Title

Local and Network Transformations in the Auditory Midbrain

Date of Completion

January 2012

Keywords

Biology, Neuroscience

Degree

Ph.D.

Abstract

Sound information is decomposed into spectro-temporal components at the cochlea and distributed into parallel processing pathways via multiple brainstem nuclei. These diverse pathways converge in the inferior colliculus (IC), the principal midbrain auditory structure, where they are comprehensively processed before being passed onto the thalamus and auditory cortex. Yet, little is known about how the IC integrates and transforms incoming sensory inputs and produces a highly processed neural representation of sounds. We used large-scale electrode arrays to measure single and population neural response to sound in the cat IC and addressed three fundamental questions and hypothesis: ^ 1) What is the functional transformation between brainstem inputs and target IC neurons (Chapter 1)? We hypothesize that the neural representation of sounds undergoes a dramatic transformation within the IC that is characterized by changes in spectral and temporal resolution.^ 2) How do local circuits in the IC process spectral and temporal sound information (Chapter 2)? We hypothesize that the IC is organized into functional zones were neighboring neurons have common spectral and temporal sensitivity. ^ 3) How does network of IC neurons efficiently encode sound information (Chapter 3)? We predict that neural sensitivity and spiking properties across the IC population are sparsely distributed across time and frequency and such a distributed response pattern ultimately allows for high levels of encoding and metabolic efficiency. ^ To test each of these hypothesis, we used large-scale tetrode arrays to measure neural activity of local and distant neural populations in the IC. In chapter 1, we provide evidence for the presence of pre-synaptic action potentials ("prepotentials") within the IC. Two types of inputs are identified that reflect the presence of functionally distinct parallel pathways to the IC. By comparing receptive field and spike train properties between putative input neurons (PIN) and target IC neurons (ICN), we found a degraded temporal resolution and an enhanced spectral resolution in the IC. In chapter 2, we examined functional properties associated with local circuitry in the IC by recording neural activity from neighboring single neurons. We found that receptive fields and spike trains of neighboring neurons were more correlated than neurons recorded across distant sites. This suggests a scheme where local circuits are organized into zones that are specialized for processing distinct spectrotemporal cues. Finally, in chapter 3 we demonstrate that network activity in the IC is sparse and uncorrelated as long as the spike train time-scales were matched to the sensory time-scales relevant to IC neurons. Correlated activity within the IC was strictly observed for neurons with best frequencies within a critical band, the perceptual frequency resolution in mammals. This dual pattern of correlated activity within and sparse asynchronous activity outside a critical band may contribute to perceptual resolution in mammals and may ultimately lead to high levels of computational and metabolic efficiency within the ICC. ^