Research paperInvestigation of auditory processing disorder and language impairment using the speech-evoked auditory brainstem response
Highlights
► Speech-evoked auditory brainstem responses reflect complex acoustics. ► Children with (C)APD and LI showed abnormal encoding for specific acoustic features. ► Response in the LI group was impaired for the temporal and frequency encoding measures. ► Responses in the (C)APD group presented abnormalities only for the temporal measures.
Introduction
About seven percent of children have significant difficulties in language functioning (receptive and/or expressive language impairment) for no apparent reason (Leonard, 1998; Tomblin et al., 1997). In other words, these children present with a developmental language impairment in the absence of mental retardation, sensory disorders, serious emotional or physiological problems, or environmental deprivation (Leonard, 1998).
Despite a significant amount of research, no consensus has yet been reached on a theory that explains, at least in part, the etiology of LI. The temporal auditory processing deficit theory suggests that one causal deficit of LI is an impaired ability to process sounds (non-speech and speech) that occur rapidly in time, as well as an abnormal neural encoding of auditory information (Farmer and Klein, 1995; Tallal and Piercy, 1974). These deficits contribute to an impaired perception of crucial acoustic cues contained in speech signals.
The ability to perceive rapidly changing temporal (on the order of milliseconds) and spectral characteristics of speech is essential for language development. Whenever there is a deficit in this rapid auditory processing system, an unstable or blurred representation of speech sound (phoneme) is produced in the brain. These unstable phoneme representations could impact speech perception and the language learning abilities of phonology, syntax, or semantics (Benasich and Tallal, 2002; Tallal, 2000).
The possible connection between auditory skills and language has led to the investigation of auditory neural activity and the behavioral manifestations of language impairment (Tallal and Piercy, 1973; Benasish and Tallal, 1996; Tallal, 2000; Banai et al., 2007; Basu et al., 2009). As such, many research groups have also tried to better understand whether the relationship between (central) auditory processing disorder and LI is causal or associated.
(C)APD can be defined as a deficit in the “perceptual processing of auditory information in the central nervous system (CNS) and the neurobiological activity that underlies that processing and gives rise to the electrophysiological auditory potentials” (American Speech-Language-Hearing Association [ASHA], 2005, p. 2). As with LI children, children with (C)APD also present with heterogenous manifestations of the disorder (ASHA, 2005; Musiek and Chermak, 2007), and many of these (C)APD children also exhibit difficulties in reading, spelling and language (ASHA, 2005; Dawes et al., 2008; Jerger and Musiek, 2000).
Similarities in the symptoms of (C)APD and LI have been described, and several researchers have investigated the performance of children with LI on behavioral tests of central auditory processing (Dawes and Bishop, 2009; Ferguson et al., 2011; Miller, 2011). For instance, children with LI exhibit abnormal temporal processing and discrimination of the frequency (Lowe and Campbell, 1965; Tallal and Piercy, 1973,; McArthur and Bishop, 2004; Mengler et al., 2005). In addition, a recent study (Ferguson et al., 2011) showed that children with (C)APD or specific language impairment, two different clinical diagnoses, performed similarly on multiple measures. In fact, the authors suggest poor attention may be the basis of previously reported listening difficulties, and they propose that (C)APD and SLI may be indistinguishable. In the same way, Miller and Wagstaff (2011) found a similar behavioral profile in children with (C)APD and SLI.
Although the presence of auditory processing deficits has been supported by many studies using behavioral measures, there is still a lack of evidence for the rapid auditory processing or discrimination deficits in the LI population (Bishop et al., 1999; Helzer et al., 1996; Sussman, 1993; Tomblin et al., 1995). Because the performance of children with LI is variable for auditory tasks, it is difficult to determine conclusively if the relationship between auditory skills and LI is causal or associated. Furthermore, from the perspective of (C)APD, the lack of agreement about a ‘gold standard’ diagnostic test makes it difficult to make a differential diagnosis (Ferguson et al., 2011). Despite these divergences, it is widely acknowledged that electrophysiological studies provide information about the sequence, timing, and location of neural events involved in auditory processing, and these studies have been useful to establish basic structure-function relationships in the human auditory system (Hall, 2007).
