Abstract
The extent to which action and perception systems of the brain are involved in semantic comprehension remains controversial. Whether figurative language, such as metaphors and idioms, is grounded in sensory-motor systems is especially contentious. Here, we used high-definition transcranial direct current stimulation (HD-tDCS) in healthy adults to examine the role of the left-hemisphere motor cortex during the comprehension of action sentences, relative to comprehension of sentences with visual verbs. Action sentences were divided into three types: literal, metaphoric, or idiomatic. This allowed us to ask whether processing of action verbs used in figurative contexts relies on motor cortex. The results revealed that action sentence comprehension response times were facilitated relative to the visual sentence control. Significant interaction relative to visual sentences was observed for literal, metaphoric, and idiomatic action sentences with HD-tDCS of the motor cortex. These results suggest that the left motor cortex is functionally involved in action sentence comprehension. Furthermore, this involvement exists when the action content of the sentences is figurative. The results provide evidence for functional links between conceptual and action systems of the brain.
Keywords: semantics, action, tDCS, embodiment, metaphor
1. Introduction
Conceptual or semantic processing is widely distributed in the brain. Across concepts of many types, lateral and medial temporal cortex, as well as inferior parietal cortex are important for semantic processing (Binder & Desai, 2011; Binder, Desai, Graves, & Conant, 2009). One question that continues to be debated is the extent to which action and perception systems play a role in conceptual processing. Neuroimaging studies have found activation of action-perception systems for processing words or sentences that load on features related to action and perception (Desai, Binder, Conant, Mano, & Seidenberg, 2011; Desai, Binder, Conant, & Seidenberg, 2010; Fernandino, Humphries, Conant, Seidenberg, & Binder, 2016; Kiefer, et al., 2012; Martin, 2016). Clinical studies have further supported this view by showing that patients with impaired action-perception systems manifest more deficits in words with high motor content compared to low motor content (Desai, Herter, Riccardi, Rorden, & Fridriksson, 2015; Johari, et al., 2019; Riccardi, Yourganov, Rorden, Fridriksson, & Desai, 2020; Riccardi, Yourganov, Rorden, Fridriksson, & Desai, 2019). For example, in Parkinson’s disease, it has been found that action verbs (e.g., running) are more impaired than non-action verbs (e.g., thinking), and this deficit is associated with the dysfunction of the dopaminergic system and its projections to the sensorimotor system (Fernandino, et al., 2013a). This notion is further supported by studies that showed better performance for action semantics during ON vs. OFF Levodopa in Parkinson’s patients (Boulenger, et al., 2008).
Brain stimulation studies have also provided insight into functional role of action-perception systems in concept processing (Pulvermuller, Hauk, Nikulin, & Ilmoniemi, 2005). For example, transcranial magnetic stimulation (TMS) studies have found that stimulation of the primary motor cortex (M1) slows down behavioral performance for action-related words compared to abstract words (Vukovic, Feurra, Shpektor, Myachykov, & Shtyrov, 2017). Additionally, TMS disruption of M1 compromised learning of novel action verbs when motor information was critical for lexico-semantic processing (Vukovic & Shtyrov, 2019). This causal relationship between action semantics and sensorimotor systems has been further bolstered by TMS studies of sentence processing, with a recent study demonstrating that stimulation of M1 impaired the comprehension of sentences involving literal (e.g. The spike was hammered into the ground) or metaphoric action (e.g. The army was hammered in the battle) verbs (Reilly, Howerton, & Desai, 2019).
