Social odor modulation of auditory cortex via the basal amygdala

PROJECT SUMMARY Olfaction is unique among the senses for its direct and intimate connections to the limbic system. This may explain the widespread subjective experience that odors can trigger powerful affective responses, especially odors from social partners. This is a fundamental mode of social communication in many species, including humans, yet the neural circuits that link odor-evoked emotional states to changes in perception and social interaction remain unclear. Our goal is to determine how odor cues from offspring influence neural and behavioral responses to infant vocalizations in mice. We will use a robust and essential maternal behavior (pup retrieval) that requires both olfaction and audition to ask: If and under what conditions does retrieval engage direct cross talk between the two modalities? and, What is the functional significance of this cross talk? One important aspect of maternal care in mice is the need to retrieve their pups when they are away from the nest and emitting ultrasonic distress vocalizations (USVs). First time mothers and nulliparous females (‘surrogates’) housed with a dam and her litter rapidly learn to recognize these calls and return the young to the nest. There are contemporaneous changes in neural responses to USVs in the auditory cortex. Direct interaction with pups is highly rewarding, suggesting that sensory experience with offspring may be a crucial trigger for neural and behavioral plasticity. Accordingly, both the smell of pups and the sound of their vocalizations are required for performance of pup retrieval. Indeed, previous work showed that pup odor modulates neuronal responses to USVs in the auditory cortex of maternally-experienced females. Our preliminary data suggest that pup odor may influence responses to USVs via a pathway to the auditory cortex (AC) from the basal amygdala (BA), a part of the brain that has been linked to maternal behavior, and to motivated behavior broadly. The fact that the projection to the AC arises from the BA, a structure critical for motivated behavior, raises the possibility that the odor signal conveyed to the AC encodes affective state information such as salience or reward. We hypothesize that the BA is a conduit for pup odors to trigger affective states that dynamically modulate the neural representation and salience of USVs. Here, we propose to test this hypothesis by combining a novel structured retrieval task, spatiotemporally controlled exposure to pup odor, and neuronal recordings in freely behaving mice. We will identify the temporal structure and behavioral determinants of BAACn activity during retrieval (Aim 1). We will determine the relationship between BAACn firing and auditory activity (Aim 2). Finally, we will test the necessity of BAACn activity during distinct behavioral components of pup retrieval (Aim 3).