Context-Dependent Encoding in the Human Auditory Brainstem Relates to Hearing Speech in Noise: Implications for Developmental Dyslexia

Abstract

SUMMARY We examined context-dependent encoding of speech in children with and without developmental dyslexia by measuring auditory brainstem responses to a speech syllable presented in a repetitive or variable context. Typically developing children showed enhanced brainstem representation of features related to voice pitch in the repetitive context, relative to the variable context. In contrast, children with developmental dyslexia exhibited impairment in their ability to modify representation in predictable contexts. From a functional perspective, we found that the extent of context-dependent encoding in the auditory brainstem positively correlated with behavioral indices of speech perception in noise. The ability to sharpen representation of repeating elements is crucial to speech perception in noise, since it allows superior ‘tagging’ of voice pitch, an important cue for segregating sound streams in background noise. The disruption of this mechanism contributes to a critical deficit in noise-exclusion, a hallmark symptom in developmental dyslexia.

Dysfunction of the auditory thalamus in developmental dyslexia

“…Building up accurate predictions about fast sensory dynamics would result in higher accuracy and processing speed when the perceptual system is confronted with taxing conditions, such as fast stimulus presentation rates or high memory load, i.e., precisely the situations in which dyslexic participants perform consistently worse than control participants (8,29,44). Because several cognitive operations may require precisely tuned sensory processing, a failure in dyslexia to tune auditory processing to relevant spectrotemporal properties of speech sounds might explain not only poor phonological processing (1,5,6), but also several other symptoms of dyslexia such as the failure to improve the discrimination of speech and nonspeech sounds with repetition (17,18), difficulties understanding speech in noisy environments (18,34,45), and attentional limitations in processing fast sequences of stimuli (10). This account would also be in line with key features of two further theories about dyslexia, i.e., the SAS hypothesis and the anchoring deficit theory (10,17).…”

“…The anchoring-deficit theory (17) is based on the finding that dyslexics, contrary to control participants, do not benefit from stimulus repetition in samedifferent judgment tasks on tones (see also ref. 18). This theory posits that dyslexics' perceptual system is deficient in predicting incoming sensory input.…”

“…A deficient tuning of sensory processing in dyslexia can also account for the difficulties that dyslexics have in understanding speech in noisy environments, for example with perceiving subtle but distinctive features of speech sounds as in "bad" and "dad" in noisy environments (18,34,45). In this case, cortical predictions could shape MGB responses to the subtle and transient but predictable spectrotemporal cues that enable the categorical recognition of speech sounds.…”

“…Second, the left MGB has been found to be altered in postmortem brains of dyslexic persons (13), leading to the speculation that dyslexia can be attributed to MGB function (11,12). Third, recent studies emphasize the fact that dyslexics' difficulties seem to result from not using previous or contextual information to finetune sensory perception for optimal performance (17,18). These findings fit well with the recent reconceptualization of sensory thalamus function: although sensory thalamic structures were previously considered as simple relay stations, they are now described as smart gatekeepers because they are tuned by cortical areas to the relevant properties of sensory input (reviewed in refs.…”

Age-Related Changes in the Relationship Between Auditory Brainstem Responses and Envelope-Following Responses

“…FFRs and EFRs are evoked in response to longer, often more spectro-temporally complex stimuli (Krishnan 1999(Krishnan , 2002Krishnan et al 2004;Swaminathan et al 2008), and are strongly influenced by rostral brainstem and midbrain generators (Kiren et al 1994;Kuwada et al 2002;Akhoun et al 2010;Chandrasekaran and Kraus 2010;Parthasarathy and Bartlett 2012). They have been used to show differences in processing of complex stimuli under various pathological conditions, such as age-related hearing loss, dyslexia, and autism (McAnally and Stein 1997;Chandrasekaran et al 2009;Russo et al 2009;Anderson et al 2012;Clinard and Tremblay 2013).…”