The role of olfactory bulb norepinephrine in early olfactory learning

Sullivan, R.M.; Zyzak, D.R.; Skierkowski, P.; Wilson, D.A.

doi:10.1016/0165-3806(92)90207-d

Cited by 119Olfactory and Sensory Function StudiesMemory and Neural MechanismsNeurogenesis and neuroplasticity mechanisms

The role of olfactory bulb norepinephrine in early olfactory learning

Sullivan, R.M., Zyzak, D.R., Skierkowski, P., Wilson, D.A.·1992·Developmental Brain Research

DOI 10.1016/0165-3806(92)90207-d

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Abstract

Wistar rat pups were implanted with bilateral olfactory bulb cannulas on postnatal day 5 (PN5). On PN6, pups were trained in an olfactory classical conditioning task with peppermint odor as the CS and tactile stimulation/stroking as the UCS. Pups were randomly assigned to either PAIRED, BACKWARD or ODOR-only conditions. Half the pups in each group received intrabulbar infusions of 100 microM propranolol and half received intrabulbar infusions of saline during the training session. Propranolol infusions blocked acquisition of the learned odor preference expressed by PAIRED saline-infused pups. Diffusion of the infusate was checked in additional pups by infusing [3H]NE and performing LSC analysis. Infusate concentration did not significantly differ between the anterior and posterior halves of the bulb, but were sharply lower in the olfactory peduncle and more posterior areas. The results suggest that olfactory bulb NE is critical for early olfactory learning.

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During the first ten days of life, learning-associated plasticity for new maternal odors in rat pups occurs within the olfactory bulb and requires an odor paired with copious amounts of NE.
“During the first ten days of life, the learning process for new maternal odors in rat pups occurs through a relatively simple neurobiological substrate. At this early age, learning-associated plasticity occurs within the olfactory bulb, the first relay station for olfactory processing. This process requires that an odor is paired with copious amounts of NE (Sullivan et al., 2000b, Sullivan et al.,”
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 Sullivan et al., 1992

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Opioid modulation of Fos protein expression and olfactory circuitry plays a pivotal role in what neonates remember.Preprint
Roth, T., Moriceau, S., & Sullivan, R. (2006) · Learning & memory (Cold Spring Harbor, N.Y.) · doi:10.1101/lm.301206 · Cited by 22 · see citing works
Rearing with artificially scented mothers attenuates conditioned odor aversion in adulthood but not its amygdala dependency
Sevelinges, Y., Lévy, F., Mouly, A., & Ferreira, G. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.11.003 · Cited by 19 · see citing works
Norepinephrine and associative conditioning in the neonatal rat somatosensory system
Landers, M. S., & Sullivan, R. M. (1999) · Developmental Brain Research · doi:10.1016/s0165-3806(99)00026-7 · Cited by 19 · see citing works
Early locus coeruleus lesions increase the density of β‐adrenergic receptors in the main olfactory bulb of rats
Woo, C. C., Wilson, D. A., Sullivan, R. M., & Leon, M. (1996) · International Journal of Developmental Neuroscience · doi:10.1016/s0736-5748(96)00041-x · Cited by 19 · see citing works
Early olfactory enrichment and deprivation both decrease β‐adrenergic receptor density in the main olfactory bulb of the rat
Woo, C. C., & Leon, M. (1995) · The Journal of Comparative Neurology · doi:10.1002/cne.903600408 · Cited by 19 · see citing works
α7-Nicotinic Acetylcholine Receptor: Role in Early Odor Learning Preference in Mice
Hellier, J. L., Arevalo, N. L., Smith, L. P., Xiong, K.-N., & Restrepo, D. (2012) · PLoS ONE · doi:10.1371/journal.pone.0035251 · Cited by 18 · see citing works
Biased Random-Walk Learning: A Neurobiological Correlate to Trial-and-Error
Anderson, R. W. (1998) · Elsevier eBooks · doi:10.1016/b978-012526420-4/50008-2 · Cited by 18 · see citing works
Olfactory bulb glycogen metabolism: noradrenergic modulation in the young rat
Coopersmith, R., & Leon, M. (1995) · Brain Research · doi:10.1016/0006-8993(94)01445-n · Cited by 17 · see citing works
Amygdala circuit transitions supporting developmentally-appropriate social behavior
Ferrara, N. C., & Opendak, M. M. (2023) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2023.107762 · Cited by 17 · see citing works
Effects of Amphetamine and Phenylethylamine on Catecholamine Release in the Glomerular Layer of the Rat Olfactory Bulb
Mesfioui, A., Math, F., Jmari, K., Hessni, A. E., Choulli, M. K., & Davrainville, J. L. (1998) · Neurosignals · doi:10.1159/000014548 · Cited by 16 · see citing works
Central Olfactory Structures
Linster, C., & Cleland, T. A. (2003) · CRC Press eBooks · doi:10.1201/9780203911457.ch8 · Cited by 15 · see citing works
α2-Adrenergic receptor activation promotes long-term potentiation at excitatory synapses in the mouse accessory olfactory bulbPreprint
Huang, G.-Z., Taniguchi, M., Zhou, Y., Zhang, J.-J., Okutani, F., Murata, Y., Yamaguchi, M., & Kaba, H. (2018) · Learning & Memory · doi:10.1101/lm.046391.117 · Cited by 14 · see citing works
Effects of a Neonatal Experience Involving Reward Through Maternal Contact on the Noradrenergic System of the Rat Prefrontal Cortex
Kalpachidou, T., Raftogianni, A., Melissa, P., Kollia, A.-M., Stylianopoulou, F., & Stamatakis, A. (2015) · Cerebral Cortex · doi:10.1093/cercor/bhv192 · Cited by 13 · see citing works
From attachment to independence: stress hormone control of ecologically relevant emergence of infants’ responses to threat
Santiago, A. N., Aoki, C. J., & Sullivan, R. M. (2017) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2016.12.010 · Cited by 13 · see citing works
Attachment Figure's Regulation of Infant Brain and Behavior
Sullivan, R. M. (2017) · Psychodynamic Psychiatry · doi:10.1521/pdps.2017.45.4.475 · Cited by 13 · see citing works
Physiology of the Main Olfactory Bulb
Ennis, M. J., & Hayar, A. M. (2008) · Elsevier eBooks · doi:10.1016/b978-012370880-9.00118-3 · Cited by 11 · see citing works
Developmental Neurobiology of the Rat Attachment System and Its Modulation by Stress
Bisaz, R., & Sullivan, R. M. (2012) · Behavioral Sciences · doi:10.3390/bs2020079 · Cited by 11 · see citing works
Lateral olfactory tract input to dentate gyrus is depressed by prior noradrenergic activation using nucleus paragigantocellularis stimulation
Babstock, D. M., & Harley, C. W. (1993) · Brain Research · doi:10.1016/0006-8993(93)90494-8 · Cited by 11 · see citing works
Castration reduces olfactory bulb norepinephrine transporter function as indicated by responses to noradrenergic uptake blockers
Shang, Y., & Dluzen, D. E. (1998) · Brain Research · doi:10.1016/s0006-8993(97)01101-3 · Cited by 10 · see citing works
Ecologically relevant neurobehavioral assessment of the development of threat learningPreprint
Boulanger-Bertolus, J., Mouly, A., & Sullivan, R. M. (2016) · Learning & Memory · doi:10.1101/lm.042218.116 · Cited by 9 · see citing works
Understanding the development of a functional brain circuit: reward processing as an illustration
Opendak, M. M., Meyer, H. C., Callaghan, B. L., Abramson, L., John, S. R., Bath, K. G., Lee, F. S., Tottenham, N., & Sullivan, R. M. (2025) · Translational Psychiatry · doi:10.1038/s41398-025-03280-z · Cited by 9 · see citing works
Cytochrome oxidase activity in the olfactory system of staggerer mutant mice
Deiss, V., Dubois, M., Lalonde, R., & Strazielle, C. (2001) · Brain Research · doi:10.1016/s0006-8993(01)02678-6 · Cited by 9 · see citing works
Long‐term effects of infant learning on adult conditioned odor aversion are determined by the last preweaning experience
Sevelinges, Y., Mouly, A., Lévy, F., & Ferreira, G. (2009) · Developmental Psychobiology · doi:10.1002/dev.20378 · Cited by 9 · see citing works
Maturation of pyramidal cells in anterior piriform cortex may be sufficient to explain the end of early olfactory learning in ratsPreprint
Oruro, E. M., Pardo, G. V. E., Lucion, A. B., Calcagnotto, M. E., & Idiart, M. (2019) · Learning & Memory · doi:10.1101/lm.050724.119 · Cited by 9 · see citing works