Consistent with TMS studies, transcranial direct current stimulation (tDCS) has also highlighted the role of action-perception systems in conceptual processing (Branscheidt, Hoppe, Freundlieb, Zwitserlood, & Liuzzi, 2017; Branscheidt, Hoppe, Zwitserlood, & Liuzzi, 2018). tDCS is a non-invasive method that provides causal associations between target regions of the brain and their functions. tDCS offers polarity-specific modulations without directly eliciting action potentials, representing a distinctive approach on relationship between brain and behavior (Filmer, Dux, & Mattingley, 2014). These studies have found that cathodal tDCS over motor and pre-motor cortex enhanced the learning of novel action words and accelerate response time for existing action words compared to abstract words in healthy subjects (Gijssels, Ivry, & Casasanto, 2018; Liuzzi, et al., 2010). Moreover, a recent study in post stroke aphasia found that anodal tDCS over left motor cortex improved action related word performance compared to object related words, supporting the view that action-related words are grounded in the motor system (Branscheidt, et al., 2018).
A recent innovation to the tDCS technique uses multiple electrodes in a configuration that determines the electric field orientation and current intensity on target regions (Ho, et al., 2016; Rawji, et al., 2018). As determined through modeling of the generated electric field, the stimulation provided by this High-Definition tDCS (HD-tDCS) technique is more focal than what can be achieved with traditional tDCS (Alam, Truong, Khadka, & Bikson, 2016). Moreover, it has been found that HD-tDCS stimulation can lead longer lasting effects after stimulation (more than 2 hours; Kuo et al. 2013) compared to traditional tDCS (Kuo, et al., 2013). This wider time window of post-stimulation effect offers greater opportunity to examine the variety of tasks in a single experimental session, which was more suitable for the purpose of current study. An additional advantage of tDCS is the blind nature of sham condition, in that subjects are unable to distinguish real or sham stimulation in most instances. This is usually not the case with TMS. One disadvantage of tDCS is its lower spatial resolution compared to TMS. Here, we used HD-tDCS, which provides significantly improved spatial resolution compared to traditional tDCS (DaSilva, et al., 2015; Dmochowski, Datta, Bikson, Su, & Parra, 2011; Garnett & den Ouden, 2015).
The goal of present study was to examine the functional effects of cathodal HD-tDCS over the hand area of the left-hemisphere M1 during the processing of action verbs used in sentence contexts. To our knowledge, no previous studies have examined the relationship between motor cortex and literal/figurative action verb processing in sentential contexts using HD-tDCS. We selected the hand region for stimulation because our verbs were mainly related to hand/arm actions (see Methods section). We asked whether processing sentences that used action verbs (e.g., pour, twist) would be modulated by polarization of the motor cortex. As a control for general linguistic processing and task effects not specific to action semantics, we used sentences with vision-related verbs (e.g., see, view). Differential modulation of action vs. vision sentences, relative to sham or control stimulation, would provide evidence of a functional role of motor cortex in processing action sentences. Several studies have used abstract sentences as controls. However, abstract concepts activate left inferior frontal regions (Wang, Conder, Blitzer, & Shinkareva, 2010), which are also associated with actions. We chose sentences with visual verbs as a control in order to minimize potential confounds related to either indirect action or executive processing associated with many abstract verbs.
We also asked a second question that relates to actions expressed in figurative or literal contexts, by dividing action sentences into three types: literal action (e.g., The firefighter is pouring water around the building), metaphoric (e.g., The demand always pushed the prices up), and idiomatic (e.g., The automobile industry pressed the panic button). The three types of action sentences can be thought of as representing increasing levels of abstraction. In a metaphor such as grasp a theory, an action verb is used on an abstract entity to convey an abstract concept (understanding a theory). An idiom such as grasp at straws is even more abstract, in that the entire idiom can be thought of as a single unit that is retrieved whole, without necessarily processing individual words at depth. Thus, second goal of the study was to examine whether modulatory effects of tDCS apply also to metaphoric and idiomatic action sentences, where no physical action is implied.
