Envelope enhancement increases cortical sensitivity to interaural envelope delays with acoustic and electric hearing

Abstract

Evidence from human psychophysical and animal electrophysiological studies suggests that sensitivity to interaural time delay (ITD) in the modulating envelope of a high-frequency carrier can be enhanced using half-wave rectified stimuli. Recent evidence has shown potential benefits of equivalent electrical stimuli to deaf individuals with bilateral cochlear implants (CIs). In the current study we assessed the effects of envelope shape on ITD sensitivity in the primary auditory cortex of normal-hearing ferrets, and profoundly-deaf animals with bilateral CIs. In normal-hearing animals, cortical sensitivity to ITDs (±1 ms in 0.1-ms steps) was assessed in response to dichotically-presented i) sinusoidal amplitude-modulated (SAM) and ii) half-wave rectified (HWR) tones (100-ms duration; 70 dB SPL) presented at the best-frequency of the unit over a range of modulation frequencies. In separate experiments, adult ferrets were deafened with neomycin administration and bilaterally-implanted with intra-cochlear electrode arrays. Electrically-evoked auditory brainstem responses (EABRs) were recorded in response to bipolar electrical stimulation of the apical pair of electrodes with singe biphasic current pulses (40 µs per phase) over a range of current levels to measure hearing thresholds. Subsequently, we recorded cortical sensitivity to ITDs (±800 µs in 80-µs steps) within the envelope of SAM and HWR biphasic-pulse trains (40 µs per phase; 6000 pulses per second, 100-ms duration) over a range of modulation frequencies. In normal-hearing animals, nearly a third of cortical neurons were sensitive to envelope-ITDs in response to SAM tones. In deaf animals with bilateral CI, the proportion of ITD-sensitive cortical neurons was approximately a fifth in response to SAM pulse trains. In normal-hearing and deaf animals with bilateral CI the proportion of ITD sensitive units and neural sensitivity to ITDs increased in response to HWR, compared with SAM stimuli. Consequently, novel stimulation strategies based on envelope enhancement may prove beneficial to individuals with bilateral cochlear implants.

Figure 1. Acoustic stimuli presented to normal-hearing animals.

Time waveforms illustrating the acoustic stimuli that were presented, including SAM (A) and HWR tones (B). An interaural time delay (ITD) was created by delaying the envelope in one channel and advancing it in the other by an equal amount. The box shows a segment of the stimulus envelope and fine structure in more detail.

Figure 2. Electrically-evoked auditory brainstem responses from a deaf animal with cochlear implants.

(A) Representative electrically-evoked auditory brainstem responses (EABR) plotted for each stimulus level. The black bar represents 1 µV. (B) Amplitude of wave IV of the EABR plotted against stimulus level.

Figure 3. Electrical stimuli presented to deaf animals with cochlear implants.

Time waveforms of the electrical stimuli that were presented, including SAM (A) and HWR biphasic-pulse trains (B). The box shows a segment of the stimulus envelope and fine structure in more detail.

Figure 4. Stimulus artifact.

(A) Example of a cortical recording in response to bilateral intra-cochlear electrical stimulation. The stimulus artifact is coincident in time with the stimulus. (B) Responses containing artifact were sub-classified using artifact rejection methods (plotted using different shades of line). (C) Example of recording following artifact rejection. Crosses mark probable neural responses. Low spike counts suggest that neural responses may have been removed with the artifact rejection method. The bar to the right of B & C represents the same amplitude and the stimulus artifact is significantly larger than the neural response.

Figure 5. Cortical responses from a normal-hearing animal.

Example of dot-raster plots (A & B) and post-stimulus time histograms (C & D) for an individual unit with a significant response to both SAM (A & C) and HWR tones (B & D). The stimulus duration is represented by the light grey bar. Dot-raster plots (A & B) show spike timing as black dots, with time and stimulus plotted on the x- and y-axes, respectively. Along the y-axis the different stimuli are arranged from higher- to lower-frequency of modulation and from positive to negative ITDs.

Figure 6. Average post-stimulus time histogram from all normal-hearing animals.

(A) Average post-stimulus time histogram across the population of units in response to SAM (black line) and HWR tones (grey line). The stimulus duration is represented by the light grey bar. (B) Mean spike rate in response to SAM (black lines) and HWR tones (grey lines) across all units, for the onset- (dashed lines) and offset-response windows (solid lines), are superimposed by aligning the stimulus onset and offset at time = 0 on the abscissa.

Figure 7. ITD functions in normal-hearing animals.

Examples of normalized ITD functions in response to SAM and HWR tones. Each ITD response function was derived from evenly spaced recording locations along the same electrode penetration, positioned orthogonal to the cortical surface.

Figure 8. ITD sensitive units in normal-hearing animals.

Percentage of responsive units with ITD sensitivity within the onset and offset response to SAM and HWR tones.

Figure 9. ITD sensitivity index in normal-hearing animals.

(A) ITD sensitivity index for individual units plotted for onset (closed circles) and offset (open circles) responses to SAM and HWR tones. (B) Mean ITD sensitivity index (± SD) plotted against stimulus condition for onset and offset responses.

Figure 10. Average ITD sensitivity index for each modulation frequency in normal-hearing animals.

Mean ITD sensitivity index (± SD) plotted against modulation frequency for (A) onset and (B) offset responses to SAM (black bars) and HWR tones (grey bars).

Figure 11. Cortical responses from a deaf animal with cochlear implants.

Example of dot-raster plots (A & B) and post-stimulus time histograms (C & D) for an individual unit with a significant response to both SAM (A & C) and HWR pulse trains (B & D). Note the x-axis plots time after the stimulus offset. Dot-raster plots (A & B) show spike timing as black dots, with time and stimulus plotted on the x- and y-axes, respectively. Along the y-axis the different stimuli are arranged from higher- to lower-frequency of modulation and from positive to negative ITDs (as in Figure 5).

Figure 12. Average post-stimulus time histogram from deaf animals with cochlear implants.

Average post-stimulus time histogram across the population of units in response to SAM (black line) and HWR pulse trains (grey line). Note the x-axis plots time after the stimulus offset.

Figure 13. ITD functions in deaf animals with cochlear implants.

Examples of normalized ITD functions in response to SAM and HWR pulse trains. Each ITD response function was derived from evenly spaced recording locations along the same electrode penetration, positioned orthogonal to the cortical surface (as in Figure 7).

Figure 14. ITD sensitivity index in deaf animals with cochlear implants.

(A) ITD sensitivity index for individual units plotted for offset responses to SAM and HWR pulse trains. (B) Mean ITD sensitivity index (± SD) plotted against stimulus condition for offset responses.