Elsevier

Neuropsychologia

Volume 96, February 2017, Pages 222-229
Neuropsychologia

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

https://doi.org/10.1016/j.neuropsychologia.2017.01.025Get rights and content

Highlights

  • We tested the causal role of the motor cortex in language comprehension.

  • Online rTMS was used to perturb left and right M1 during semantic and lexical tasks.

  • Left M1 stimulation causally affected processing of word meaning specifically.

Abstract

Among various questions pertinent to grounding human cognitive functions in a neurobiological substrate, the association between language and motor brain structures is a particularly debated one in neuroscience and psychology. While many studies support a broadly distributed model of language and semantics grounded, among other things, in the general modality-specific systems, theories disagree as to whether motor and sensory cortex activity observed during language processing is functional or epiphenomenal. Here, we assessed the role of motor areas in linguistic processing by investigating the responses of 28 healthy volunteers to different word types in semantic and lexical decision tasks, following repetitive transcranial magnetic stimulation (rTMS) of primary motor cortex. We found that early rTMS (delivered within 200 ms of word onset) produces a left-lateralised and meaning-specific change in reaction speed, slowing down behavioural responses to action-related words, and facilitating abstract words – an effect present only during semantic, but not lexical, decision. We interpret these data in light of action-perception theory of language, bolstering the claim that motor cortical areas play a functional role in language comprehension.

Introduction

The centrality of language in mediating socio-cultural and economic interactions, as well as the devastating impact on quality of life which follows impairments of the complex language-processing system, strongly underscore the importance of studying its neurophysiological foundations. Investigations of mechanisms underpinning the comprehension of meaning (i.e., semantics), have been a focus of neuroscience, linguistics, and psychology for decades. Nevertheless, the complex details relating to where and how semantics is processed and represented in the brain remain to be fully elucidated. The traditional model, borne out of early aphasiology research, functionally locates language in a network comprised of inferior frontal and superior temporal areas of the left hemisphere, with the former in charge of speech production and grammatical processing, and the latter subserving comprehension and perception of language (Geschwind, 1970, Ojemann, 1991). However, subsequent neuroimaging studies have drawn into question this model by showing that linguistic – and in particular semantic – processing appears to be linked to activation of neural circuits outside of the “core system” including what has always been considered as modality-specific areas (such as motor, auditory, or visual cortices; see e.g., Binder and Desai (2011), Boulenger et al. (2012) and Meteyard et al. (2010)). There are two broad ways in which researchers have attempted to reconcile the classical understanding with these brain and behavioural data (Barsalou, 2008, Glenberg and Gallese, 2011). One strand argues that activity outside the left perisylvian areas is epiphenomenal to language understanding, and reflects purely correlational, downstream activity, not necessary for efficient extraction of meaning from linguistic input (Mahon and Caramazza, 2008). Others, however, have proposed that language has an additional basis in modality-specific areas, particularly sensorimotor ones, and that the functional contribution of these areas becomes readily apparent when we look at comprehension of specific semantic categories (Pulvermüller, 2011). Thus, there is presently a lack of consensus in the literature regarding the involvement of sensorimotor areas in language comprehension, highlighting the need for additional research. In particular, a distributed view of language faculty in the brain necessitates understanding whether and how activity in these areas might support comprehension of different aspects of word meaning.

The putative association between language and extra-sylvian modality-specific brain structures can be addressed by looking at the motor cortex, not least because of its distinctive neuronal activity profile and its somatotopic layout. For example, fMRI studies have shown that reading action words such as “run”, “punch” or “kiss” leads to increased blood flow to brain areas selectively controlling leg, arm and mouth movements, respectively (Hauk et al., 2004). 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 subjectʼs 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 (Hauk and Pulvermüller, 2004, Shtyrov et al., 2014; however, see a discussion of the effect timing in commentaries by Papeo and Caramazza (2014), and Shtyrov and 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). As such, this approach does not consider extra-sylvian brain areas as “peripheral” to language, but as functionally involved in encoding and subsequently representing modality-specific aspects of word meaning.

