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.

Chronic early life stress induced by limited bedding and nesting (LBN) material in rodents: critical considerations of methodology, outcomes and translational potential

“…The value of the maternal odor is also compromised: the deaf and blind pups depend upon their mother’s odor for interactions with the mother. While LBN pups express the survival dependent behaviors with the mother, they are significantly slower behaviorally and there is less robust connectivity between olfactory and limbic structures (Perry, Al Aïn, Raineki, Sullivan, & Wilson, 2016). Indeed, LBN pups have accelerated amygdala development, which prematurely ends the sensitive period for attachment learning (T.…”

Neurobehavioral assessment of maternal odor in developing rat pups: implications for social buffering

“…Pups had to choose between an alley containing maternal odor (air stream: 2 L/min flow rate, 1:10 maternal odor:air) versus familiar clean bedding (20 mL clean shavings in a petri dish), or were tested using familiar clean bedding versus acetophenone odor (20 mL of acetophenone diluted to 10 parts per million (PPM) with mineral oil on a KimWipe, Kimthech Science, Dallas, Texas). Acetophenone was chosen due to its relative attractiveness to rat pups (Perry, Al Aïn, McSky, Wilson, & Sullivan, 2014). The odor stimuli were placed at the end of the alleys.…”

Neurobiology of infant attachment: attachment despite adversity and parental programming of emotionality

“…Additionally, the experience-driven neurobiological mechanisms supporting attachment formation allow the infant to bond with multiple caregivers once outside of the womb. A recent publication has highlighted the extent that attachment formation is experience-driven [11]. Perry et al altered the smell of rat mothers’ natural odor via manipulation of their diet.…”

“…Furthermore, rodent research exploring ways to repair the impact of early-life caregiver adversity on later-life emotionality discovered that in adulthood the presence of maternal odor can paradoxically normalize depressive-like and fear behaviors that arise as a result of early-life adversity [41]. Since maternal odor typically loses its regulatory power by weaning [11], this indicates that maternal cues become regulatory at a delayed, developmentally-inappropriate time point following infant experience with negative caregiving. These findings provide exciting advances for research efforts attempting to re-open sensitive periods of maternal regulation of emotional development, in order to enduringly repair early-life effects of negative caregiving in adulthood.…”