Fast and slow effects of medial olivocochlear efferent activity in humans

Abstract

Background: The medial olivocochlear (MOC) pathway modulates basilar membrane motion and auditory nerve activity on both a fast (10-100 ms) and a slow (10-100 s) time scale in guinea pigs. The slow MOC modulation of cochlear activity is postulated to aide in protection against acoustic trauma. However in humans, the existence and functional roles of slow MOC effects remain unexplored.

Methodology/principal findings: By employing contralateral noise at moderate to high levels (68 and 83 dB SPL) as an MOC reflex elicitor, and spontaneous otoacoustic emissions (SOAEs) as a non-invasive probe of the cochlea, we demonstrated MOC modulation of human cochlear output both on a fast and a slow time scale, analogous to the fast and slow MOC efferent effects observed on basilar membrane vibration and auditory nerve activity in guinea pigs. The magnitude of slow effects was minimal compared with that of fast effects. Consistent with basilar membrane and auditory nerve activity data, SOAE level was reduced by both fast and slow MOC effects, whereas SOAE frequency was elevated by fast and reduced by slow MOC effects. The magnitudes of fast and slow effects on SOAE level were positively correlated.

Conclusions/significance: Contralateral noise up to 83 dB SPL elicited minimal yet significant changes in both SOAE level and frequency on a slow time scale, consistent with a high threshold or small magnitude of slow MOC effects in humans.

Figure 1. Schematic of the experimental paradigm.

Each SOAE was monitored for 302 s. Baseline SOAE level and frequency were established in the pre-stimulation window. Contralateral broadband noise pulses (3-s long, 68 dB SPL) were presented in the 102-s stimulation window with 3-s inter-pulse intervals. Blue arrows represent SOAE estimates in the pre- and post-stimulation windows, red arrows during noise pulses, and green arrows during inter-pulse intervals. This color convention is consistent throughout the paper. Each arrow represents an estimate of SOAE level or frequency averaged over a 1-s window.

Figure 2. Example of MOC effects on one SOAE (subject WTPF01).

SOAE level over six consecutive repetitions of the stimulation paradigm (A), and averaged level over six repetitions (C) are shown in the top row (blue: pre- and post-stimulation windows; red: during noise pulses; green: inter-pulse intervals). The black rectangular box in Panel A represent the noise pulses which are shown only for the first experimental run but were repeated six times. Baseline () is defined as the median SOAE level/frequency in the 30-s window before noise onset. Similarly, SOAE levels/frequencies during the first two noise pulses (), during the last two noise pulses (), during the last two inter-pulse intervals () and in the 30-s window after noise offset () were quantified. Differences from the baseline were defined as fast change (-), adaptation change (-), buildup change (-) and slow change (-). Error bars represent one standard deviation.

Figure 3. Scatter plot of MOC-induced changes in SOAE level (left column) and frequency (middle and right columns) as functions of baseline SOAE level (upper row) and frequency (lower row).

Filled and open symbols represent statistically significant (t-test, p<0.01) and non-significant (t-test, p≥0.01) changes from baseline, respectively. Fast and adaptation changes are larger in magnitude than buildup and slow changes.

Figure 4. Comparison of magnitudes of fast, adaptation, buildup and slow changes (N = 32, 33, 44, 44, respectively) in SOAE level (A) and frequency (B, C).

The results of a paired Wilcoxon signed-rank test demonstrated that slow and buildup changes were significantly smaller than fast and adaptation changes (*: p<1e-6). The central line on each box is the median value. The top and bottom edge lines represent 25^th and 75^th percentiles, respectively. Whiskers cover all data points within 1.5 interquartile range from the top and bottom edge lines. Red crosses mark outliers beyond the whiskers.

Figure 5. Correlation between MOC-induced fast and slow changes in SOAE level (A) and frequency (B, C).

Filled symbols indicate that both fast and slow changes were statistically significant (t-test, p<0.01), whereas open symbols indicate otherwise. A positive correlation for SOAE level was observed. Dashed lines represent best linear fits to all of the data points.

Figure 6. Comparison of slow changes elicited by two contralateral noise levels, 68 and 83 dB SPL, in SOAE level (A) and frequency (B) (subjects WTPF01, WPTF31 and WTPF38).

Filled symbols indicate slow changes elicited by both noise levels were statistically significant (t-test, p<0.01), whereas open symbols indicate otherwise. No prominent elicitor-level effect on slow changes was observed.