To assess the auditory pathway integrity, the auditory brainstem response (ABR) to acoustic stimuli (e.g. clicks or tones) has been used in clinical practice (Moller, 1999; Starr and Don, 1988). Additionally, the ABR can be evoked by more complex stimuli such as speech signals (Cunningham et al., 2001; Russo et al., 2004; Wible et al., 2004).
Several studies of the brainstem encoding of speech sounds have been conducted in native English, Arabic, Hebrew, and Chinese speakers (Russo et al., 2004a; Karawani and Banai, 2010; Krishnan et al., 2010). As a consequence of the specific characteristics of acoustic signals that are maintained and reflected with remarkable precision in the subcortical pathway, those studies were able to provide direct information on how speech syllables are neuronally encoded by the auditory system (Chandrasekaran and Kraus, 2010; Johnson et al., 2005, 2008; Russo et al., 2004).
An increasing number of studies using speech signals to assess the auditory processing of linguistic elements have shown that the neural encoding of the speech stimulus /da/ is compromised in individuals with abnormal cortical speech processing, language, reading, and learning impairments (Abrams et al., 2006; Banai et al., 2009; Hornickel, Skoe, & Kraus, 2009a; Karawani and Banai, 2010; Krishnan, 2002; Russo et al., 2004).
The previously mentioned studies have reported a particular difficulty in differentiating between a diagnosis of (C)APD and of LI, have provided evidence of the similarities between the behavioral and cognitive profiles of children with (C)APD and SLI, and have established links between speech encoding, auditory processing, and language ability. Motivated by these findings, our first question was whether LI and (C)APD children may also have similarities in electrophysiological responses.
Therefore, this study aimed to investigate, through speech-evoked ABR, how the speech sounds are encoded in the brainstems of children with LI and (C)APD compared with typically developing children and if the encoding of the speech is disrupted in these children. More specifically, this study focused on whether there are differences between the speech-evoked ABR in 1) children who had received a diagnosis of LI from a Speech-Language Pathologist and in 2) children who had received a diagnosis of (C)APD from an Audiologist. Considering the extensive research describing the temporal processing abnormalities in LI children, the hypothesis of this study was that children with LI and (C)APD would likewise demonstrate greater deficits in the neural encoding of speech sounds in the subcortical auditory pathways in response to a rapid speech rate. Accordingly, this study aimed to provide additional information about the central auditory function in individuals with LI and (C)APD. This work was also designed to provide assistance with an early differential diagnosis, thereby providing earlier opportunities to better develop and implement appropriate and effective remediation strategies.
Section snippets
Methods
This study was carried out in the Auditory Processing Laboratory, Universidade de São Paulo School of Medicine (USP), São Paulo, Brazil, in accordance with the Institutional Review Board, which approved this research (Protocol no. 1049/07). All of the legal guardians and parents of the participating children signed forms acknowledging their informed consent prior to the evaluation.
Timing measures
The timing measure was defined as the latencies of the seven prominent response peaks (denoted V, A, C, D, E, F, and O) obtained from the waveform of each individual. These responses were analyzed and compared using one-way ANOVA and the Tukey adjusted multiple comparison tests (Tables 2 and 3).
The grand averaged speech-evoked ABR responses for the three groups are shown in Fig. 2. Overall the TD and (C)APD waveform morphologies were more similar in comparison with the LI waveform morphology,
Discussion
The comparative analysis of the speech-evoked auditory brainstem responses revealed abnormal encoding for specific acoustic features in the responses of the (C)APD and LI groups. These findings corroborated other studies on the difficulties in speech perception that might reflect abnormal speech-evoked ABR (Cunningham et al., 2001; Russo et al., 2004; Billiet & Bellis, 2011).
The grand averaged speech-evoked ABR response waveform (Fig. 2) comparisons among the groups showed more morphological
Conclusion
This study found abnormal encoding for specific acoustic features, which are the speech characteristics of children with (C)APD and LI. These findings appear to confirm that abnormal speech-evoked ABR should manifest as difficulties in speech perception. However, it was verified that the (C)APD group presented with abnormalities for the temporal measures only, while the LI group was impaired for both the temporal measures and the frequency encoding measures. In other words, the LI group
Declaration of interest
The authors report no conflict of interest.
Acknowledgments
We would like to thank all the study participants. The author would like to give special thanks to Nina Kraus and Erika Skoe for providing us the Matlab Analysis Program (Brainstem Toolbox). This study was supported by São Paulo Research Foundation – FAPESP.
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