While many studies support this broadly distributed model of language and semantics, there are many others that argue that motor cortex activity observed in studies such as those above can be reconciled with classical models after all. The main argument proposed by critics of the action-perception model is that such activity may arise as a downstream by-product of language processing, and is therefore functionally “redundant” and irrelevant to the efficient meaning comprehension (Lotto et al., 2009, Mahon and Caramazza, 2008). Indeed, some theorists rightly point out that available neuroimaging results provide largely correlational, not causal evidence for sensorimotor cortices’ involvement in representing meaning. The claim of somatotopic mapping of action word semantics in the motor cortex has also been questioned. For example, Postle et al. (2008) have found increased fMRI activity in areas adjacent to motor cortex, which was correlated to generic action words, but there was no strong evidence of somatotopic organisation of this activation for words relating to effectors. The authors concluded that what is so far missing, but required, to support a motor theory of action semantics is “a demonstration that lesions to discrete motor areas have deleterious effects on the understanding of action words” (Postle et al., 2008). In conclusion, current literature contains contrasting accounts - to assess these contradictory claims and ascertain whether the motor system functionally contributes to language processing, we need experimental methodologies which allow for causal inferencing.

Transcranial magnetic stimulation (TMS) is a neurostimulation and neuromodulatory technique which allows the experimenter to directly interfere with ongoing activity in a local patch of cortical neural tissue. Depending on stimulation parameters, TMS may induce a variety of changes in cortical excitability (Walsh and Rushworth, 1998). It is generally agreed that trains of repetitive TMS (rTMS) may be delivered at a specific intensity and frequency to transiently disrupt the function of a target area, the so-called “virtual lesion” approach (Pascual-Leone et al., 2000). The non-invasiveness, reversibility, and temporal precision of TMS application make it a great tool for investigating functional interactions and changes in motor cortex during language processing.

Surprisingly, very few studies to date have directly assessed online modality-specific semantic processing in the brain using TMS. Some studies have used indirect measures, such as motor-evoked muscle potentials (MEPs) elicited by TMS during a behavioural task. For instance, Buccino et al. (2005) found that listening to action-related sentences specifically suppresses the TMS-elicited hand- and foot-muscle MEPs, while Gianelli and Dalla Volta (2015) showed that passive viewing of hand-related verbs leads to an amplitude increase in MEPs recorded from hand muscles. Papeo et al. (2014) showed that MEPs to action verbs were larger than for non-action verbs, but this difference was not significant after repetitive TMS (rTMS) to superior temporal areas, leading the authors to conclude that only the latter are “true” carriers of semantic information, cognitively mediating activity arising in motor cortices. Thus, there are conflicting experimental findings in the literature, with confusion compounded by the fact that the influence of TMS on motor cortex during verb processing was mostly assessed using MEPs, and not directly through language performance as such. Note that motor-evoked potentials merely reflect the status of the motor system and do not provide any causal evidence about a semantic role of motor cortex in comprehension: They only show that linguistic processing affects the excitability of the motor cortex, which could in principle be a downstream and a semantically shallow effect. To show the reverse, namely, that motor cortex stimulation influences language processing, one must measure direct behavioural effects of motor-system TMS on linguistic performance.

