Phase Entrainment of Brain Oscillations Causally Modulates Neural Responses to Intelligible Speech

Abstract

SummaryDue to their periodic nature, neural oscillations might represent an optimal “tool” for the processing of rhythmic stimulus input [1, 2, 3]. Indeed, the alignment of neural oscillations to a rhythmic stimulus, often termed phase entrainment, has been repeatedly demonstrated [4, 5, 6, 7]. Phase entrainment is central to current theories of speech processing [8, 9, 10] and has been associated with successful speech comprehension [11, 12, 13, 14, 15, 16, 17]. However, typical manipulations that reduce speech intelligibility (e.g., addition of noise and time reversal [11, 12, 14, 16, 17]) could destroy critical acoustic cues for entrainment (such as “acoustic edges” [7]). Hence, the association between phase entrainment and speech intelligibility might only be “epiphenomenal”; i.e., both decline due to the same manipulation, without any causal link between the two [18]. Here, we use transcranial alternating current stimulation (tACS [19]) to manipulate the phase lag between neural oscillations and speech rhythm while measuring neural responses to intelligible and unintelligible vocoded stimuli with sparse fMRI. We found that this manipulation significantly modulates the BOLD response to intelligible speech in the superior temporal gyrus, and the strength of BOLD modulation is correlated with a phasic modulation of performance in a behavioral task. Importantly, these findings are absent for unintelligible speech and during sham stimulation; we thus demonstrate that phase entrainment has a specific, causal influence on neural responses to intelligible speech. Our results not only provide an important step toward understanding the neural foundation of human abilities at speech comprehension but also suggest new methods for enhancing speech perception that can be explored in the future.

Entrained theta oscillations guide perception of subsequent speech: behavioural evidence from rate normalisation

“…literature on locally time-reversed, interrupted, alternated, and filtered speech; Drullman, Festen, & Plomp, 1994a;Drullman, Festen, & Plomp, 1994b;Elliott & Theunissen, 2009;Ghitza, 2012;Peelle & Davis, 2012;Saberi & Perrott, 1999;Shannon, Zeng, Kamath, Wygonski, & Ekelid, 1995;Ueda, Nakajima, Ellermeier, & Kattner, 2017). However, the functional role of this neural entrainment in speech perception remains a topic of debate: is entrainment causally involved in shaping successful speech perception (Riecke, Formisano, Sorger, Başkent, & Gaudrain, 2018;Zoefel, Archer-Boyd, & Davis, 2018) or is it merely a response-driven epiphenomenon of speech processing (Obleser, Herrmann, & Henry, 2012)? The present study will put forward psychoacoustic findings suggesting that, not only does neural entrainment to a particular syllable rate shape the decoding of concurrent speech (Experiment 1), but also that neural entrainment might persist when the entraining rhythm has ceased, influencing the perception of subsequently presented words (Experiments 2 and 3).…”

Perception of rhythmic speech is modulated by focal bilateral tACS

“…In this study, we therefore tested whether we can use tACS to modulate the success of speech perception rather than auditory scene analysis. Similar to some of the previous studies cited above (Experiment 1 in Zoefel, Archer-Boyd, et al, 2018), we systematically varied the phase relation between tACS and rhythmic speech (Fig. 1A).…”

“…Previous studies have used tACS to suggest a causal role of neural entrainment for speech processing. Combining left-lateralised tACS over auditory brain regions with functional magnetic resonance imaging (fMRI), Zoefel, Archer-Boyd, & Davis (2018) showed that the phase relation between tACS and rhythmic speech impacts the blood-oxygen level dependent (BOLD) response to intelligible but not to matched, unintelligible speech. Two other tACS studies found that bilateral neural modulation also impacts on word report for spoken sentences; Wilsch, Neuling, Obleser, & Herrmann (2018) and Riecke, Formisano, Sorger, Başkent, & Gaudrain (2018) both found that word report accuracy (a measure of speech perception success) depends on the time delay between envelope-shaped tACS stimulation and speech signals.…”

“…1A). Instead of presenting two competing speakers as in , we used rhythmic sequences of isolated words whose intelligibility was manipulated using noise-vocoding (Shannon, Zeng, Kamath, Wygonski, & Ekelid, 1995) as in the tACS-fMRI study reported by Zoefel, Archer-Boyd, et al (2018). By using intrinsic acoustic degradation (cf.…”

“…We also compared two different stimulation protocols in their efficacy of modulating speech perception (Fig. 1B): The first (Experiment 1), using standard square electrodes and unilateral stimulation over left Superior Temporal Gyrus (STG), is identical to that which was combined with fMRI by Zoefel, Archer-Boyd, et al (2018). The second (Experiment 2) consisted of bilateral stimulation over STG, using ring electrodes, shown to improve the focality of the stimulation (Datta et al, 2009;Saturnino, Antunes, & Thielscher, 2015; see also Heise et al, 2016).…”