Neural correlates of perceptual learning in the auditory brainstem: efferent activity predicts and reflects improvement at a speech-in-noise discrimination task

Abstract

An extensive corticofugal system extends from the auditory cortex toward subcortical nuclei along the auditory pathway. Corticofugal influences reach even into the inner ear via the efferents of the olivocochlear bundle, the medial branch of which modulates preneural sound amplification gain. This corticofugal system is thought to contribute to neuroplasticity underlying auditory perceptual learning. In the present study, we investigated the involvement of the medial olivocochlear bundle (MOCB) in perceptual learning as a result of auditory training. MOCB activity was monitored in normal-hearing adult listeners during a 5 d training regimen on a consonant-vowel phoneme-in-noise discrimination task. The results show significant group learning, with great inter-individual variability in initial performance and improvement. As observed in previous auditory training studies, poor initial performers tended to show greater learning. Strikingly, MOCB activity measured on the first training day strongly predicted the subsequent amount of improvement, such that weaker initial MOCB activity was associated with greater improvement. Moreover, in listeners that improved significantly, an increase in MOCB activity was observed after training. Thus, as discrimination thresholds of listeners converged over the course of training, differences in MOCB activity between listeners decreased. Additional analysis showed that MOCB activity did not explain variation in performance between listeners on any training day but rather reflected an individual listener's performance relative to their personal optimal range. The findings suggest an MOCB-mediated listening strategy that facilitates speech-in-noise perception. The operation of this strategy is flexible and susceptible to training, presumably because of task-related adaptation of descending control from the cortex.

Figure 1.

Behavioral results. A, Average discrimination threshold as a function of training day. Error bars show SEM. B, C, Example learning curves of individual participants showing significant (learner) and nonsignificant (nonlearner) improvement. D, Distribution of learning slopes for learners and nonlearners. Box plot shows median and interquartile range. E, Initial discrimination threshold versus fitted learning slope. Open circle shows outlier not included in correlation analysis. F, Average discrimination threshold as a function of training day for learners (open circles) and nonlearners (filled circles).

Figure 2.

Physiological results. Average contralateral suppression of CEOAEs as a function of training day. Left column (A, C), Amplitude suppression at 30 dB SL. Right column (B, D), I/O suppression. A, B, Average suppression over all participants. C, D, Average suppression of CEOAEs for learners (open circles) and nonlearners (filled circles). *p < 0.05; **p < 0.01.

Figure 3.

Correlation between behavioral and physiological measures. All plots refer to suppression of CEOAEs on the first training day. Left column (A, C), Amplitude suppression at 30 dB SL. Right column (B, D), I/O suppression. Top row (A, B), Suppression versus learning slope. Bottom row (C, D), Suppression versus initial discrimination threshold. Open circles indicate individual values for learners and filled circles for nonlearners.