title: Development of Odor Hedonics: Experience-Dependent Ontogeny of Circuits Supporting Maternal and Predator Odor Responses in Rats.
abstract: A major component of perception is hedonic valence: perceiving stimuli as pleasant or unpleasant. Here, we used early olfactory experiences that shape odor preferences and aversions to explore developmental plasticity in circuits mediating odor hedonics. We used 2-deoxyglucose autoradiographic mapping of neural activity to identify circuits differentially activated by biologically relevant preferred and avoided odors across rat development. We then further probed this system by increasing or decreasing hedonic value. Using both region of interest and functional connectivity analyses, we identified regions within primary olfactory, amygdala/hippocampal, and prefrontal cortical networks that were activated differentially by maternal and male odors. Although some activated regions remained stable across development (postnatal days 7-23), there was a developmental emergence of others that resulted in an age-dependent elaboration of hedonic-response-specific circuitry despite stable behavioral responses (approach/avoidance) to the odors across age. Hedonic responses to these biologically important odors were modified through diet suppression of the maternal odor and co-rearing with a male. This allowed assessment of hedonic circuits in isolation of the specific odor quality and/or intensity. Early experience significantly modified odor-evoked circuitry in an age-dependent manner. For example, co-rearing with a male, which induced pup attraction to male odor, reduced activity in amygdala regions normally activated by the unfamiliar avoided male odor, making this region more consistent with maternal odor. Understanding the development of odor hedonics, particularly within the context of altered early life experience, provides insight into the development of sensory processes, food preferences, and the formation of social affiliations, among other behaviors.
  
  
  
  Odor hedonic valence controls approach-avoidance behaviors, but also modulates ongoing behaviors ranging from food preferences and social affiliation with the caregiver to avoidance of predator odors. Experiences can shape hedonic valence. This study explored brain circuitry involved in odor hedonic encoding throughout development using maternal and predator odors and assessed the effects of early life experience on odor hedonic encoding by increasing/decreasing the hedonic value of these odors. Understanding the role of changing brain circuitry during development and its impact on behavioral function is critical for understanding sensory processing across development. These data converge with exciting literature on the brain's hedonic network and highlight the significant role of early life experience in shaping the neural networks of highly biologically relevant stimuli.
authors.affiliation: Emotional Brain Institute, Nathan Kline Institute for Psychiatric Research, Orangeburg, New York 10962, Department of Child and Adolescent Psychiatry, New York University Langone Medical School, New York, New York 10016, and Department of Neuroscience and Physiology, Sackler Institute, New York University School of Medicine, New York, New York 10016 rosemarie.perry@nyumc.org donald.wilson@nyumc.org.
authors.forename: Rosemarie E
authors.initials: RE
authors.lastname: Perry
authors.affiliation: Emotional Brain Institute, Nathan Kline Institute for Psychiatric Research, Orangeburg, New York 10962, Department of Child and Adolescent Psychiatry, New York University Langone Medical School, New York, New York 10016, and.
authors.forename: Syrina
authors.initials: S
authors.lastname: Al Aïn
authors.affiliation: Emotional Brain Institute, Nathan Kline Institute for Psychiatric Research, Orangeburg, New York 10962, Department of Child and Adolescent Psychiatry, New York University Langone Medical School, New York, New York 10016, and.
authors.forename: Charlis
authors.identifier: 0000-0003-1655-5935
authors.initials: C
authors.lastname: Raineki
authors.affiliation: Emotional Brain Institute, Nathan Kline Institute for Psychiatric Research, Orangeburg, New York 10962, Department of Child and Adolescent Psychiatry, New York University Langone Medical School, New York, New York 10016, and.
authors.forename: Regina M
authors.initials: RM
authors.lastname: Sullivan
authors.affiliation: Emotional Brain Institute, Nathan Kline Institute for Psychiatric Research, Orangeburg, New York 10962, Department of Child and Adolescent Psychiatry, New York University Langone Medical School, New York, New York 10016, and rosemarie.perry@nyumc.org donald.wilson@nyumc.org.
authors.forename: Donald A
authors.initials: DA
authors.lastname: Wilson
mesh_terms: D059445:Anhedonia / Q000502:physiology*; D000818:Animals; D000831:Animals, Newborn; D001345:Autoradiography; D001362:Avoidance Learning / Q000502:physiology; D001921:Brain / Q000000981:diagnostic imaging / Q000502:physiology*; D003847:Deoxyglucose / Q000378:metabolism; D004644:Emotions / Q000502:physiology; D005260:Female; D008297:Male; D009812:Odorants; D009833:Olfactory Pathways / Q000000981:diagnostic imaging / Q000502:physiology*; D055696:Olfactory Perception / Q000502:physiology*; D051381:Rats; D020318:Rats, Long-Evans; D012903:Smell
chemical_list: D003847:Deoxyglucose
keywords: development; hedonics; maternal odor; olfaction; predator odor; smell