Understanding degraded speech leads to perceptual gating of a brainstem reflex in human listeners.

The ability to navigate "cocktail party" situations by focusing on sounds of interest over irrelevant, background sounds is often considered in terms of cortical mechanisms. However, subcortical circuits such as the pathway underlying the medial olivocochlear (MOC) reflex modulate the activity of the inner ear itself, supporting the extraction of salient features from auditory scene prior to any cortical processing. To understand the contribution of auditory subcortical nuclei and the cochlea in complex listening tasks, we made physiological recordings along the auditory pathway while listeners engaged in detecting non(sense) words in lists of words. Both naturally spoken and intrinsically noisy, vocoded speech-filtering that mimics processing by a cochlear implant (CI)-significantly activated the MOC reflex, but this was not the case for speech in background noise, which more engaged midbrain and cortical resources. A model of the initial stages of auditory processing reproduced specific effects of each form of speech degradation, providing a rationale for goal-directed gating of the MOC reflex based on enhancing the representation of the energy envelope of the acoustic waveform. Our data reveal the coexistence of 2 strategies in the auditory system that may facilitate speech understanding in situations where the signal is either intrinsically degraded or masked by extrinsic acoustic energy. Whereas intrinsically degraded streams recruit the MOC reflex to improve representation of speech cues peripherally, extrinsically masked streams rely more on higher auditory centres to denoise signals.

Differences between children and adults in the neural encoding of voice fundamental frequency in the presence of noise and reverberation.

Environmental noise and reverberation challenge speech understanding more significantly in children than in adults. However, the neural/sensory basis for the difference is poorly understood. We evaluated the impact of noise and reverberation on the neural processing of the fundamental frequency of voice (f0 )-an important cue to tag or recognize a speaker. In a group of 39 6- to 15-year-old children and 26 adults with normal hearing, envelope following responses (EFRs) were elicited by a male-spoken /i/ in quiet, noise, reverberation, and both noise and reverberation. Due to increased resolvability of harmonics at lower than higher vowel formants that may affect susceptibility to noise and/or reverberation, the /i/ was modified to elicit two EFRs: one initiated by the low frequency first formant (F1) and the other initiated by mid to high frequency second and higher formants (F2+) with predominantly resolved and unresolved harmonics, respectively. F1 EFRs were more susceptible to noise whereas F2+ EFRs were more susceptible to reverberation. Reverberation resulted in greater attenuation of F1 EFRs in adults than children, and greater attenuation of F2+ EFRs in older than younger children. Reduced modulation depth caused by reverberation and noise explained changes in F2+ EFRs but was not the primary determinant for F1 EFRs. Experimental data paralleled modelled EFRs, especially for F1. Together, data suggest that noise or reverberation influences the robustness of f0 encoding depending on the resolvability of vowel harmonics and that maturation of processing temporal/envelope information of voice is delayed in reverberation, particularly for low frequency stimuli.

High-Frequency Resonance in the Gerbil Medial Superior Olive.

A high-frequency, subthreshold resonance in the guinea pig medial superior olive (MSO) was recently linked to the efficient extraction of spatial cues from the fine structure of acoustic stimuli. We report here that MSO neurons in gerbil also have resonant properties and, based on our whole-cell recordings and computational modeling, that a low-voltage-gated potassium current, IKLT, underlies the resonance. We show that resonance was lost following dynamic clamp replacement of IKLT with a leak conductance and in the model when voltage-gating of IKLT was suppressed. Resonance was characterized using small amplitude sinusoidal stimuli to generate impedance curves as typically done for linear systems analysis. Extending our study into the nonlinear, voltage-dependent regime, we increased stimulus amplitude and found, experimentally and in simulations, that the subthreshold resonant frequency (242Hz for weak stimuli) increased continuously to the resonant frequency for spiking (285Hz). The spike resonance of these phasic-firing (type III excitable) MSO neurons and of the model is of particular interest also because previous studies of resonance typically involved neurons/models (type II excitable, such as the standard Hodgkin-Huxley model) that can fire tonically for steady inputs. To probe more directly how these resonances relate to MSO neurons as slope-detectors, we presented periodic trains of brief, fast-rising excitatory post-synaptic potentials (EPSCs) to the model. While weak subthreshold EPSC trains were essentially low-pass filtered, resonance emerged as EPSC amplitude increased. Interestingly, for spike-evoking EPSC trains, the threshold amplitude at spike resonant frequency (317Hz) was lower than the single ESPC threshold. Our finding of a frequency-dependent threshold for repetitive brief EPSC stimuli and preferred frequency for spiking calls for further consideration of both subthreshold and suprathreshold resonance to fast and precise temporal processing in the MSO.

Subthreshold resonance properties contribute to the efficient coding of auditory spatial cues.

Neurons in the medial superior olive (MSO) and lateral superior olive (LSO) of the auditory brainstem code for sound-source location in the horizontal plane, extracting interaural time differences (ITDs) from the stimulus fine structure and interaural level differences (ILDs) from the stimulus envelope. Here, we demonstrate a postsynaptic gradient in temporal processing properties across the presumed tonotopic axis; neurons in the MSO and the low-frequency limb of the LSO exhibit fast intrinsic electrical resonances and low input impedances, consistent with their processing of ITDs in the temporal fine structure. Neurons in the high-frequency limb of the LSO show low-pass electrical properties, indicating they are better suited to extracting information from the slower, modulated envelopes of sounds. Using a modeling approach, we assess ITD and ILD sensitivity of the neural filters to natural sounds, demonstrating that the transformation in temporal processing along the tonotopic axis contributes to efficient extraction of auditory spatial cues.

Auditory Brainstem Models: Adapting Cochlear Nuclei Improve Spatial Encoding by the Medial Superior Olive in Reverberation.

Listeners typically perceive a sound as originating from the direction of its source, even as direct sound is followed milliseconds later by reflected sound from multiple different directions. Early-arriving sound is emphasised in the ascending auditory pathway, including the medial superior olive (MSO) where binaural neurons encode the interaural-time-difference (ITD) cue for spatial location. Perceptually, weighting of ITD conveyed during rising sound energy is stronger at 600 Hz than at 200 Hz, consistent with the minimum stimulus rate for binaural adaptation, and with the longer reverberation times at 600 Hz, compared with 200 Hz, in many natural outdoor environments. Here, we computationally explore the combined efficacy of adaptation prior to the binaural encoding of ITD cues, and excitatory binaural coincidence detection within MSO neurons, in emphasising ITDs conveyed in early-arriving sound. With excitatory inputs from adapting, nonlinear model spherical bushy cells (SBCs) of the bilateral cochlear nuclei, a nonlinear model MSO neuron with low-threshold potassium channels reproduces the rate-dependent emphasis of rising vs. peak sound energy in ITD encoding; adaptation is equally effective in the model MSO. Maintaining adaptation in model SBCs, and adjusting membrane speed in model MSO neurons, 'left' and 'right' populations of computationally efficient, linear model SBCs and MSO neurons reproduce this stronger weighting of ITD conveyed during rising sound energy at 600 Hz compared to 200 Hz. This hemispheric population model demonstrates a link between strong weighting of spatial information during rising sound energy, and correct unambiguous lateralisation of a speech source in reverberation.