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.

Medial Olivocochlear-Induced Transient-Evoked Otoacoustic Emission Amplitude Shifts in Individual Subjects

“…Activation of the MEMR has been shown to reduce OAE amplitudes (Whitehead et al 1991). Many studies of MOC shifts using TEOAEs have therefore inferred the absence of MEMR activation by using noise levels that do not elicit the MEMR as assessed using standard clinical measurements employing a 226-Hz probe tone (e.g., Collet et al 1990;De Boer and Thornton 2008;De Ceulaer et al 2001). However, others have suggested that subclinical activation of the MEMR may be sufficient to impact measurement of MOC shifts (Feeney and Keefe 2001;Guinan et al 2003), which would limit the usefulness of clinical measurement criteria.…”

“…Some previous studies have inferred lack of MEMR activation based on clinical immittance measurements (e.g., Collet et al 1990;De Boer and Thornton 2008;De Ceulaer et al 2001). However, it is possible that subclinical activation of the MEMR could confound or contaminate MOC shifts (Feeney and Keefe 2001;Guinan et al 2003).…”

Subcortical Plasticity Following Perceptual Learning in a Pitch Discrimination Task

“…Previous reports of plasticity in the adult human auditory system have been generally limited to cortical measures of auditory processing. There is, however, increasing evidence that short-term training (de Boer and Thornton 2008;Song et al 2008) or short-term sensory deprivation (Munro and Blount 2009) can modify subcortical measures of auditory processing even in adulthood. The results of our study complement a growing body of research indicating that long-term experience in the discrimination and identification of pitch-evoking stimuli, obtained through the acquisition of a tone language or musical practice, modifies auditory processing at the level of the brainstem (see Tzounopoulos and Kraus 2009; Krishnan and Gandour 2009 for reviews).…”

“…In a recent study, de Boer and Thornton (2008) found that activity of the medial olivocochlear bundle, which sends efferent signals from the brainstem to the cochlea, and is part of the corticofugal efferent system, reflected improvements on a speech in noise discrimination task after a period of auditory discrimination training. The corticofugal system, that projects from the auditory cortex to all major brainstem nuclei (Winer 2006), is likely to play a crucial role in subcortical plasticity.…”

Separating medial olivocochlear from acoustic reflex effects on transient evoked otoacoustic emissions in unanesthetized mice

“…Descending neural pathways in the mammalian auditory system are believed to modulate the function of the peripheral auditory system [3,8,10]. These pathways include the medial olivocochlear (MOC) efferent innervation to the cochlear outer hair cells (OHCs) and the acoustic reflex pathways mediating middle ear muscle (MEM) contractions.…”