Perceptual Gap Detection Is Mediated by Gap Termination Responses in Auditory Cortex

Abstract

Background Understanding speech in the presence of background noise often becomes increasingly difficult with age. These age-related speech processing deficits reflect impairments in temporal acuity. Gap detection is a model for temporal acuity in speech processing, in which a gap inserted in white noise acts as a cue that attenuates subsequent startle responses. Lesion studies have shown that auditory cortex is necessary for the detection of brief gaps, and auditory cortical neurons respond to the end of the gap with a characteristic burst of spikes called the gap termination response (GTR). However, it remains unknown whether or how the GTR plays a causal role in gap detection. We tested this by optogenetically suppressing the activity of somatostatin- or parvalbumin-expressing inhibitory interneurons, or CaMKII-expressing excitatory neurons, in auditory cortex of behaving mice during specific epochs of a gap detection protocol. Results Suppressing interneuron activity during the post-gap interval enhanced gap detection. Suppressing excitatory cells during this interval attenuated gap detection. Suppressing activity preceding the gap had the opposite behavioral effects, whereas prolonged suppression across both intervals had no effect on gap detection. Conclusions In addition to confirming cortical involvement, here we demonstrate for the first time a causal relationship between post-gap neural activity and perceptual gap detection. Furthermore, our results suggest that gap detection involves an ongoing comparison of pre- and post-gap spiking activity. Finally, we propose a simple, yet biologically plausible neural circuit that reproduces each of these neural and behavioral results.

Cortical Interneurons Differentially Regulate the Effects of Acoustic Context

“…For example, decreased forward suppression may be important for detecting gaps in noise—an important component of interpreting speech in noise—because it has recently been shown that increasing cortical responses after brief gaps (which would effectively reduce forward suppression) increases the ability to detect gaps (Weible et al, 2014). …”

Reductions in cortical alpha activity, enhancements in neural responses and impaired gap detection caused by sodium salicylate in awake guinea pigs

“…Interestingly, Weible et al . () found that suppressing cortical neural activity using optogenetics following a gap could attenuate subsequent behavioural startle responses for gaps with durations of ≤ 25 ms, but not for 50 ms gaps (the duration used here), which further suggests that cortical involvement is important only for shorter durations. Therefore, the effect on gap‐induced reductions of cortical evoked potentials that we have observed here may simply be a reflection of processing further down the auditory system.…”

“…Weible et al . () recently demonstrated that they could affect the degree of startle attenuation (as measured behaviourally) by using optogenetics to alter inhibitory and excitatory activity in the auditory cortices of mice, while preserving MGDTs. This therefore implies that there may be disparate underlying mechanisms between gap detection thresholds, which they suggested are a measure of temporal acuity, and inhibition of a startle response by a preceding gap, which they proposed as a measure of gap salience.…”

Auditory cortex interneuron development requires cadherins operating hair-cell mechanoelectrical transduction

“…After the fitting of cochlear implants, some of these patients have been reported to face unusual speech-recognition difficulties not observed in patients with mutations of other deafness genes (53). These difficulties might be related to the involvement of PV interneurons in the experience-driven neural plasticity underlying AC maturation (8,54) and the temporal precision of sound detection critical for speech perception (55). The shaping of the perception of several acoustic features throughout life, including frequency discrimination acuity (56) and the detection of unexpected sounds, also involves PV interneurons of the AC (57).…”