Social learning enhances auditory cortex sensitivity and task acquisition

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PROJECT SUMMARY Skill acquisition can be facilitated by social experience, usually through exposure to a conspecific performing a well-defined behavior. In fact, social learning (SL) is pivotal to the acquisition of many core behaviors, including aural communication. Although the neural bases for auditory SL remain uncertain, one plausible hypothesis is that social experience may induce experience-dependent plasticity in auditory cortex (AC), as found for many forms of learning, thereby facilitating auditory task acquisition. Social learning may also have implications for developmental hearing loss (HL), a prevalent sensory impairment that is associated with persistent deficits in speech and language acquisition, especially since social factors are thought to facilitate language acquisition in children with HL. Three Aims test predictions that emerge from this hypothesis: Aim 1 first demonstrates the positive impact of SL on task learning: Naïve Observer gerbils receive five days of exposure to a trained Demonstrator performing an amplitude modulation rate discrimination task. An opaque divider separates Observer and Demonstrator, such that visual cues are absent. Observer gerbils are then permitted to practice the auditory task, and the rate of learning assessed. To test the prediction that AC activity is required, AC will be inactivated during social experience. Aim 1 will go on to test the prediction that dopaminergic neuromodulation within AC is be necessary for social learning. We will first determine whether dopamine is released in AC during social experience, using fiber photometry and a genetically expressed dopamine sensor. We will then block dopamine receptors in AC during social exposure to determine whether the benefits of social experience are diminished. Aim 2 tests the prediction that AC neuron sensitivity to auditory cues will be enhanced during SL. Gerbils will be instrumented with electrode arrays in AC, and recorded during five days of social exposure. Single neuron and population responses to auditory task stimuli will be assessed to determine if improved neural sensitivity during observation can explain the rate of task acquisition rate during practice. To test the contribution of an auditory social cue (i.e., Demonstrator vocalizations), recordings will be obtained from Observers exposed to auditory task cues plus playback of demonstrator vocalizations. Aim 3 tests the prediction that SL will improve task acquisition in hearing loss-reared animals. Juvenile gerbils will receive either permanent (malleus removal) or transient (earplugs) conductive HL. Animals will then be instrumented with electrode arrays in AC, and assessed as in Aim 2. Innovations in this proposal are to: (i) extend current auditory learning paradigms to include social cues, (ii) use wireless recordings during learning to make within- animal comparisons of neural and behavioral sensitivity, and (iii) shift the current emphasis in HL research from a focus on degraded sensory processing to one that considers how social factors may facilitate auditory skills. If successful, the project will identify a CNS mechanism that mediates socially-enhanced auditory learning, and provide a novel approach to remediate sensory and cognitive barriers in children with HL.