Sensory systems must detect and discriminate stimuli, but also play a role in attaching meaning to the stimulus to evoke an appropriate approach/avoidance response. This may be particularly true in the olfactory system which is heavily and reciprocally connected to limbic structures such as amygdala, orbitofrontal cortex and hippocampus. Convergence of olfactory pathway and limbic circuits could help tag odor hedonics to the representation of the odor itself. Odor hedonics (pleasantness and unpleasantness) are a major factor in such varied functions as food preferences and social affiliations, thus understanding how hedonic valence is incorporated into odor representation could have wide ranging implications for health and well-being. The present proposal uses a novel model system to determine critical circuits involved in attaching hedonic valence to odor. Given the important role, early experience plays in shaping lifelong odor preferences, and the relatively early functional development of the olfactory system, the proposed work also addresses whether these circuits change developmentally or are stable throughout life to support consistent behavioral outcomes.
Aim 1 will compare the ontogeny of neural circuits (collections of functionally interconnected brain regions) activated by appetitive and aversive odors. Are circuit-level representations of aversive and appetitive odors stable across ontogeny? We hypothesize that a core functional neural circuit will be present in neonates for encoding odor hedonics, and that although with age additional components will be added, this core circuit will be maintained through life.
Aim 2 will compare functional circuits activated during response to odors with either learned or innate hedonic meaning at different ages. Are similar circuits activated by learned aversive odors as are activated by innately aversive odors? We hypothesize that learned odors will activate an overlapping, though not identical functional circuit as that active during response to odor with the same, though innate hedonic valence. Finally, Aim 3 will test hypotheses about the role of specific olfactory and limbic components in the assignment of odor hedonic valence during development through the use of reversible lesions. Can circuit components be identified that are critical for odor hedonic valence assignment across development?

Public Health Relevance

Sensory processing allows detection and discrimination of environmental stimuli and serves a basic and critical role in all goal-directed behavior. However in addition, sensory processing allows attachment of hedonic valence to stimuli. Abnormal levels of aversive associations may contribute to phobias or post-traumatic responses, while abnormal levels of appetitive associations may contribute to addictions. Furthermore, hedonic associations acquired early in development can have lifelong consequences, influencing behavioral outcomes in diverse and potentially unexpected contexts. The proposed work will have significance for our understanding of how sensory representations come to include a hedonic component, the central functional circuits involved in this representation, and whether these circuits change over development, or remain largely stable despite emergence of new circuit components.

Agency
National Institute of Health (NIH)
Institute
National Institute on Deafness and Other Communication Disorders (NIDCD)
Type
Research Project (R01)
Project #
5R01DC009910-05
Application #
8510409
Study Section
Somatosensory and Chemosensory Systems Study Section (SCS)
Program Officer
Sullivan, Susan L
Project Start
2009-08-01
Project End
2014-07-31
Budget Start
2013-08-01
Budget End
2014-07-31
Support Year
5
Fiscal Year
2013
Total Cost
$316,829
Indirect Cost
$70,015
Name
New York University
Department
Psychiatry
Type
Schools of Medicine
DUNS #
121911077
City
New York
State
NY
Country
United States
Zip Code
10016
Debiec, Jacek; Sullivan, Regina M (2016) The neurobiology of safety and threat learning in infancy. Neurobiol Learn Mem :
Tallot, L; Doyère, V; Sullivan, R M (2016) Developmental emergence of fear/threat learning: neurobiology, associations and timing. Genes Brain Behav 15:144-54
Perry, Rosemarie E; Al Aïn, Syrina; Raineki, Charlis et al. (2016) Development of Odor Hedonics: Experience-Dependent Ontogeny of Circuits Supporting Maternal and Predator Odor Responses in Rats. J Neurosci 36:6634-50
Boulanger Bertolus, Julie; Mouly, Anne-Marie; Sullivan, Regina M (2016) Ecologically relevant neurobehavioral assessment of the development of threat learning. Learn Mem 23:556-66
Gunnar, Megan R; Hostinar, Camelia E; Sanchez, Mar M et al. (2015) Parental buffering of fear and stress neurobiology: Reviewing parallels across rodent, monkey, and human models. Soc Neurosci 10:474-8
Sadrian, Benjamin; Wilson, Donald A (2015) Optogenetic Stimulation of Lateral Amygdala Input to Posterior Piriform Cortex Modulates Single-Unit and Ensemble Odor Processing. Front Neural Circuits 9:81
Raineki, Charlis; Sarro, Emma; Rincón-Cortés, Millie et al. (2015) Paradoxical neurobehavioral rescue by memories of early-life abuse: the safety signal value of odors learned during abusive attachment. Neuropsychopharmacology 40:906-14
Sullivan, Regina M; Perry, Rosemarie E (2015) Mechanisms and functional implications of social buffering in infants: Lessons from animal models. Soc Neurosci 10:500-11
Rincón-Cortés, Millie; Barr, Gordon A; Mouly, Anne Marie et al. (2015) Enduring good memories of infant trauma: rescue of adult neurobehavioral deficits via amygdala serotonin and corticosterone interaction. Proc Natl Acad Sci U S A 112:881-6
Cohen, Yaniv; Putrino, David; Wilson, Donald A (2015) Dynamic cortical lateralization during olfactory discrimination learning. J Physiol 593:1701-14

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