Discrimination of Speech Stimuli Based on Neuronal Response Phase Patterns Depends on Acoustics But Not Comprehension

Abstract

Speech stimuli give rise to neural activity in the listener that can be observed as waveforms using magnetoencephalography. Although waveforms vary greatly from trial to trial due to activity unrelated to the stimulus, it has been demonstrated that spoken sentences can be discriminated based on theta-band (3-7 Hz) phase patterns in single-trial response waveforms. Furthermore, manipulations of the speech signal envelope and fine structure that reduced intelligibility were found to produce correlated reductions in discrimination performance, suggesting a relationship between theta-band phase patterns and speech comprehension. This study investigates the nature of this relationship, hypothesizing that theta-band phase patterns primarily reflect cortical processing of low-frequency (<40 Hz) modulations present in the acoustic signal and required for intelligibility, rather than processing exclusively related to comprehension (e.g., lexical, syntactic, semantic). Using stimuli that are quite similar to normal spoken sentences in terms of low-frequency modulation characteristics but are unintelligible (i.e., their time-inverted counterparts), we find that discrimination performance based on theta-band phase patterns is equal for both types of stimuli. Consistent with earlier findings, we also observe that whereas theta-band phase patterns differ across stimuli, power patterns do not. We use a simulation model of the single-trial response to spoken sentence stimuli to demonstrate that phase-locked responses to low-frequency modulations of the acoustic signal can account not only for the phase but also for the power results. The simulation offers insight into the interpretation of the empirical results with respect to phase-resetting and power-enhancement models of the evoked response.

A Precluding But Not Ensuring Role of Entrained Low-Frequency Oscillations for Auditory Perception

“…The optimal frequency band for quantifying auditory-driven oscillations was determined as the frequency band exhibiting strongest entrainment (phase-locking) to natural sounds. Previous work has shown that entrainment of auditory oscillations derived from EEG, MEG, or intracortical data is strongest between 2 and 9 Hz (Luo and Poeppel, 2007;Kayser et al, 2009;Howard and Poeppel, 2010;Ding and Simon, 2012;Ng et al, 2012). For our experimental setup and natural sounds, we determined the optimal band using data acquired in a previous study (Ng et al, 2012), in which we presented a series of naturalistic sounds (a subset of those used to construct the background cacophony in the present study) for a prolonged period of time (52 s).…”

“…Low-frequency rhythms in visual cortex time-lock to the presentation of video clips (Montemurro et al, 2008), and delta and theta oscillations in auditory cortex are found to entrain to the envelope of natural sounds (Luo and Poeppel, 2007;Howard and Poeppel, 2010). This auditory entrainment can be sufficiently precise and reliable that individual stimulus epochs can be reliably discriminated from oscillatory phase patterns (Luo and Poeppel, 2007;Ng et al, 2012), suggesting that it may serve as a key mechanism for segmenting auditory scenes and the integration of auditory information over time (Giraud and Poeppel, 2012;Zion Golumbic et al, 2012).…”

“…Slow delta and theta oscillations entrain to sound sequences or speech, as evidenced by studies on humans (Luo and Poeppel, 2007;Howard and Poeppel, 2010;Ng et al, 2012;Pasley et al, 2012) or animals Kayser et al, 2009). One possibility by which entrainment can arise is that slow envelope modulations prominent in many natural sounds directly imprint on periodic excitability changes in cortical networks and effectively provide an intrinsic copy of the slow stimulus dynamics (Howard and Poeppel, 2010;Ding and Simon, 2012;Zion Golumbic et al, 2012). However, it could also well be that entrainment is induced by finer-grained (e.g., spectral) features of acoustic stimuli or higher-order properties of the temporal modulation spectrum, even in the absence of clearly visible envelope modulations (Ghitza, 2011).…”

Induced activity in EEG in response to auditory stimulation

“…The auditory induced response of the brain has been studied with specific stimulus types such as perturbed and unperturbed sequences of pure tones [6,7,8,9], repeated identical words [10], targeted words in specifically designed sentences [11], and repeating modified and unmodified sentences (changing the pitch of the last word) [12,13]. For example, the gamma band is activated in response to pure-tones with temporal perturbations [6], it is also affected when subjects are presented with different types of keywords in sentences [11], and an increase in 40 Hz power has been observed in response to standard but not deviant repeating words [10].…”

“…As mentioned before, there are a limited number of studies on the brain's response to normal speech such as words and sentences [10,12,13,11,19,20,21]. In addition, not all of these studies target the induced response but rather focus on the evoked response to these stimuli.…”