Understanding speech and other important sounds in noisy environments is difficult for individuals with hearing impairment. The brain has evolved mechanisms to optimize performance in these challenging situations, which involve rapid changes in sensory representation to enhance the discriminability of stimuli relevant to current behavioral demands. Most studies of the neuronal bases of how engagement in an auditory task influences neuronal activity have been performed in auditory cortex (AC), but recent work has shown that similar modulations can occur subcortically. Engaging in a simple pure tone detection task rapidly changes sensory representations in the inferior colliculus (IC). As in AC, single unit neural responses to noise stimuli (distractors) are typically suppressed, and the suppression is greater when the best frequency of the neuron matches the frequency of the target tone. These results support a contrast-matched filter model, in which changes in the population response enhance neural discriminability between reference and target. However, most prior studies of neurophysiological activity during auditory behavior, including the work in IC, have required sensory discriminations far above psychophysical thresholds. In these conditions, an animal's ability to perform the task may be more dependent on learning the appropriate sensory-motor association than the actual discrimination between target tones and noise distractors. The work proposed here will investigate near-threshold behavioral performance and task-induced changes in neuronal representation in the IC. Task difficulty will be controlled by changing the signal-to-noise ratio (SNR) of a target tone embedded in noise. For each animal, sensory threshold measurements will be used to establish high-SNR (easy) and low-SNR (difficult) task conditions. A variation in performance on behavioral trials using an identical probe target presented in both conditions will indicate of changes in animal effort. Single unit activity will be recorded in the IC during presentation of task stimuli during passive listening and during behavior in either difficulty condition. Changes in neural activity between difficultly conditions will characterize the effects of relative effort on representation in IC. Furthermore, changes in overall arousal will be monitored via pupillometry and compared to effects of effort on behavior and neural activity. Finally, the hypothesis that task-dependent changes in the IC are mediated by the large descending, corticofugal projection from AC will be explored. Optogenetic perturbation will be used to rapidly and reversibly inactivate AC during behavior. Behavioral performance as well as neuronal activity in the IC will be compared between light-on and light-off conditions. Together these experiments will describe auditory brain mechanisms involved in enhancing behaviorally relevant stimuli in contexts that more closely mimic the challenge faced by patients with hearing impairments.
Effective communication relies on the ability of the brain to extract meaningful information from the mixture and adjust to different contextual environments. These abilities can be severely impaired in individuals with dysfunctions of the auditory periphery or central auditory regions. With the goal of developing more sophisticated devices and treatments for these debilitating conditions, we seek to understand how the healthy brain extracts useful information from sounds in order to guide behavior.
