoproterenol infusion or reinstatement of neonatal LC receptor activity. These results suggest that LC autoreceptor functional changes rather than olfactory bulb changes underlie sensitive period termination.
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Odors associated with early-life experiences acquire a rewarding value that promotes behaviors essential for survival.
“odors associated with early-life experiences acquire a rewarding value that promotes behaviors essential for survival [65].”
From Positive early-life olfactory memory is rooted in the olfactory bulb and triggers large-scale changes beyond the olfactory system (2026) · cites this paper as [65]
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Fear conditioning and extinction across development: Evidence from human studies and animal models
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Rodent model of infant attachment learning and stress
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Transitions in sensitive period attachment learning in infancy: The role of corticosterone
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Self-citationCentrifugal Drive onto Local Inhibitory Interneurons of the Olfactory Bulb
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Long-Lasting Neural Circuit Dysfunction Following Developmental Ethanol Exposure
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Neonatal handling alters the structure of maternal behavior and affects mother–pup bonding
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Tuning to the Positive: Age-Related Differences in Subjective Perception of Facial Emotion
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Olfactory classical conditioning in neonatal mouse pups using thermal stimuli
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The lateral habenula integrates age and experience to promote social transitions in developing rats
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Developmental Neurobiology of the Rat Attachment System and Its Modulation by Stress
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Neurobehavioral Development of Infant Learning and Memory: Implications for Infant Attachment
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Self-citation
- Authors
- Moriceau, S., & Sullivan, R. M.
- Affiliations
- University of Oklahoma (US)
- ORCID
- Sullivan, Regina M.
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2004-02-04
- Volume
- 24
- Issue
- 5
- Pages
- 1182-1189
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC1868533
- OpenAlex
- W1963661711
- Cited by
- 141
- References
- 106
- Citations by year
- 2026: 4 · 2025: 2 · 2024: 3 · 2023: 3 · 2021: 4 · 2020: 2 · 2019: 7 · 2018: 6 · 2017: 5 · 2016: 10 · 2015: 6 · 2014: 9 · 2013: 6 · 2012: 9
- FWCI
- 4.00
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- Funders
- National Science Foundation (0117234)
- University of Oklahoma
- Oklahoma Center for the Advancement of Science and Technology
- National Institute of Child Health and Human Development
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (HD33402, R01HD033402)
- Topics
- Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Keywords
- locus coeruleus, noradrenaline release, olfactory bulb, neonatal rats, classical conditioning, isoproterenol, cholinergic stimulation
- MeSH terms
- Acetylcholine, Adrenergic alpha-Agonists, Animals, Animals, Newborn, Choice Behavior, Critical Period, Psychological, Drug Administration Routes, Female, Imprinting, Psychological, Infusion Pumps, Learning, Locus Coeruleus, Male, Nerve Net, Norepinephrine, Olfactory Bulb, Olfactory Pathways, Phenylephrine, Smell, Cholinergic Agents, Maze Learning, Rats, Long-Evans, Rats
About these checks
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.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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