The question of involvement to action-related brain areas for figurative action sentences has been somewhat controversial due to inconsistent findings. Desai, Conant, Binder, Park, and Seidenberg (2013) found that a higher order action area in the anterior inferior parietal cortex was activated by literal and metaphoric action sentences, but not by action idioms that used the same verbs. This suggested that idioms are abstracted away from the action-perception system, such that an abstract meaning can be retrieved directly without grounding in the motor system. Fernandino, et al. (2013b) examined processing of the same sentence types in Parkinson’s patients, and found that both literal and idiomatic action sentences were impaired in patients relative to abstract sentences. Boulenger, Hauk, and Pulvermuller (2009) reported activation in the motor cortex in a somatotopic manner for action idioms. During reading of idioms, rapid activation of motor cortex was reported by Boulenger, Shtyrov, and Pulvermuller (2012) in a MEG study. In a TMS study, Cacciari, et al. (2011) found motor-evoked potentials (MEPs) were modulated for both metaphoric and fictive motion sentences due to TMS, but not for idiomatic motion. Reilly, et al. (2019) found that both literal and metaphoric sentences were modulated by single-pulse TMS to hand motor cortex, whereas idiomatic sentences were not examined in this study. Other fMRI studies have also reported activation for action or perception regions for processing metaphors related to action, (Aziz-Zadeh, Wilson, Rizzolatti, & Iacoboni, 2006), texture (Lacey, Stilla, & Sathian, 2012), and body parts (Lacey, et al., 2017). Overall, evidence for grounding in the motor cortex is strong for (non-idiomatic) metaphors, considering both neuroimaging and brain stimulation studies. For idioms, it is less consistent.
Here, we first test the hypothesis that HD-tDCS on motor cortex specifically modulates action-related sentences. We examined the three action sentence types individually (literal, metaphoric, idiomatic) to investigate the role of the motor cortex in processing figurative (metaphoric or idiomatic) action sentences, which may shed light on the debate above. We hypothesized that each action sentence type, relative to the visual control, will be modulated by HD-tDCS of motor cortex. We also examined action sentences as a group to test for a main effect of action verbs and explored interactions among action sentence types to test the hypothesis that figurative action sentences may differ from literal action sentences.
2. Method
2.1. Subjects
Twenty-three right-handed subjects participated in the present study (10 females; mean age 24.2, SD 3, range 18–29; mean number of years of formal education 16.3, SD 2.4, range 12–19). Two subjects were excluded due to the high and unstable impedance of electrodes during stimulation (>100kΩ), leaving 21 subjects for analysis. They had normal vision and hearing, with no reported history of neurological and psychiatric disorders nor speech language impairments. The study was approved by the University of South Carolina Institutional Review Board. Informed consent was obtained from all individual participants included in the study. Subjects were either paid or received extra credits for their participation.
2.2. Materials
The stimuli consisted of 160 sensible sentences and 60 nonsense sentences (the full list of stimuli is provided in the Supplementary Materials). For each stimulation session, we used 80 sensible and 30 nonsense sentences. The task required subjects to respond, by using one of two different response keys, whether a sentence was meaningful or nonsense. The sensible sentences contained 120 action and 40 visual sentences. The action sentences were used in two previous studies (Desai, et al., 2013; Fernandino, et al., 2013b) and contained action verbs (e.g., pinch, push, twist). The action sentences were further divided into equal groups of literal action (e.g. The firefighter is pouring water around the building), non-idiomatic metaphoric action (e.g. The demand always pushed the prices up), and idiomatic action (e.g. The automobile industry pressed the panic button). The 40 sentences in each of the action-related sentences were formed by combining a single set of action verbs associated with hand/arm actions with different noun phrases. The stimuli were constructed in triples such that the same action verb was used in three contexts. The agents denoted by the noun phrases were selected so as to direct interpretation of the verb toward either a literal or a figurative meaning. The subject of the literal action sentences was a person (e.g., The firefighter) whereas for figurative sentences, it was an entity (e.g., The automobile industry) that is unlikely to perform physical actions. This decision was made to encourage a figurative interpretation even by the time the verb is encountered. The verbs in visual sentences were all were vision-related verbs (e.g., see, view, perceive). The idiomaticity of the idiomatic sentences as well as non-idiomatic status of the metaphoric sentences was verified by an online idiom dictionary compiled from the Cambridge International Dictionary of Idioms and the Cambridge Dictionary of American Idioms (http://idioms.thefreedictionary.com). The four conditions were matched in sentence length, (number of letters, number of phonemes, number of syllables and number words) as well as response time (RT) and accuracy (Acc), according to English Lexicon Project (ELP, Balota, et al. (2007); all p>.05). Nonsense sentences were grammatically correct and used the same verbs, but were difficult to make sense of (e.g. The business is pinching the sunset). All experimental parameters (e.g., timing of trials and randomizing) were administered with Eprime (Psychology Software Tools, Pittsburgh, PA). For each subject, half of the sentences from each condition (20 for each sensible sentence type, and 30 for nonsense sentences) were used during stimulation of the targeted area, while the other half was used during sham stimulation. These halves were counterbalanced across subjects.
