Abnormal cortical processing of the syllable rate of speech in poor readers

Abstract

Children with reading impairments have long been associated with impaired perception for rapidly presented acoustic stimuli and recently have shown deficits for slower features. It is not known whether impairments for low-frequency acoustic features negatively impact processing of speech in reading-impaired individuals. Here we provide neurophysiological evidence that poor readers have impaired representation of the speech envelope, the acoustical cue that provides syllable pattern information in speech. We measured cortical-evoked potentials in response to sentence stimuli and found that good readers indicated consistent right-hemisphere dominance in auditory cortex for all measures of speech envelope representation, including the precision, timing, and magnitude of cortical responses. Poor readers showed abnormal patterns of cerebral asymmetry for all measures of speech envelope representation. Moreover, cortical measures of speech envelope representation predicted up to 41% of the variability in standardized reading scores and 50% in measures of phonological processing across a wide range of abilities. Our findings strongly support a relationship between acoustic-level processing and higher-level language abilities, and are the first to link reading ability with cortical processing of low-frequency acoustic features in the speech signal. Our results also support the hypothesis that asymmetric routing between cerebral hemispheres represents an important mechanism for temporal encoding in the human auditory system, and the need for an expansion of the temporal processing hypothesis for reading disabilities to encompass impairments for a wider range of speech features than previously acknowledged.

Figure 1.

Top, Grand average cortical responses from left- (Tp7, blue) and right- (Tp8, red) hemisphere temporal lobe electrodes and the broadband speech envelope (black) for “clear” (left) and “compressed” (right) stimulus conditions. Ninety-five milliseconds of the prestimulus period are plotted. The speech envelope was shifted forward in time 85 ms to enable comparison to cortical responses; this time shift is for display purposes only. The “onset” period of the response is defined as 0–250 ms after stimulus; the “envelope-following” period is 250–1500 ms for the clear condition, and 250–750 ms for the compressed condition. Bottom, Grand mean cross-correlograms calculated between the speech envelope and subjects' cortical responses during the envelope-following period.

Figure 2.

Average phase-locking precision (top) and timing (bottom) values. Values represent the average collapsed left- (blue; T3, T5, Tp7) and right- (red; T4, T6, Tp8) hemisphere results. Error bars represent 1 SEM.

Figure 3.

Average phase-locking magnitude for the envelope-following period measured at six electrode locations. The envelope-following period was defined as 250–1500 ms (clear and conversational speech conditions) or 250–750 ms (compressed speech condition). Blue symbols represent left-hemisphere electrodes, and red symbols represent right-hemisphere electrodes.

Figure 4.

Three measures of cortical speech envelope representation and standardized measures of reading (top row) and phonological processing (bottom row). The ordinate for all plots is standard score. Left column, The abscissa is the left- and right-hemisphere r values from the cross-correlation analysis of the compressed speech condition, entered into the asymmetry index (R − L)/(R + L). Middle column, The abscissa is the left- and right-hemisphere lags from the cross-correlation analysis, averaged across the three speech conditions, and entered into the asymmetry index (R − L)/(R + L). Right column, The abscissa is the left- (T3 and Tp7) and right- (T4 and Tp8) hemisphere envelope-following RMS amplitude for the compressed speech condition, entered into the asymmetry index (R − L)/(R + L).