Behavioral and neural effects of stimulation during olfactory experience in preweanling rats
Sullivan, R. M., & Leon, M. (1986) · Infant Behavior and Development · doi:10.1016/s0163-6383(86)80375-7
Norepinephrine and learning-induced plasticity in infant rat olfactory system
Sullivan, R., Wilson, D., & Leon, M. (1989) · The Journal of Neuroscience · doi:10.1523/jneurosci.09-11-03998.1989 · Cited by 261 · see citing works
Norepinephrine and Learning-Induced Plasticity in Infant Rat
System, O., Sullivan, R. M., Wilson, A. D. A., & Leon, M. (2013)
Norepinephrine-induced plasticity and one-trial olfactory learning in neonatal rats
Sullivan, R. M., McGaugh, J. L., & Leon, M. (1991) · Developmental Brain Research · doi:10.1016/0165-3806(91)90050-s · Cited by 112 · see citing works
Chemical dependencies of learning in the rabbit olfactory bulb: Acquisition of the transient spatial pattern change depends on norepinephrine.
Gray, C. M., Freeman, W. J., & Skinner, J. E. (1986) · Behavioral Neuroscience · doi:10.1037//0735-7044.100.4.585 · Cited by 162 · see citing works

Authors: Sullivan, R. M., Zyzak, D. R., Skierkowski, P., & Wilson, D. A.
Affiliations: University of Oklahoma (US)
Corresponding author: Sullivan, R.M.
ORCID: Sullivan, R.M.
Wilson, D.A.
Venue: Developmental Brain Research
Publisher: Elsevier BV
Published: 1992-11
Volume: 70
Issue: 2
Pages: 279-282
ISSN: 0165-3806 (ISSN-L)
DOI: 10.1016/0165-3806(92)90207-d
OpenAlex: W1987713348
Cited by: 119
References: 18
Citations by year: 2026: 1 · 2025: 2 · 2023: 3 · 2022: 1 · 2020: 3 · 2019: 4 · 2018: 4 · 2017: 6 · 2016: 5 · 2015: 4 · 2014: 3 · 2013: 1 · 2012: 4
FWCI: 3.31
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Developmental Brain Research (publishedVersion)
PubMed (publishedVersion)
Funders: National Institute on Deafness and Other Communication Disorders (DC00489)
Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01HD033402)
Topics: Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
Keywords: norepinephrine, olfactory bulb, olfactory learning, propranolol, odor preference, postnatal development, olfactory peduncle, tactile stimulation
MeSH terms: Animals, Animals, Newborn, Conditioning, Classical, Learning, Norepinephrine, Odorants, Olfactory Bulb, Propranolol, Smell, Touch, Rats, Wistar, Rats

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The role of olfactory bulb norepinephrine in early olfactory learning

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