Speech comprehension is correlated with temporal response patterns recorded from auditory cortex

Abstract

Speech comprehension depends on the integrity of both the spectral content and temporal envelope of the speech signal. Although neural processing underlying spectral analysis has been intensively studied, less is known about the processing of temporal information. Most of speech information conveyed by the temporal envelope is confined to frequencies below 16 Hz, frequencies that roughly match spontaneous and evoked modulation rates of primary auditory cortex neurons. To test the importance of cortical modulation rates for speech processing, we manipulated the frequency of the temporal envelope of speech sentences and tested the effect on both speech comprehension and cortical activity. Magnetoencephalographic signals from the auditory cortices of human subjects were recorded while they were performing a speech comprehension task. The test sentences used in this task were compressed in time. Speech comprehension was degraded when sentence stimuli were presented in more rapid (more compressed) forms. We found that the average comprehension level, at each compression, correlated with (i) the similarity between the frequencies of the temporal envelopes of the stimulus and the subject's cortical activity ("stimulus-cortex frequency-matching") and (ii) the phase-locking (PL) between the two temporal envelopes ("stimulus-cortex PL"). Of these two correlates, PL was significantly more indicative for single-trial success. Our results suggest that the match between the speech rate and the a priori modulation capacities of the auditory cortex is a prerequisite for comprehension. However, this is not sufficient: stimulus-cortex PL should be achieved during actual sentence presentation.

Figure 1

Compressed speech stimuli. Shown here are two sample sentences used in the experiment. Rows 1 and 3 show the spectrogram of the sentences “black cars cannot park” and “black dogs cannot bark,” respectively. Rows 2 and 4 show the corresponding temporal envelopes of these sentences. Columns correspond to compression ratios of (left to right) 0.2, 0.35, 0.5, and 0.75.

Figure 2

An example of MEG signals recorded during the task, and the measures derived from them (S MS). (A) Averaged temporal envelopes (magenta) and the first three PCs (PC1–3, blue, red, and green, respectively, scaled in proportion to their eigen values) of the averaged responses. (B) Power spectra of the stimulus envelope (magenta) and PC1 (blue). (C) Time domain cross correlation between the envelope and PC1; black, raw correlation; blue, after band-pass filtering at ±1 octave around the stimulus modal frequency.

Figure 3

Neuronal correlates for speech comprehension. A–C measures were averaged across PC1–3 (see Methods) and normalized to the maximal value of the comprehension curve; neuronal correlates with negative values were first “shifted” up by adding a constant so that their minimal value became 0. (A and B) Comprehension (black thick curve) and neuronal correlates (magenta, rms; green, Fdiff; blue, PL) for the S depicted in Fig. 2 (MS) and for another S (JW). (C) Average comprehension and neuronal correlates across all Ss (mean ± SEM, n = 13). (D) Scatter plot of thresholds for comprehension and Fdiff for all Ss. For each variable and each S, threshold was the (interpolated) compression ratio corresponding to 0.75 of the range spanned by that variable. The red line is a linear regression.

Figure 4

Correlates as a function of trial success. Each of the correlates was averaged separately over correct (blue), incorrect (red), and don't know (black) trials across all Ss. Mean ± SEM are depicted. Values (rms) are scaled by using arbitrary scaling.