Cortical auditory signal processing in poor readers

Abstract

Magnetoencephalographic responses recorded from auditory cortex evoked by brief and rapidly successive stimuli differed between adults with poor vs. good reading abilities in four important ways. First, the response amplitude evoked by short-duration acoustic stimuli was stronger in the post-stimulus time range of 150-200 ms in poor readers than in normal readers. Second, response amplitude to rapidly successive and brief stimuli that were identical or that differed significantly in frequency were substantially weaker in poor readers compared with controls, for interstimulus intervals of 100 or 200 ms, but not for an interstimulus interval of 500 ms. Third, this neurological deficit closely paralleled subjects' ability to distinguish between and to reconstruct the order of presentation of those stimulus sequences. Fourth, the average distributed response coherence evoked by rapidly successive stimuli was significantly weaker in the beta- and gamma-band frequency ranges (20-60 Hz) in poor readers, compared with controls. These results provide direct electrophysiological evidence supporting the hypothesis that reading disabilities are correlated with the abnormal neural representation of brief and rapidly successive sensory inputs, manifested in this study at the entry level of the cortical auditory/aural speech representational system(s).

Figure 1

(A) Behavioral performance at a task in which subjects had to identify and temporally order rapidly successive brief (20-ms duration) tonal stimuli that in some trials did, and in other trials did not, differ in frequency. Performance was defined during MEG recording sessions conducted for poor readers and controls (–12). The normal readers in the control group performed this task with almost no errors. Poor readers (see Methods for subject selection) made many errors, even at long (500-ms) ISIs. All poor readers performed better at longer than at shorter ISIs. (B) Examples of evoked magnetic responses recorded in the 37 channels centered on left hemisphere auditory cortex, averaged from ≈100 artifact-free presentation of stimulus-pairs at 200-ms ISI in a control subject. The timing of stimulus events is indicated in green. (C–E) Examples of rms waveforms computed across sensors at each time sample for three different control subjects, for tonal stimulus pairs presented with 200-ms ISIs. Stimulus events are indicated in green. Small vertical arrows mark the 100-ms poststimulus time (the time of occurrence of the expected evoked M100 response) for the initial and the second stimulus of the pair. (F) Example of evoked magnetic field response for a 200-ms ISI condition for a poor-reading subject. Whereas a normal-strength response was evoked by the first stimulus, the second rapidly successive stimulus evoked only a weak response. (G–I) Example rms waveforms from three poor-reading subjects.

Figure 2

Mean rms and rms-difference waveforms recorded from good-reader (thick blue lines) and poor-reader (thin red lines) subject groups. Error bars indicate jackknife error estimates of the mean across subjects at each time sample. For clarity, error bars (one-sided) are shown at every fifth time point. Stimulus events are indicated in green. Stars indicate epochs, computed over 90-ms nonoverlapping sliding time windows, that were statistically significant at P < 0.0001. (A) rms waveforms for stimulus pair with 500-ms ISIs. (B and C) rms difference waveforms for stimulus pairs with 100 (B) and 200 (C) ms ISIs. These rms differences were computed for each subject by subtracting the rms for the 500-ms ISI condition from the rms waveforms in the 100- and 200-ms ISI conditions over the first 500-ms poststimulus period. These waveforms reflect the sole contribution of the second stimulus to the response. Stars indicate the center of 90-ms-epoch windows in which differences in the responses to the second stimulus were statistically significant between poor readers vs. good readers at P < 0.0001.

Figure 3

Average transformed magnitude coherence across sensors expressed over a 750-ms period after the first stimulus of a pair in good readers (thick blue) and poor readers (thin red), at 200 ms (A) and 500 ms (B) ISIs. Mean ± one-sided jackknife errors are shown. The dashed line indicates the coherence obtained by random chance. Stars indicate the center of 5-Hz nonoverlapping sliding frequency windows in which coherence is statistically significant (for small stars P < 0.01, and large stars, P < 0.001). Significant differences were observed in β- and γ-band ranges (20–60 Hz).