Abnormal neural encoding of repeated speech stimuli in noise in children with learning problems
Introduction
The ability of a listener to understand real speech in a natural environment places many demands on the auditory system. Among these demands are the accurate representation of rapidly changing spectral information comprising the speech signal and the separation of this signal from background noise. While all listeners clearly demonstrate impaired perception at extremes in speaking rate and background noise, a subset of listeners experiences enhanced sensitivity to the detrimental effects of repeated stimulation and background noise. Many studies have shown that subjects diagnosed with language-based learning disabilities perform poorly when processing rapid acoustic signals (Tallal and Piercy, 1974, Farmer and Klein, 1995, Hari and Kiesila, 1996, Wright et al., 1997, Nagarajan et al., 1999, Cestnick and Jerger, 2000, Temple et al., 2000). Similarly diagnosed subjects have exceptional difficulty processing acoustic signals which are presented in the presence of noise (Jerger et al., 1987, Breedin et al., 1989, Katz, 1992, Katz et al., 1992, Welsh et al., 1996, Bellis, 1996, Chermak and Musiek, 1997, Cunningham et al., 2001). Neurobiological abnormalities accompany many of these auditory processing deficits (Nagarajan et al., 1999, Temple et al., 2000, Cunningham et al., 2001). These findings contribute to an understanding that some language-based learning disabilities are rooted, in part, in altered representations of acoustic information. Distorted encoding of acoustic speech signals could underlie weakened perception and categorization of phonemic information (Kraus et al., 1996, King et al., 2002). Such deficits could certainly contribute to difficulties in the development of reading and other language skills (Godfrey et al., 1981, Reed, 1989, McBride-Chang, 1996).
While the primary goal of the current study was to understand auditory processing in children with learning problems, there was also motivation to further understand normal neural mechanisms which underlie processing of repeated stimuli, and stimuli in noise, especially when these stresses are combined, as they are in most real listening environments. Studies of normal subjects have shown that cortical responses decrease in amplitude and increase in latency upon repetition of stimuli (Woods and Elmasian, 1986, Budd et al., 1998) and following the addition of noise (Whiting et al., 1998, Martin et al., 1999).
Inspired by the aforementioned findings, the present study was designed to further examine effects of stimulus repetition and background noise on the neural representation of auditory stimuli in normal and learning impaired subjects. Specifically, the intent was to expand upon previous studies, which investigated rapid or repetitive stimuli or noise in isolation, often using simple tonal stimuli. By simultaneously stressing the auditory system with stimulus repetition and background noise, and by using a complex speech stimulus, the present study incorporated conditions which simulated real listening situations more accurately than studies which incorporated some of these features in isolation. Additionally, non-linear transformations throughout the auditory system make difficult the prediction of responses to complex signal patterns based on knowledge of responses to simpler stimuli (Sachs et al., 1983, Rauschecker, 1997). Responses elicited by our paradigm thus provide further insight into the neural representation of speech under ‘real world’ conditions. Since learning disabilities manifest themselves outside of the laboratory in normal, everyday life, it is by mimicking real conditions that we may most accurately describe any neural abnormalities underlying such problems.
Section snippets
Subjects
Subjects were 25 English-speaking children (mean age 11.1±1.8 years) with normal bilateral hearing (pure tone thresholds <20 dB HL for octaves 500–4000 Hz). These children were chosen from a pool of subjects who participated in earlier related studies conducted by this laboratory. In accordance with the approval of this research by the Northwestern University Institutional Review Board, all subjects and their legal guardians signed forms which acknowledged their informed consent. Thirteen
Normal, unstressed response
Average responses are shown in Fig. 1. In the best cases, usually in the unstressed responses (i.e. initial stimulus in train, prior to repetition, in quiet), the normal P1/N1/P2/N2 complex could be observed. These consist of the positively deflected P1 occurring around 75 ms post-stimulus-onset, followed by the N1 negativity. These are followed by the second major positive deflection, P2, occurring around 150 ms, followed by the major N2 negativity. The response then gradually returns to
Discussion
This is the first study to investigate the simultaneous effects of background noise and stimulus repetition on speech-evoked cortical responses in normal and learning impaired children. This study demonstrated a deficiency in the neural representation of repeated speech stimuli in noise in children diagnosed with learning problems. Specifically, the timing and subsequent shape of the repeated responses, as reflected by the correlation between responses in noise, were distorted in the learning
Conclusions
A group of children diagnosed with language-based learning problems were shown to encode auditory information in an abnormal way. Specifically, these children exhibited distortion of the timing of cortical responses to repeated speech in noise. This measure of response distortion was related to behavioral measures that tested abilities to perceive and manipulate speech sounds. These findings further support theories that argue for abnormal sensory-encoding bases of higher-level learning
Acknowledgements
Much thanks goes to Cynthia King, Erin Hayes, Catherine Warrier, Jenna Cunningham, Steven Zecker, Ann Bradlow and Jim Baker. This work was supported by National Institutes of Health Grants R01DC01510 and T32DC0001517.
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