An amygdalo-cortical circuit for multisensory processing in maternal behavior

Nowlan, Alexandra C (April 2021) An amygdalo-cortical circuit for multisensory processing in maternal behavior. PhD thesis, Cold Spring Harbor Laboratory.

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Abstract

Social encounters are commonly constructed from stimuli of more than one modality. The ability to integrate separate streams of information from conspecifics likely improves the fidelity of social communication, yet the neural circuitry that supports this operation is poorly understood. Much of the research investigating the neural correlates of multisensory integration has focused on the binding of visual and auditory stimuli and has largely ignored the contribution of olfactory input. Mice, however, rely heavily on odors to communicate social information, which can significantly modify neural activity across sensory modalities and alter the behavioral output of the animal. Because social behaviors like reproduction and parental care are essential for survival, the underlying circuits are evolutionarily conserved, allowing animal models to provide detailed insight on neural circuits with real implications for human health. Studies of maternal behavior in mice have revealed incredible detail about hypothalamic and neuroendocrine systems that underlie a repertoire of stereotyped behaviors in natural mothers. However, the neural networks that support maternal behavior are not solely dependent on hormonal input. Instead, prolonged exposure to novel multisensory cues provided by pups is suspected to be the essential component enhancing the salience of specific stimuli. For example, in maternally experienced females, odor presentation enhances auditory responses to ethologically relevant stimuli. In this scenario, olfactory signaling conveys the context in which to detect and respond to certain auditory stimuli. Though compelling, this theory did not possess an anatomical substrate to support this function. Here we identify a pathway from neurons in the basal amygdala to the auditory cortex (BA-AC) by which female mice may merge olfactory and auditory signals from pups to guide maternal behavior. BA-AC neurons both detect pup odor and show elevated activity while searching for pups in distress. Optogenetic activation of BA-AC neurons modifies auditory cortical activity in an experience-dependent manner, switching from suppression to enhancement of auditory responses in maternally experienced females. BA-AC neurons, therefore, constitute a conduit for pup odor to act directly on the primary sensory cortex to alter vocal perception. We propose that the BA may influence goal-directed maternal behavior beyond merging multisensory stimuli by incorporating the animal’s affective state to enhance the salience of pup vocalizations, resulting in adept pup retrieval.

Item Type: Thesis (PhD)
Subjects: organs, tissues, organelles, cell types and functions > tissues types and functions > amygdala
organs, tissues, organelles, cell types and functions > cell types and functions > cell functions > auditory plasticity
organism description > animal behavior > maternal
neurobiology > neuroscience > multisensory integration
organism description > animal behavior > olfactory
organism description > animal behavior > social
CSHL Authors:
Communities: CSHL labs > Shea lab
School of Biological Sciences > Theses
Depositing User: Sasha Luks-Morgan
Date: 7 April 2021
Date Deposited: 31 Aug 2021 20:39
Last Modified: 31 Aug 2021 20:39
URI: https://repository.cshl.edu/id/eprint/40335

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