The latter was attempted in even fewer studies. In their seminal study, Pulvermüller et al. (2005) measured reaction times (RTs) in a lexical decision task (LDT) using a single pulse TMS protocol and demonstrated a somatotopy-specific improvement/facilitation in behavioural performance. Similar patterns were shown in Willems et al. (2011), who also employed a lexical decision task, and, unlike previous studies, stimulated premotor areas, rather than the primary motor cortex. While these studies show a facilitative effect of TMS stimulation on action word processing, and thus suggest some motor cortex involvement in language, they still do not provide direct evidence that sensorimotor cortical interference can disrupt semantic processing, which would be necessary to support a causal role for these areas in language comprehension. Moreover, these studies used a semantically relatively shallow task – lexical decision. While there is abundant evidence that (aspects of) meaning become activated spontaneously in a variety of language tasks (Dilkina et al., 2010, Lagrou et al., 2011, Lagrou et al., 2012, Vukovic and Williams, 2014, Yap et al., 2015), judging whether a string of letters is familiar or not per se does not require deep semantic processing, particularly not of motor semantic features – see Barsalou et al. (2008) for evidence of shallower meaning access in these and similar tasks, as well as Solomon and Barsalou (2004) and Kan et al. (2003). An approach is therefore needed, which would explicitly control for linguistic performance by using tasks requiring variable activation of semantic features, including motor ones. A TMS study which compared performance in multiple behavioural tasks was conducted by Tomasino et al. (2008), whose participants performed a silent reading task, a visual imagery task, and a frequency judgement task (how often a word appears in newspapers). The authors found that TMS did not influence performance in spontaneous linguistic processing, unlike during explicit imagery, where stimulation of hand primary-motor (M1) cortex facilitated responses. However, similarly to above, it can be argued that these experimental tasks do not explicitly require full retrieval of meaning – which is particularly true for judging how frequently a word appears in newspapers (a task which is highly unusual, and in fact led to average response latencies around 1200 ms – twice as long as is typical in language tasks; for example, see Faust (2012)).

In conclusion, although direct causal evidence for the role of motor cortex in processing of action-semantic aspects of meaning would be highly important in delineating neurobiological mechanisms of language comprehension, it is surprisingly scarce in the TMS literature. Further, to substantiate or refute the claims of sensorimotor semantics, it is essential to test whether any disruptive influence of motor cortex stimulation could occur during linguistic processing, requiring studies using an online TMS approach, as opposed to offline stimulation research (Repetto et al., 2013, Willems et al., 2011).

Section snippets

Current study

The present study was aimed at addressing the causal role of motor areas in linguistic processing, contrasting performance in concreteness judgement tasks and lexical decision tasks. As was already noted, Motor Evoked Potentials (similarly to EEG or fMRI) allow only correlational inferencing; therefore, our study directly measured behavioural outcomes, i.e., reaction times in linguistic tasks as the dependent variable. To assess effects of motor cortex stimulation on action word comprehension

Participants

We tested 28 right-handed (Oldfield, 1971) native speakers of Russian. Of those, ten were male, and eighteen female. The participants’ average age was 23.10 (SD=3.64). All participants had normal or corrected-to-normal vision, no history of neurological or language disorders, and no counter indications to TMS (Rossi et al., 2009). Prior to testing, participants gave written informed consent, and were monetarily compensated for taking part in the study. The study protocol conformed to the

Results

All participants successfully completed both tasks. The repeated measures ANOVA of error rates returned a significant main effect of Task [F(1, 27)=73.57, p<0.001, partial Eta2=0.732]: as expected, participants made fewer errors on the easier task, i.e. lexical decision, with only 3.3% incorrect responses on average, as opposed to 9.1% of the trials involving concreteness judgements. No other main effects or interactions were significant in the error-rate analysis.

After accounting for the

Discussion

We set out to test functional contributions of the primary motor cortex in language tasks which do or do not require access to action-semantic features using an MR-navigated online rTMS protocol. Analysis of the specific reaction time changes in our study revealed that early (within 200 ms) disruption of the motor cortex hand representation during word processing led to hemisphere-, task-, and meaning-specific changes in the speed of behavioural responses. Significant effects were only observed

Conclusion

In conclusion, we found evidence that an early motor cortex-TMS interference protocol produces a left-lateralised, task-, and meaning-specific change is response latencies, slowing down processing of action-related words, compared to faster abstract word responses. We interpret these data in light of the action-perception theory of language comprehension, bolstering the claim that cortical areas supporting action play a functional role in language processing. Thus, the results strongly suggest

Acknowledgements

This work was supported by Aarhus University (Denmark), Lundbeck Foundation (Denmark; NeoLex: R140-2013-12951, Project 15480), HSE Centre for Cognition and Decision Making (Moscow) and by the Russian Academic Excellence Programme5-100’.

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