2.3. Procedure
Subjects received cathodal and sham stimulation over left-hemisphere hand motor cortex for 20 minutes, applied with an M×N HD-tDCS Stimulator (Soterix Medical Inc., NY, USA). The configuration of the electrodes and their corresponding current intensities are displayed in Table 1. HD-Explore™ software (Soterix Medical Inc., NY, USA) was used for optimal electrode configurations, based on current simulation. Figure 1 shows the electrode locations and anatomical position of the target area over the left-hemisphere hand motor cortex (MNI: x=−57, y=3, z=14) and the modeled pattern of current flow intensity for cathodal and sham HD-tDCS, respectively.
Table 1.
Cathodal | Sham | ||||
---|---|---|---|---|---|
| |||||
Location | Current | Field Intensity in Left Hand | Location | Current | Field Intensity in Left Hand |
| |||||
CP3 | −1.85 mA | 0.51 V/m | FC3 | +1 mA | 0.05 V/m |
Cz | +0.88 mA | FC1 | −1 mA | ||
C1 | +0.14 mA | CP1 | +1mA | ||
FC3 | +0.84mA | CP3 | −1 mA | ||
FC1 | −0.01mA |
To administer HD-tDCS, a standard 10–20 EEG cap (Easy-Cap GmbH, Germany) was placed on the subject’s head, with the Cz position midway between inion and nasion, and between the two mastoids. The control stimulation was an ‘active sham’, where stimulation was administered for the entire 20 minutes but in a montage where the current was modeled to bypass the cortex (Davis, Gold, Pascual-Leone, & Bracewell, 2013; Garnett & den Ouden, 2015; J. D. Richardson, et al., 2014) and have minimal stimulation of the target motor cortex. Four electrodes were placed in proximal pairs so that the current was flowing in and out at adjacent electrodes. To better disguise sham by having equal numbers of electrodes on the participant’s scalp across stimulation types, an additional electrode that did not administer any current was added so that five electrodes are positioned on the scalp in every condition. Particularly with high-definition multiple-electrode configurations, the sham method often used in traditional tDCS is to ramp up and then ramp down the current to induce the sensation of stimulation onset, but this may not be sufficient to fully neutralize differences in sensitivity between active and sham stimulation (J. Richardson, Datta, Dmochowski, Parra, & Fridriksson, 2015). Even though a low level of excitation/inhibition of neurons under the sham electrodes cannot be completely ruled out with an active sham used here, this was not expected to substantially affect responses to motor reaction time tasks (Ambrus, et al., 2012; Kessler, Turkeltaub, Benson, & Hamilton, 2012).
