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Phase-locked responses to speech in human auditory cortex are enhanced during comprehension.

Peelle JE, Gross J, Davis MH - Cereb. Cortex (2012)

Bottom Line: This enhanced phase locking was left lateralized and localized to left temporal cortex.Together, our results demonstrate that entrainment to connected speech does not only depend on acoustic characteristics, but is also affected by listeners' ability to extract linguistic information.This suggests a biological framework for speech comprehension in which acoustic and linguistic cues reciprocally aid in stimulus prediction.

View Article: PubMed Central - PubMed

Affiliation: MRC Cognition and Brain Sciences Unit, Cambridge CB2 7EF, UK.

ABSTRACT
A growing body of evidence shows that ongoing oscillations in auditory cortex modulate their phase to match the rhythm of temporally regular acoustic stimuli, increasing sensitivity to relevant environmental cues and improving detection accuracy. In the current study, we test the hypothesis that nonsensory information provided by linguistic content enhances phase-locked responses to intelligible speech in the human brain. Sixteen adults listened to meaningful sentences while we recorded neural activity using magnetoencephalography. Stimuli were processed using a noise-vocoding technique to vary intelligibility while keeping the temporal acoustic envelope consistent. We show that the acoustic envelopes of sentences contain most power between 4 and 7 Hz and that it is in this frequency band that phase locking between neural activity and envelopes is strongest. Bilateral oscillatory neural activity phase-locked to unintelligible speech, but this cerebro-acoustic phase locking was enhanced when speech was intelligible. This enhanced phase locking was left lateralized and localized to left temporal cortex. Together, our results demonstrate that entrainment to connected speech does not only depend on acoustic characteristics, but is also affected by listeners' ability to extract linguistic information. This suggests a biological framework for speech comprehension in which acoustic and linguistic cues reciprocally aid in stimulus prediction.

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Stimulus characteristics. (A) Spectrograms of a single example sentence in the 4 speech conditions, with the amplitude envelope for each frequency band overlaid. Spectral change for the 16 channel sentence is absent from the 1 channel sentence. This spectral change is created by differences between the amplitude envelopes in multichannel vocoded speech. (B) Despite differences in spectral detail, the overall amplitude envelope contains only minor differences among the 4 conditions. (C) The modulation power spectrum of sentences in each condition shows 1/f noise as expected. Shading indicates 4–7 Hz where speech signals are expected to have increased power. (D) Residual modulation power spectra for each of the 4 speech conditions: after 1/f noise is subtracted highlights the peak in modulatory power between 4 and 7 Hz. (E) Word report accuracy for sentences presented in each of the 4 speech conditions. Error bars here and elsewhere reflect standard error of the mean with between-subject variability removed (Loftus and Masson 1994).
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BHS118F1: Stimulus characteristics. (A) Spectrograms of a single example sentence in the 4 speech conditions, with the amplitude envelope for each frequency band overlaid. Spectral change for the 16 channel sentence is absent from the 1 channel sentence. This spectral change is created by differences between the amplitude envelopes in multichannel vocoded speech. (B) Despite differences in spectral detail, the overall amplitude envelope contains only minor differences among the 4 conditions. (C) The modulation power spectrum of sentences in each condition shows 1/f noise as expected. Shading indicates 4–7 Hz where speech signals are expected to have increased power. (D) Residual modulation power spectra for each of the 4 speech conditions: after 1/f noise is subtracted highlights the peak in modulatory power between 4 and 7 Hz. (E) Word report accuracy for sentences presented in each of the 4 speech conditions. Error bars here and elsewhere reflect standard error of the mean with between-subject variability removed (Loftus and Masson 1994).

Mentions: In the current study we investigate phase-locked cortical responses to slow amplitude modulations in trial-unique speech samples using magnetoencephalography (MEG). We focus on whether the phase locking of cortical responses benefits from linguistic information, or is solely a response to acoustic information in connected speech. We also use source localization methods to address outstanding questions concerning the lateralization and neural source of these phase-locked responses. To separate linguistic and acoustic processes we use a noise-vocoding manipulation that progressively reduces the spectral detail present in the speech signal but faithfully preserves the slow amplitude fluctuations responsible for speech rhythm (Shannon et al. 1995). The intelligibility of noise-vocoded speech varies systematically with the amount of spectral detail present (i.e. the number of frequency channels used in the vocoding) and can thus be adjusted to achieve markedly different levels of intelligibility (Fig. 1A). Here, we test fully intelligible speech (16 channel), moderately intelligible speech (4 channel), and 2 unintelligible control conditions (4 channel rotated and 1 channel). Critically, the overall amplitude envelope—and hence the primary acoustic signature of speech rhythm—is preserved under all conditions, even in vocoded speech that is entirely unintelligible (Fig. 1B). Thus, if neural responses depend solely on rhythmic acoustic cues, they should not differ across intelligibility conditions. However, if oscillatory activity benefits from linguistic information, phase-locked cortical activity should be enhanced when speech is intelligible.Figure 1.


Phase-locked responses to speech in human auditory cortex are enhanced during comprehension.

