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Neural Mechanisms of Spatial Stream Segregation Along the Ascending Auditory Pathway

Abstract

In a complex auditory scene, listeners are capable of disentangling multiple competing sequences of sounds that originate from distinct sources. This process is referred to as “stream segregation”, where each “stream" represents the perception of a sound sequence from a particular source. Spatial separation of sound sources facilitates the recognition of multiple sequences of sounds (i.e., multiple “streams”) as belonging to distinct sources. Several neurophysiological studies in laboratory animals have shown that perceptual streams are represented by distinct mutually-synchronized neural populations in the auditory cortex. However, the mechanisms leading to those cortical responses are unknown. This dissertation explores the neural substrates and mechanisms of spatial stream segregation (“SSS”) at several stages in the ascending auditory pathway.

We recorded in vivo extracellular spike activity from neurons along different stations of the ascending auditory system of the anesthetized rat, from the midbrain, thalamus, and cortex. Several novel observations were made: (1) The rat primary auditory cortex (area A1) was exclusively tuned to the contralateral hemifield and and was level-tolerant across a 30-dB range of sound levels. (2) Level-tolerant contralateral hemifield spatial sensitivity arises independently along the tectal and lemniscal pathways, highlighting two parallel brainstem pathways for spatial hearing. (3) A linear discriminator analysis of cortical spike counts exhibited high spatial acuity for near-midline sounds and poor discrimination for off-midline locations, which is consistent with previous findings describing the rat’s sound localization behavior. (4) Under stimulus conditions at which human listeners report SSS, neural SSS is weak in the central nucleus of the IC (ICC), it appears in the nucleus of the brachium of the IC (BIN) and in about two thirds of neurons in the ventral MGB (MGBv), and is prominent in A1. Cortical SSS reflects the spatial sensitivity of neurons enhanced by forward suppression. (5) GABA receptor blockers showed no change on cortical forward suppression, suggesting that it does not result from GABAergic inhibition but might reflect synaptic depression at the thalamocortical synapse. Overall, these findings provide substantial evidence that auditory streams are increasingly segregated along the ascending auditory pathways that culminate in distinct mutually-synchronized neural populations in the auditory cortex.

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