Neural correlate of the construction of sentence meaning

Abstract

The neural processes that underlie your ability to read and understand this sentence are unknown. Sentence comprehension occurs very rapidly, and can only be understood at a mechanistic level by discovering the precise sequence of underlying computational and neural events. However, we have no continuous and online neural measure of sentence processing with high spatial and temporal resolution. Here we report just such a measure: intracranial recordings from the surface of the human brain show that neural activity, indexed by γ-power, increases monotonically over the course of a sentence as people read it. This steady increase in activity is absent when people read and remember nonword-lists, despite the higher cognitive demand entailed, ruling out accounts in terms of generic attention, working memory, and cognitive load. Response increases are lower for sentence structure without meaning ("Jabberwocky" sentences) and word meaning without sentence structure (word-lists), showing that this effect is not explained by responses to syntax or word meaning alone. Instead, the full effect is found only for sentences, implicating compositional processes of sentence understanding, a striking and unique feature of human language not shared with animal communication systems. This work opens up new avenues for investigating the sequence of neural events that underlie the construction of linguistic meaning.ow does a sequence of sounds emerging from one person's mouth create a complex meaning in another person's mind? Although we have long known where language is processed in the brain (1-3), we still know almost nothing about how neural circuits extract and represent the meaning of a sentence. A powerful method for addressing this question is intracranial recording of neural activity directly from the cortical surface in neurosurgery patients (i.e., electrocorticography or ECoG) (4, 5). Although opportunities for ECoG data collection are rare, determined by clinical-not scientific-priorities, they nonetheless offer an unparalleled combination of spatial and temporal resolution, and further provide direct measures of actual neural activity, rather than indirect measures via blood flow (as in PET, fMRI, and near infrared spectroscopy/optical imaging). ECoG data are particularly valuable for the study of uniquely human functions like language, where animal models are inadequate. Here we used ECoG to identify the neural events that occur online as the meaning of a sentence is extracted and represented.Prior intracranial recording studies of language have largely focused on speech perception and production (e.g., refs. 6-11) and word-level processes (e.g., refs. 12-26). However, the most distinctive feature of human language is its compositionality: the ability to create and understand complex meanings from novel combinations of words structured into phrases and sentences (27). As a first step toward understanding the neural basis of sentence comprehension, we recorded intracranial responses while participants read sentences and...

Neurophysiological dynamics of phrase-structure building during sentence processing

“…This effect flipped for words 6-10 in TP and aSTS, where activity continued to increase in the sentence condition and became significantly higher in sentences than word lists. Those findings are congruent with a previous report of a systematic increase in intracranial high-gamma activity across successive words in sentences but not word lists (21) and suggest that working memory demands may saturate after five unrelated words.…”

“…With the high temporal resolution afforded by intracranial recordings, phrase structure indeed appears as a major determinant of the dynamic profile of brain activity in language areas. A recent study monitored high-gamma intracranial signals during sentence processing and, after averaging across a variety of sentence structures, concluded that high-gamma activity increases monotonically with the number of words in a sentence (21). The present results suggest that this is only true on average: When time-locking on the onset and offset of phrase structures, we found that this overall increase, in fact, was frequently punctuated by sudden decreases in activity that occur at phrase boundaries.…”

“…The intracranial approach to language processing has led to important advances in phonetics (19) and single-word processing (20). At the sentence level, a monotonic increase in activity, broadly distributed in the left hemisphere, was found during sentence processing (21), but its relation to sentence-internal structure-building operations remained unexplored. An entrainment of magneto-encephalographic and intracranial responses at the frequency with which phrase structures recurred in short sentences was recently reported (18).…”

Amplification of local changes along the timescale processing hierarchy

“…This hierarchy, as well as the divergence of neural responses observed here, is additionally consistent with previously proposed linguistic hierarchies: low-level regions (A1+) represent phonemes (32,33), syllables (34), and pseudowords (35), while medium-level regions (areas along A1+ to STS) represent sentences (36,37). At the top of the hierarchy, high-level regions (bilateral TPJ, precuneus, and medial prefrontal cortex) can integrate words and sentences into a meaningful, coherent whole narrative (5,15,(38)(39)(40).…”

Entropy Reduction correlates with temporal lobe activity

“…In intracranial recording, neurological patients volunteer to perform a task while electrodes, implanted in their brains for clinical reasons, continuously monitor neural activity. It offers the most direct measure possible of neural activity in humans, and as such is attractive to researchers from across many disciplines (Fedorenko et al, 2016;Martin et al, 2016;Rutishauser et al, 2006). Recordings can be made either from the cortical surface (referred to here as ECoG, short for electrocorticogram) or from beneath the cortical surface (referred to here as depth recordings).…”