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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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
Barnes, Dylan C; Wilson, Donald A (2014) Slow-wave sleep-imposed replay modulates both strength and precision of memory. J Neurosci 34:5134-42
Debiec, Jacek; Sullivan, Regina Marie (2014) Intergenerational transmission of emotional trauma through amygdala-dependent mother-to-infant transfer of specific fear. Proc Natl Acad Sci U S A 111:12222-7
Hostinar, Camelia E; Sullivan, Regina M; Gunnar, Megan R (2014) Psychobiological mechanisms underlying the social buffering of the hypothalamic-pituitary-adrenocortical axis: a review of animal models and human studies across development. Psychol Bull 140:256-82
Sarro, Emma C; Wilson, Donald A; Sullivan, Regina M (2014) Maternal regulation of infant brain state. Curr Biol 24:1664-9
Perry, Rosemarie; Sullivan, Regina M (2014) Neurobiology of attachment to an abusive caregiver: short-term benefits and long-term costs. Dev Psychobiol 56:1626-34
Borkowski, Anne H; Barnes, Dylan C; Blanchette, Derek R et al. (2011) Interaction between ? opioid receptors and benzodiazepines in CO?-induced respiratory responses in mice. Brain Res 1396:54-9
Wilson, Donald A; Sullivan, Regina M (2011) Cortical processing of odor objects. Neuron 72:506-19
Barnes, Dylan C; Chapuis, Julie; Chaudhury, Dipesh et al. (2011) Odor fear conditioning modifies piriform cortex local field potentials both during conditioning and during post-conditioning sleep. PLoS One 6:e18130
Sevelinges, Yannick; Mouly, Anne-Marie; Raineki, Charlis et al. (2011) Adult depression-like behavior, amygdala and olfactory cortex functions are restored by odor previously paired with shock during infant's sensitive period attachment learning. Dev Cogn Neurosci 1:77-87

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