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.human ͉ MEG ͉ time compression ͉ accelerated speech ͉ phase-locking C omprehension of speech depends on the integrity of its temporal envelope, that is, on the temporal variations of spectral energy. The temporal envelope contains information that is essential for the identification of phonemes, syllables, words, and sentences (1). Envelope frequencies of normal speech are usually below 8 Hz (ref. 2; see Figs. 1 and 2). The critical frequency band of the temporal envelope for normal speech comprehension is between 4 and 16 Hz (3, 4); envelope details above 16 Hz have only a small [although significant (5)] effect on comprehension. Across this low-frequency modulation range, comprehension does not usually depend on the exact frequencies of the temporal envelopes of incoming speech, because the temporal envelope of normal speech can be compressed in time down to 0.5 of its original duration before comprehension is significantly affected (6, 7). Thus, normal brain mechanisms responsible for speech perception can adapt to different input rates within this range (see refs. 8-10). This online adaptation is crucial for speech perception, because speech rates vary between different speakers and change according to the emotional state of the speaker.Poor readers, many of whom have poor successive-signal auditory (11-17) and visual (18) processing,...

Direct Recordings from the Auditory Cortex in a Cochlear Implant User

“…Representation of the temporal stimulus envelope in the cortical activity was quantified in the time domain using cross-correlation analysis (Ahissar et al 2001;Abrams et al 2008;Nourski et al 2009). Envelopes of the speech stimuli were obtained by calculating the magnitude of the Hilbert transform of the speech signal waveform and low-pass filtering at 50 Hz using a fourth-order Butterworth filter.…”

“…Previous studies in normalhearing listeners have demonstrated that time compression of speech led to decreases in intelligibility and in phase locking of the auditory cortical responses to the temporal envelopes of these sentences (Ahissar et al 2001;Ahissar and Ahissar 2005). Our previous studies have used these stimuli to establish that time locking to the speech temporal envelope could be present in core auditory cortex even when speech was severely time-compressed and, as a result, incomprehensible (compression ratio 0.20).…”

“…Phase locking of the cortical response to the stimulus envelope at different compression ratios was quantified using cross-correlation analysis (Ahissar et al 2001;Abrams et al 2008;Nourski et al 2009). Envelope following by the AEP and ERBP was measured as peaks of cross-correlograms between speech envelopes and AEPs and high-frequency ERBP envelope (70-150 Hz; see "Methods"), respectively.…”

Contrasting functional imaging parametric maps: The mislocation problem and alternative solutions

“…Procedure to generate simulated maps of coherence with a reference signal Our simulations of coherence with a reference signal were designed to tightly match real brain-speech entrainment data in which MEG signals from auditory regions of a listener are coherent with the temporal envelope of heard speech at~0.5 Hz and 4-8 Hz (Ahissar et al, 2001;Bourguignon et al, 2013a;Luo and Poeppel, 2007;Molinaro et al, 2016;Peelle et al, 2013;Vander Ghinst et al, 2016). Accordingly, we simulated coherence at 0.5 Hz between MEG data and a fixed reference signal taken as the speech envelope of a 5-min audio recording of a person reading a continuous text.…”

“…In that method, we use a bootstrap procedure (Efron, 1979) to estimate a sample distribution of coordinates of maxima in the to-be-compared conditions, and we test the null hypothesis that the distance is zero. The sensitivity and specificity of this test are evaluated on simulated data and on real brain-speech entrainment data wherein brain activity is coherent with heard speech in a natural speech listening task (Ahissar et al, 2001;Bourguignon et al, 2013a;Luo and Poeppel, 2007;Molinaro et al, 2016;Peelle et al, 2013;Vander Ghinst et al, 2016).…”