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      Neural Correlates of Semantic Prediction and Resolution in Sentence Processing

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          Abstract

          Most brain-imaging studies of language comprehension focus on activity following meaningful stimuli. Testing adult human participants with high-density EEG, we show that, already before the presentation of a critical word, context-induced semantic predictions are reflected by a neurophysiological index, which we therefore call the semantic readiness potential (SRP). The SRP precedes critical words if a previous sentence context constrains the upcoming semantic content (high-constraint contexts), but not in unpredictable (low-constraint) contexts. Specific semantic predictions were indexed by SRP sources within the motor system—in dorsolateral hand motor areas for expected hand-related words (e.g., “write”), but in ventral motor cortex for face-related words (“talk”). Compared with affirmative sentences, negated ones led to medial prefrontal and more widespread motor source activation, the latter being consistent with predictive semantic computation of alternatives to the negated expected concept. Predictive processing of semantic alternatives in negated sentences is further supported by a negative-going event-related potential at ∼400 ms (N400), which showed the typical enhancement to semantically incongruent sentence endings only in high-constraint affirmative contexts, but not to high-constraint negated ones. These brain dynamics reveal the interplay between semantic prediction and resolution (match vs error) processing in sentence understanding.

          SIGNIFICANCE STATEMENT Most neuroscientists agree on the eminent importance of predictive mechanisms for understanding basic as well as higher brain functions. This contrasts with a sparseness of brain measures that directly reflects specific aspects of prediction, as they are relevant in the processing of language and thought. Here we show that when critical words are strongly expected in their sentence context, a predictive brain response reflects meaning features of these anticipated symbols already before they appear. The granularity of the semantic predictions was so fine grained that the cortical sources in sensorimotor and medial prefrontal cortex even distinguished between predicted face- or hand-related action words (e.g., the words “lick” or “pick”) and between affirmative and negated sentence meanings.

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          Most cited references38

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          Semantic priming and retrieval from lexical memory: Roles of inhibitionless spreading activation and limited-capacity attention.

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            Active perception: sensorimotor circuits as a cortical basis for language.

            Action and perception are functionally linked in the brain, but a hotly debated question is whether perception and comprehension of stimuli depend on motor circuits. Brain language mechanisms are ideal for addressing this question. Neuroimaging investigations have found specific motor activations when subjects understand speech sounds, word meanings and sentence structures. Moreover, studies involving transcranial magnetic stimulation and patients with lesions affecting inferior frontal regions of the brain have shown contributions of motor circuits to the comprehension of phonemes, semantic categories and grammar. These data show that language comprehension benefits from frontocentral action systems, indicating that action and perception circuits are interdependent.
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              What is the Bereitschaftspotential?

              Since discovery of the slow negative electroencephalographic (EEG) activity preceding self-initiated movement by Kornhuber and Deecke [Kornhuber HH, Deecke L. Hirnpotentialänderungen bei Willkurbewegungen und passiven Bewegungen des Menschen: Bereitschaftspotential und reafferente Potentiale. Pflugers Archiv 1965;284:1-17], various source localization techniques in normal subjects and epicortical recording in epilepsy patients have disclosed the generator mechanisms of each identifiable component of movement-related cortical potentials (MRCPs) to some extent. The initial slow segment of BP, called 'early BP' in this article, begins about 2 s before the movement onset in the pre-supplementary motor area (pre-SMA) with no site-specificity and in the SMA proper according to the somatotopic organization, and shortly thereafter in the lateral premotor cortex bilaterally with relatively clear somatotopy. About 400 ms before the movement onset, the steeper negative slope, called 'late BP' in this article (also referred to as NS'), occurs in the contralateral primary motor cortex (M1) and lateral premotor cortex with precise somatotopy. These two phases of BP are differentially influenced by various factors, especially by complexity of the movement which enhances only the late BP. Event-related desynchronization (ERD) of beta frequency EEG band before self-initiated movements shows a different temporospatial pattern from that of the BP, suggesting different neuronal mechanisms for the two. BP has been applied for investigating pathophysiology of various movement disorders. Volitional motor inhibition or muscle relaxation is preceded by BP quite similar to that preceding voluntary muscle contraction. Since BP of typical waveforms and temporospatial pattern does not occur before organic involuntary movements, BP is used for detecting the participation of the 'voluntary motor system' in the generation of apparently involuntary movements in patients with psychogenic movement disorders. In view of Libet et al.'s report [Libet B, Gleason CA, Wright EW, Pearl DK. Time of conscious intention to act in relation to onset of cerebral activity (readiness-potential). The unconscious initiation of a freely voluntary act. Brain 1983;106:623-642] that the awareness of intention to move occurred much later than the onset of BP, the early BP might reflect, physiologically, slowly increasing cortical excitability and, behaviorally, subconscious readiness for the forthcoming movement. Whether the late BP reflects conscious preparation for intended movement or not remains to be clarified.
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                Author and article information

                Journal
                J Neurosci
                J. Neurosci
                jneuro
                jneurosci
                J. Neurosci
                The Journal of Neuroscience
                Society for Neuroscience
                0270-6474
                1529-2401
                3 May 2017
                3 May 2017
                : 37
                : 18
                : 4848-4858
                Affiliations
                [1] 1Brain Language Laboratory, Department of Philosophy and Humanities, Freie Universität Berlin, 14195 Berlin, Germany,
                [2] 2Berlin School of Mind and Brain, Humboldt Universität zu Berlin, 10099 Berlin, Germany, and
                [3] 3Einstein Center for Neurosciences, 10117 Berlin, Germany
                Author notes
                Correspondence should be addressed to either Dr. Luigi Grisoni or Dr. Friedemann Pulvermüller, Brain and Language Laboratory, Department of Philosophy and Humanities, WE4, Freie Universität Berlin, Habelschwerdter Allee 45, 14195 Berlin, Germany. grisoniluigi@ 123456zedat.fu-berlin.de or friedemann.pulvermuller@ 123456fu-berlin.de

                Author contributions: L.G., T.M.M., and F.P. designed research; L.G., T.M.M., and F.P. performed research; L.G. and F.P. analyzed data; L.G., T.M.M., and F.P. wrote the paper.

                Author information
                http://orcid.org/0000-0002-8807-165X
                http://orcid.org/0000-0003-3742-837X
                http://orcid.org/0000-0003-3210-7112
                Article
                2800-16
                10.1523/JNEUROSCI.2800-16.2017
                5426574
                28411271
                cb976dd6-61b7-4c71-9e37-f7cd5c21f22c
                Copyright © 2017 Grisoni et al.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License Creative Commons Attribution 4.0 International, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

                History
                : 6 September 2016
                : 15 March 2017
                : 17 March 2017
                Categories
                Research Articles
                Behavioral/Cognitive

                grounded cognition,semantic processing,semantic readiness potentials

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