The experiment was conducted in a sound attenuated booth. Sentences were displayed on a screen in their entirety and presented in a pseudo-random order. Subjects were asked press one key on the keyboard if the sentence made sense, and another key if it did not. The order of keys was counterbalanced. Practice was given before the task. During the neurostimulation session, subjects performed a non-language distraction task (silently working on a jigsaw puzzle) and started doing the tasks immediately after the stimulation finished. The order of the stimulation sessions was counterbalanced between the subjects. Half of the subjects received cathodal stimulation in the first session following with sham stimulation in the second session. The rest of subjects received sham and cathodal stimulations in first and second sessions, respectively. Stimulation sessions were separated by at least 24 hours (range: 1 to 24 days). Subjects were not aware of the type of stimulation they were receiving in each session. Two other tasks dealing with lexical semantics were also included in the experimental session: lexical decision and semantic similarity judgment. The lexical decision task consisted of real verbs and nouns and pronounceable pseudowords presented to the participant one-at-a-time. The participant pressed one of two buttons to indicate whether the word was real or not. The semantic similarity judgment task consisted of verb or noun word triplets presented on the screen in a triangular array. The participant must indicate, via button press, which of the bottom two words was most similar in meaning to the top. For a complete description of the psycholinguistic properties of the words used in these tasks, see (Desai, et al., 2015; Riccardi, et al., 2020; Riccardi, et al., 2019). The order of the three tasks was counterbalanced across participants. Within each participant, the order of the three tasks was kept the same for both real and sham stimulation sessions. The lexical decision and semantic similarity judgment tasks measure lexical semantic processing below the sentence level and are therefore beyond the scope of the current manuscript, which focuses specifically on verb processing in sentential contexts. Each experimental session lasted around 1 hour, with 15–20 minutes being devoted to the sentence task depending on participant response speed.
2.4. Data analysis
The response time for each condition was obtained by the time difference between stimuli presentations and subjects’ response on the keyboard. For each subject, trials ± 3 SD away from the mean were considered outliers and were excluded from statistical analysis. The outlier percentages were similar across sentence and stimulation type (below 3%). All statistical analyses were performed in R (R-Core-Team, 2014).
2.4. Statistical analysis
To examine the effect of stimulation on reaction time, linear mixed effects (LME) model was used with stimulation type (cathodal vs. sham) and sentence type (literal, idiomatic, metaphoric vs. visual) as a fixed factor, and subjects as random factor1. We also adopted random intercepts and random slopes (Barr, Levy, Scheepers, & Tily, 2013). Follow up analyses were performed to compare three action sentences with visual sentences separately.
Critically, the hypotheses concern the interaction between stimulation (cathodal, sham) and sentence type (action, vision). The absolute values and main effects are not relevant to the hypotheses. Because the task involved a physical action (pressing a button), stimulation of motor cortex was expected to affect all conditions, which interacts with any effects due to sentence semantics. Changes in RTs of individual conditions due to stimulation cannot be meaningfully interpreted in terms of semantics, due to effects on the button-press action, and other general effects of tDCS. Only a stimulation x sentence type interaction can indicate whether there is a differential effect of stimulation depending on the sentence type, which can be attributed to semantics. The interactions are equivalent to computing a “net RT” (cathodalRT-shamRT) for each condition, and comparing conditions with a t-test, with the difference that directional testing is possible for t-tests (Fernandino, et al., 2013b; Howell, 2012). Finally, an LME model was used to compare response time for idiomatic and metaphoric sentences with literal sentences.
Cathodal stimulation is often thought of as ‘inhibitory’ stimulation, and 1 mA stimulation often shows inhibitory effects (Furubayashi, et al., 2008; Medeiros, et al., 2012). However, experimental findings have shown that 2 mA stimulation of the motor cortex for 20 min results in excitability enhancement rather than inhibition (Batsikadze, Moliadze, Paulus, Kuo, & Nitsche, 2013). Studies of language processing are also consistent with this finding, where cathodal stimulation at 2 mA results in facilitation or faster response times (Gijssels, et al., 2018). Facilitation with cathodal stimulation is seen even outside of motor cortex. Faster picture naming responses were observed with cathodal simulation over inferior frontal as well as inferior parietal areas (Garnett, Malyutina, Datta, & den Ouden, 2015). Hence, we used one-tailed statistics in the direction of facilitation relative to the control condition. The nonsense sentences contained a mix of verbs with majority being action related, were only used as ‘catch trials,’ and were excluded from the main statistical analysis.
3. Results
3.1. Stimulation effect action sentence compared to visual sentences
The mean and standard errors are shown in Table 2. LEM analysis revealed a 4 (sentences type)×2(stimulation) significant interaction (F(3, 2956.43) =2.87, p =0.015).
