Sensation to Perception: Transformations in the representation and plasticity of sound features across sensory and limbic hierarchies

Abstract

Our perception of sounds is so much more than a mere summation of acoustic waves entering our ear. It is well established that the auditory nerve and brainstem faithfully track rapidly changing vibration patterns in the cochlea. However there is a gap in knowledge on how these sensory representations are modulated by internal state variables such as expectations and emotions to shape what we perceive. The overarching goal of my dissertation is to understand how neural circuits further along the auditory neural axis and beyond enable this transformation from sensation to perception.

We began by addressing a transformation in sound features that are encoded by neurons along the auditory midbrain-thalamus-cortex hierarchy. By simultaneously recording from hundreds of neurons along this hierarchy, we found that low-level midbrain neurons robustly encoded local temporal features, while sensitivity to slowly developing patterns emerges only at the level of neocortex.

Next, we characterized experience-dependent plasticity in a descending branch of this hierarchy. We used wide-field calcium imaging to track activity changes in layer 5 corticocollicular axons before and after a single exposure to intense noise. We found that corticocollicular axons also innervate amygdala and striatum and show disproportionate growth in response amplitude with changes in sound level after noise exposure. These findings suggest a biological mechanism that may link the sensory and affective phenotypes commonly observed in persons with noise-induced tinnitus and hyperacusis.

Finally, we investigated the neural underpinnings of how an innately neutral sound transforms to a distressing sound. We simultaneously recorded from neural ensembles in higher-order auditory cortex and basolateral amygdala (BLA) alongside endogenous acetylcholine release before, during and after the association of certain sounds with mild aversive shocks. We found enhanced neural response to the emotionally distressing sound in BLA where the neuromodulatory signal also supported the associative plasticity, and enhanced functional coupling from cortical neurons to BLA ensemble activity during the presentation of conditioned stimuli.

Overall, this dissertation describes transformations in auditory temporal coding and experience-dependent plasticity in the midbrain, thalamic and distributed limbic and sensory forebrain regions as hearing turns distressing either with learned aversive associations or after hearing loss.