Linguistic Structure and Meaning Organize Neural Oscillations into a Content-Specific Hierarchy.

Neural oscillations track linguistic information during speech comprehension (Ding et al., 2016; Keitel et al., 2018), and are known to be modulated by acoustic landmarks and speech intelligibility (Doelling et al., 2014; Zoefel and VanRullen, 2015). However, studies investigating linguistic tracking have either relied on non-naturalistic isochronous stimuli or failed to fully control for prosody. Therefore, it is still unclear whether low-frequency activity tracks linguistic structure during natural speech, where linguistic structure does not follow such a palpable temporal pattern. Here, we measured electroencephalography (EEG) and manipulated the presence of semantic and syntactic information apart from the timescale of their occurrence, while carefully controlling for the acoustic-prosodic and lexical-semantic information in the signal. EEG was recorded while 29 adult native speakers (22 women, 7 men) listened to naturally spoken Dutch sentences, jabberwocky controls with morphemes and sentential prosody, word lists with lexical content but no phrase structure, and backward acoustically matched controls. Mutual information (MI) analysis revealed sensitivity to linguistic content: MI was highest for sentences at the phrasal (0.8-1.1 Hz) and lexical (1.9-2.8 Hz) timescales, suggesting that the delta-band is modulated by lexically driven combinatorial processing beyond prosody, and that linguistic content (i.e., structure and meaning) organizes neural oscillations beyond the timescale and rhythmicity of the stimulus. This pattern is consistent with neurophysiologically inspired models of language comprehension (Martin, 2016, 2020; Martin and Doumas, 2017) where oscillations encode endogenously generated linguistic content over and above exogenous or stimulus-driven timing and rhythm information.SIGNIFICANCE STATEMENT Biological systems like the brain encode their environment not only by reacting in a series of stimulus-driven responses, but by combining stimulus-driven information with endogenous, internally generated, inferential knowledge and meaning. Understanding language from speech is the human benchmark for this. Much research focuses on the purely stimulus-driven response, but here, we focus on the goal of language behavior: conveying structure and meaning. To that end, we use naturalistic stimuli that contrast acoustic-prosodic and lexical-semantic information to show that, during spoken language comprehension, oscillatory modulations reflect computations related to inferring structure and meaning from the acoustic signal. Our experiment provides the first evidence to date that compositional structure and meaning organize the oscillatory response, above and beyond prosodic and lexical controls.

Low-Frequency Cortical Oscillations Entrain to Subthreshold Rhythmic Auditory Stimuli.

Many environmental stimuli contain temporal regularities, a feature that can help predict forthcoming input. Phase locking (entrainment) of ongoing low-frequency neuronal oscillations to rhythmic stimuli is proposed as a potential mechanism for enhancing neuronal responses and perceptual sensitivity, by aligning high-excitability phases to events within a stimulus stream. Previous experiments show that rhythmic structure has a behavioral benefit even when the rhythm itself is below perceptual detection thresholds (ten Oever et al., 2014). It is not known whether this "inaudible" rhythmic sound stream also induces entrainment. Here we tested this hypothesis using magnetoencephalography and electrocorticography in humans to record changes in neuronal activity as subthreshold rhythmic stimuli gradually became audible. We found that significant phase locking to the rhythmic sounds preceded participants' detection of them. Moreover, no significant auditory-evoked responses accompanied this prethreshold entrainment. These auditory-evoked responses, distinguished by robust, broad-band increases in intertrial coherence, only appeared after sounds were reported as audible. Taken together with the reduced perceptual thresholds observed for rhythmic sequences, these findings support the proposition that entrainment of low-frequency oscillations serves a mechanistic role in enhancing perceptual sensitivity for temporally predictive sounds. This framework has broad implications for understanding the neural mechanisms involved in generating temporal predictions and their relevance for perception, attention, and awareness.SIGNIFICANCE STATEMENT The environment is full of rhythmically structured signals that the nervous system can exploit for information processing. Thus, it is important to understand how the brain processes such temporally structured, regular features of external stimuli. Here we report the alignment of slowly fluctuating oscillatory brain activity to external rhythmic structure before its behavioral detection. These results indicate that phase alignment is a general mechanism of the brain to process rhythmic structure and can occur without the perceptual detection of this temporal structure.