Table 2.
Sentence types | ||||||
---|---|---|---|---|---|---|
| ||||||
Group | All action | Idiomatic | Literal | Metaphoric | Visual | Nonsense |
Cathodal | 2714 ± 297 | 2697 ± 304 | 2689 ± 278 | 2754 ± 310 | 2700 ± 330 | 2790 ± 319 |
Sham | 2761 ± 287 | 2787 ± 301 | 2763 ± 284 | 2734 ± 279 | 2467 ± 231 | 2935 ± 350 |
Follow up planned comparisons with sentence type (visual vs. each action sentence type) and stimulation (sham vs. cathodal ) yielded to significant interaction (equivalent to t-tests using net RTs mentioned above) for visual vs. literal (F(1, 1538.8) = 6.9582, p <0.0001) , visual vs. idiomatic (F(1, 1416.93) = 5.80, p=0.008), and an interaction for visual vs. metaphoric (F(1, 1510.3) = 2.733, p=0.045). (Figure 2). The interaction arose from an increase in RT for the control condition, relative to a flat response or a small decrease in RT for the action sentences. Thus, compared to the baseline of visual control sentences, action sentences demonstrated relative facilitation due to simulation.
Collapsing across the action sentence types, a significant interaction was seen between action and visual sentences (F(1, 2959.72) = 7.56, p < 0.0001) . Results from nonsense sentences were not of interest and are inherently difficult to interpret. We note that because majority of the nonsense as well as sensible sentences were action related, it is not surprising that nonsense sentences also showed an effect that patterned with that of the action sentences.
3.2. Effect of stimulation on literal vs. metaphoric and idiomatic sentences
LME analysis did not reveal significant interactions between stimulation and action sentence type: literal vs. idiomatic (F(1, 1410.461) = 0.0009, p=0.46) and literal vs. metaphoric (F(1, 1510.3) = 0.94, p=0.15) sentences. This suggests similar effects of stimulation for all three action sentence types.
4. Discussion
The present study investigated the effect of HD-tDCS centered over the left-hemisphere motor cortex on sensibility judgment reaction times for action and visual sentences. We found an interaction such that HD-tDCS to motor cortex significantly facilitated performance on literal, idiomatic, and metaphoric action sentences relative to the visual control condition. No interaction between the three action sentence types was seen. These results show that modulation of the left motor cortex has an effect on sentence comprehension, and that the effect of this modulation differs depending on the action-related content of the sentences.
4.1. Action sentences compared to visual
Several investigations of action language processing have demonstrated that primary and higher-order motor cortices are activated by, and functionally involved in, the comprehension of action-related language. This evidence comes from a variety of methods, including neuroimaging (Aziz-Zadeh, et al., 2006; Desai, et al., 2013), neurostimulation (Pulvermuller, et al., 2005; Reilly, et al., 2019; Vukovic, et al., 2017), and patient studies (Desai, et al., 2015; Kemmerer, Rudrauf, Manzel, & Tranel, 2012; Riccardi, et al., 2020; Riccardi, et al., 2019). The current finding, that 2 mA cathodal M1 stimulation resulted in relative facilitation of action language processing compared to the visual condition, aligns well with facilitation effects in action language processing in both tDCS and TMS studies (Gijssels, et al., 2018; Pulvermuller, et al., 2005; Willems, Labruna, D’Esposito, Ivry, & Casasanto, 2011). Batsikadze et al. (2013) showed increased excitability for 2 mA cathodal as well as anodal tDCS over motor cortex, with increased MEP amplitudes. Increased excitability can lead to effects of stimulus/response congruence. Responding via button press for visual sentences can be thought of as an ‘incongruent’ condition, leading to relative increase in RTs compared to sham. Action sentences describing actions performed with the right hand and response via the same hand is congruent, leading to relative facilitation. In other words, motor tDCS has a general effect on task performance due to the button press, which interacts with any semantic effects, due to which changes in individual conditions cannot be meaningfully interpreted as semantic. Only condition x stimulation interactions, which account for the general effects of tDCS on task performance, can show effects of sentence semantics.
