Automatic ultrarapid activation and inhibition of cortical motor systems in spoken word comprehension

Abstract

To address the hotly debated question of motor system involvement in language comprehension, we recorded neuromagnetic responses elicited in the human brain by unattended actionrelated spoken verbs and nouns and scrutinized their timecourse and neuroanatomical substrates. We found that already very early on, from ∼80 ms after disambiguation point when the words could be identified from the available acoustic information, both verbs and nouns produced characteristic somatotopic activations in the motor strip, with words related to different body parts activating the corresponding body representations. Strikingly, along with this category-specific activation, we observed suppression of motorcortex activation by competitor words with incompatible semantics, documenting operation of the neurophysiological principles of lateral/surround inhibition in neural word processing. The extremely early onset of these activations and deactivations, their emergence in the absence of attention, and their similar presence for words of different lexical classes strongly suggest automatic involvement of motor-specific circuits in the perception of actionrelated language.embodied cognition | lexical semantics | magnetoencephalography | MEG | mismatch negativity T he old debate on localization of cognitive functions in the brain was recently reinvigorated with the advent of a concept of mirror neurons and a closely related framework of grounded cognition (1-8). The mirror neuron theory stemmed from a seminal discovery of neurons that activate equally when a specific action is performed by the tested individual or when observing the same action performed by others, giving a strong neurophysiological proof for the concept of comprehension and learning through simulation (for a review, see ref. 1). This is enabled by the presence of perception-action circuits in the brain that can provide motor areas with multimodal sensory information (2). An array of findings in mirror neuron and related research strongly suggest that the motor system is not merely a "slave" or an "output" of any central processing, but that it also takes an active role in perception and comprehension of external events. In cognitive science, which had suggested the emergence of concepts from individual experiences long before these neurophysiological discoveries (3-5), a similar strand of research led to a more general framework of "grounding" (or "embodiment") of cognitive functions and representations in bodily sensations and actions, which was supported through a range of behavioral and neurophysiological experiments (6-8).Nowhere these approaches resonated more than in the neuroscience of language. Following breakthrough neurological studies of the 19th century (9, 10), the human language function was for many decades confined to a small set of cortical areas in the left hemisphere. More recent research, however, challenged these views in favor of linguistic representations distributed over a range of brain areas, which span beyond the core language cortices of B...

Are the motor features of verb meanings represented in the precentral motor cortices? Yes, but within the context of a flexible, multilevel architecture for conceptual knowledge

“…Furthermore, in an electrophysiological study that involved subliminal presentation of verbs for arm/hand actions, Boulenger et al (2008b) found that the stimuli modulated the readiness potential (an index of motor preparation) associated with subsequent reaching movements, and also influenced the kinematics of those movements. In addition, several investigations have employed magnetoencephalography to demonstrate that action verbs engage body-part-congruent precentral motor areas with remarkable speed, in some cases as soon as 100 ms after the words can be uniquely identified (Shtyrov et al, 2014; see also Pulvermüller et al, 2005b;Moseley et al, 2013;Klepp et al, 2014; for a critique see Papeo & Caramazza, 2014). Taken together, these findings show that action verbs can trigger somatotopic frontal activity in an apparently automatic manner, without the need for deep semantic processing.…”

Primary motor cortex functionally contributes to language comprehension: An online rTMS study

“…Moreover, electrophysiological (electro-and magnetoencephalography, EEG/MEG) studies demonstrate that this motor activity increases extremely fast: For instance, the rholandic mu rhythm in the alpha and lower beta range, a characteristic signature of the motor system status, desynchronises within 200 ms from seeing action words in the subject's first and even second language (Vukovic and Shtyrov 2014), and motor-related evoked EEG/MEG responses dissociate between semantic categories within 80-200 ms after the visual onset or spoken word recognition point Shtyrov et al 2014; however, see a discussion of the effect timing in commentaries by Stroganova 2015). These and similar findings provide support to an "action-perception" model of language, which posits that comprehension consists of partial re-activation of networks formed and used during immersed, real-world learning and experience, and grounds word meaning in distributed cortical circuits comprised (in addition to core language areas) of the same perceptual and motor structures that support action and perception (Barsalou 2010).…”

What can autism teach us about the role of sensorimotor systems in higher cognition? New clues from studies on language, action semantics, and abstract emotional concept processing

“…With a particular focus on action cognition, empirical neuroscience has demonstrated that sounds, spoken and written words with action-related meaning produce somatotopic semantic activation of the human motor system (in particular motor and premotor cortex) across multiple experimental contexts (Aziz-Zadeh & Damasio, 2008;Grisoni, Dreyer, & Pulvermü ller, 2016;Grisoni, McCormick-Miller, & Pulvermü ller, 2017;Hauk, Johnsrude, & Pulvermü ller, 2004;Hauk, Shtyrov, & Pulvermü ller, 2008;Kana, Blum, Ladden, & Ver Hoef, 2012;Pulvermü ller, Shtyrov, & Ilmoniemi, 2005;Shtyrov, Butorina, Nikolaeva, & Stroganova, 2014;Shtyrov, Hauk, & Pulvermü ller, 2004;Tettamanti et al, 2005). Neural control of movement includes a cascade of cortical areas (primary motor, premotor and supplementary motor cortex, located in precentral gyrus and adjacent sulci [BA 4 and BA 6]) and subcortical regions (such as the striatum and the putamen) along with the cerebellum, most of which have been seen to be activated by words with action affordances .…”

“…First, although task conditions may suppress it, motor system activation whilst processing action-related stimuli is manifest even if participants do not actively attend to language input (Grisoni et al, 2016;Moseley, Pulvermü ller, & Shtyrov, 2013;Pulvermü ller, Shtyrov, et al, 2005;Shtyrov et al, 2004Shtyrov et al, , 2014Trumpp, Traub, & Kiefer, 2013;Trumpp, Traub, Pulvermü ller, & Kiefer, 2014). Second, motor activation during processing of action language is flexible, following the pattern expected for semantic mechanisms (for discussion, see .…”

“…These findings are consistent with full ignition of frontotemporal circuits for words in control participants, but partial failure of ignition in ASC, specifically in the frontal and motor components of these circuits. Note again that much neuroimaging and neuropsychological work suggests that in TD participants, the frontotemporal (including motor) areas activate even if participants perceive meaningful language passively (e.g., D'Ausilio et al, 2009;Shtyrov et al, 2004Shtyrov et al, , 2014Wilson, Saygin, Sereno, & Iacoboni, 2004).…”