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.

National Institute of Health (NIH)
National Institute on Deafness and Other Communication Disorders (NIDCD)
Research Project (R01)
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Somatosensory and Chemosensory Systems Study Section (SCS)
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Sullivan, Susan L
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New York University
Schools of Medicine
New York
United States
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Al Aïn, Syrina; Perry, Rosemarie E; Nuñez, Bestina et al. (2017) Neurobehavioral assessment of maternal odor in developing rat pups: implications for social buffering. Soc Neurosci 12:32-49
Santiago, Adrienne; Aoki, Chiye; Sullivan, Regina M (2017) From attachment to independence: Stress hormone control of ecologically relevant emergence of infants' responses to threat. Curr Opin Behav Sci 14:78-85
Opendak, Maya; Gould, Elizabeth; Sullivan, Regina (2017) Early life adversity during the infant sensitive period for attachment: Programming of behavioral neurobiology of threat processing and social behavior. Dev Cogn Neurosci 25:145-159
Tallot, L; Doyère, V; Sullivan, R M (2016) Developmental emergence of fear/threat learning: neurobiology, associations and timing. Genes Brain Behav 15:144-54
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
Rincón-Cortés, M; Sullivan, R M (2016) Emergence of social behavior deficit, blunted corticolimbic activity and adult depression-like behavior in a rodent model of maternal maltreatment. Transl Psychiatry 6:e930
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
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
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

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