Peelle JE, Gross J, Davis MH - Cereb. Cortex (2012)

Stimulus characteristics. (A) Spectrograms of a single example sentence in the 4 speech conditions, with the amplitude envelope for each frequency band overlaid. Spectral change for the 16 channel sentence is absent from the 1 channel sentence. This spectral change is created by differences between the amplitude envelopes in multichannel vocoded speech. (B) Despite differences in spectral detail, the overall amplitude envelope contains only minor differences among the 4 conditions. (C) The modulation power spectrum of sentences in each condition shows 1/f noise as expected. Shading indicates 4–7 Hz where speech signals are expected to have increased power. (D) Residual modulation power spectra for each of the 4 speech conditions: after 1/f noise is subtracted highlights the peak in modulatory power between 4 and 7 Hz. (E) Word report accuracy for sentences presented in each of the 4 speech conditions. Error bars here and elsewhere reflect standard error of the mean with between-subject variability removed (Loftus and Masson 1994).
© Copyright Policy - creative-commons
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC3643716&req=5

BHS118F1: Stimulus characteristics. (A) Spectrograms of a single example sentence in the 4 speech conditions, with the amplitude envelope for each frequency band overlaid. Spectral change for the 16 channel sentence is absent from the 1 channel sentence. This spectral change is created by differences between the amplitude envelopes in multichannel vocoded speech. (B) Despite differences in spectral detail, the overall amplitude envelope contains only minor differences among the 4 conditions. (C) The modulation power spectrum of sentences in each condition shows 1/f noise as expected. Shading indicates 4–7 Hz where speech signals are expected to have increased power. (D) Residual modulation power spectra for each of the 4 speech conditions: after 1/f noise is subtracted highlights the peak in modulatory power between 4 and 7 Hz. (E) Word report accuracy for sentences presented in each of the 4 speech conditions. Error bars here and elsewhere reflect standard error of the mean with between-subject variability removed (Loftus and Masson 1994).
Mentions: In the current study we investigate phase-locked cortical responses to slow amplitude modulations in trial-unique speech samples using magnetoencephalography (MEG). We focus on whether the phase locking of cortical responses benefits from linguistic information, or is solely a response to acoustic information in connected speech. We also use source localization methods to address outstanding questions concerning the lateralization and neural source of these phase-locked responses. To separate linguistic and acoustic processes we use a noise-vocoding manipulation that progressively reduces the spectral detail present in the speech signal but faithfully preserves the slow amplitude fluctuations responsible for speech rhythm (Shannon et al. 1995). The intelligibility of noise-vocoded speech varies systematically with the amount of spectral detail present (i.e. the number of frequency channels used in the vocoding) and can thus be adjusted to achieve markedly different levels of intelligibility (Fig. 1A). Here, we test fully intelligible speech (16 channel), moderately intelligible speech (4 channel), and 2 unintelligible control conditions (4 channel rotated and 1 channel). Critically, the overall amplitude envelope—and hence the primary acoustic signature of speech rhythm—is preserved under all conditions, even in vocoded speech that is entirely unintelligible (Fig. 1B). Thus, if neural responses depend solely on rhythmic acoustic cues, they should not differ across intelligibility conditions. However, if oscillatory activity benefits from linguistic information, phase-locked cortical activity should be enhanced when speech is intelligible.Figure 1.

Bottom Line: This enhanced phase locking was left lateralized and localized to left temporal cortex.Together, our results demonstrate that entrainment to connected speech does not only depend on acoustic characteristics, but is also affected by listeners' ability to extract linguistic information.This suggests a biological framework for speech comprehension in which acoustic and linguistic cues reciprocally aid in stimulus prediction.

View Article: PubMed Central - PubMed

Affiliation: MRC Cognition and Brain Sciences Unit, Cambridge CB2 7EF, UK.

ABSTRACT
A growing body of evidence shows that ongoing oscillations in auditory cortex modulate their phase to match the rhythm of temporally regular acoustic stimuli, increasing sensitivity to relevant environmental cues and improving detection accuracy. In the current study, we test the hypothesis that nonsensory information provided by linguistic content enhances phase-locked responses to intelligible speech in the human brain. Sixteen adults listened to meaningful sentences while we recorded neural activity using magnetoencephalography. Stimuli were processed using a noise-vocoding technique to vary intelligibility while keeping the temporal acoustic envelope consistent. We show that the acoustic envelopes of sentences contain most power between 4 and 7 Hz and that it is in this frequency band that phase locking between neural activity and envelopes is strongest. Bilateral oscillatory neural activity phase-locked to unintelligible speech, but this cerebro-acoustic phase locking was enhanced when speech was intelligible. This enhanced phase locking was left lateralized and localized to left temporal cortex. Together, our results demonstrate that entrainment to connected speech does not only depend on acoustic characteristics, but is also affected by listeners' ability to extract linguistic information. This suggests a biological framework for speech comprehension in which acoustic and linguistic cues reciprocally aid in stimulus prediction.

Show MeSH
Related in: MedlinePlus