Emergence of Spatial Stream Segregation in the Ascending Auditory Pathway

Abstract

Stream segregation enables a listener to disentangle multiple competing sequences of sounds. A recent study from our laboratory demonstrated that cortical neurons in anesthetized cats exhibit spatial stream segregation (SSS) by synchronizing preferentially to one of two sequences of noise bursts that alternate between two source locations. Here, we examine the emergence of SSS along the ascending auditory pathway. Extracellular recordings were made in anesthetized rats from the inferior colliculus (IC), the nucleus of the brachium of the IC (BIN), the medial geniculate body (MGB), and the primary auditory cortex (A1). Stimuli consisted of interleaved sequences of broadband noise bursts that alternated between two source locations. At stimulus presentation rates of 5 and 10 bursts per second, at which human listeners report robust 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 approximately two-thirds of neurons in the ventral MGB (MGBv), and is prominent throughout A1. The enhancement of SSS at the cortical level reflects both increased spatial sensitivity and increased forward suppression. We demonstrate that forward suppression in A1 does not result from synaptic inhibition at the cortical level. Instead, forward suppression might reflect synaptic depression in the thalamocortical projection. Together, our findings indicate that auditory streams are increasingly segregated along the ascending auditory pathway as distinct mutually synchronized neural populations.

Spectral breadth and laminar distribution of thalamocortical inputs to A1

“…Note that even prior studies using higher (5 mM) muscimol doses found no difference between the effects of muscimol alone vs. its effects when paired with a drug intended to block any action at GABA-B receptors (Happel et al 2014(Happel et al , 2010. Similarly, intracortical blockade of GABA-B receptors had no effect on the ability of neurons in rat A1 to follow trains of acoustic stimuli, i.e., no evidence for forward suppression mediated by GABA-B receptors (Yao et al 2015). Nonetheless, our results do not address the question of whether muscimol at higher doses affects presynaptic receptors in A1, an issue that future experiments will need to resolve.…”

Cortical Interneurons Differentially Regulate the Effects of Acoustic Context

“…We instead propose that short-term synaptic plasticity at interneurons’ inputs, rather than lingering inhibition from the masker tone, mediates the strength and frequency dependence of forward suppression. A more recent study (Yao et al, 2015) infused GABA receptor antagonists into the AC and found no attenuation of forward suppression. However, such antagonists act upon all sources of synaptic inhibition and may conflate the distinct effects of interneuron types observed in the current study.…”

“…Neural responses to a sound are often completely abolished when preceded by a spectrally similar sound and more weakly suppressed when preceded by a spectrally dissimilar sound—a phenomenon called forward suppression (FWS) (Brosch and Schreiner, 1997; Calford and Semple, 1995). Although forward suppression is also present subcortically (Malone and Semple, 2001; Schreiner, 1981; Watanabe and Simada, 1971), responses in the auditory cortex (AC) tend to recover more slowly from forward suppression (Fitzpatrick et al, 1999) and are unable to follow fast repetition rates (Creutzfeldt et al, 1980; Miller et al, 2002; Yao et al, 2015), suggesting that forward suppression is enhanced within the AC. How does this enhancement occur?…”

Animal models for auditory streaming

“…Spatial sensitivity for stream segregation and forward suppression was increased along the auditory pathway up to the primary auditory cortex providing for separate populations of neurons representing the streams of sounds from the different directions. Application of GABA receptor antagonists to the primary auditory cortex neurons suggested that forward suppression due to depression at the thalamo-cortical synapse is a major factor in auditory stream segregation [61].…”