4.2. Action sentences comparisons
Both metaphoric and idiomatic sentences showed an effect of stimulation. For the metaphor condition, the results support the previously discussed evidence implicating the action-perception system in action metaphor comprehension (Cacciari, et al., 2011; Desai, et al., 2013; Reilly, et al., 2019). Regarding action idioms, previous findings have been less consistent, with some studies finding evidence of action-perception system involvement (Boulenger, et al., 2012; Fernandino, et al., 2013b) while other studies suggest that idiomatic meanings are abstracted away from action-perception systems (Cacciari, et al., 2011; Desai, et al., 2013). The present results suggest that the left M1 and surrounding motor cortex does, within the spatial resolution of HD-tDCS, have a functional link to the comprehension of action-related figurative language, even in the case of idioms. These results were found even though literal interpretations of action verbs in figurative sentences was discouraged by choosing noun phrases unlikely to produce or evoke physical actions (i.e., The company) as agents. Hence, results are unlikely due to noun-related priming of literal action simulation. Relative contribution of the hand primary motor cortex versus nearby regions in the precentral and postcentral gyri, typically associated with action schemas, cannot be distinguished given the spatial resolution of HD-tDCS.
Non-compositional models of idiom processing suggest that idioms are stored and retrieved as chunks of constructions (e.g., Gibbs, 1994a; Swinney & Cutler, 1979). This view proposes that idioms are processed as single lexical items associated with the abstract meaning. Compositional models propose that idioms are analyzed compositionally at some level, and single words can have influence on its interpretation (e.g., Cacciari & Tabossi, 1988; Hamblin & Gibbs, 1999). Hybrid models that take elements of both proposals also exist (Titone & Connine, 1999). The current results support compositional and hybrid models, by showing that action idioms are grounded in the motor system at some level and are not necessarily processed as abstract lexical items.
While no interaction was observed between different action conditions, the numerical magnitude of effects for metaphors was somewhat weaker compared to literal and idiomatic sentences. We speculate that this may reflect some contribution from the right hemisphere in metaphor comprehension. Neuroimaging and behavioral evidence suggests that, compared to literal language or highly conventionalized metaphors, the right hemisphere is preferentially involved processing novel metaphors, especially in sentential contexts (Lai, van Dam, Conant, Binder, & Desai, 2015; Mashal & Faust, 2008, 2009; Yang, 2014). Even though metaphors used in this study were not designed to be novel or creative, a tentative suggestion is that increased involvement of the right hemisphere when processing metaphoric sentences may explain the numerically weaker effect of left M1 stimulation for action metaphors.
An ongoing controversy in figurative language comprehension has been between direct access models (Gibbs, 1994b; Glucksberg, 2008) and indirect access models (Janus & Bever, 1985; Searle, 1979). These models assume that there are two distinct meanings – a literal meaning and an abstract/figurative meaning – associated with metaphors. Direct access models state that the figurative meaning can be accessed directly without intervening access to the literal meaning. Indirect access models claim that the literal meaning is accessed first, followed by the abstract meaning. We dispute this underlying assumption of two distinct meanings. The figurative and supposedly abstract meaning can in fact be based in the literal sense, blurring the binary distinction between the literal and the metaphoric. As proposed by Reilly, et al. (2019), it is possible that action verbs, even when used figuratively, possess a motor component that is: (1) partially grounded in action-perception systems of the brain and (2) accessed somewhat automatically. Such a view is also consistent with the Underspecification Model of figurative language (Frisson & Pickering, 2001). This model argues that, during comprehension, a single and underspecified meaning of a word is activated, which is later refined. We suggest that in the case of action verbs, this underspecified meaning includes the word’s motor components, among other attributes. The underspecified meaning is then ‘honed’ through context, leading to eventual comprehension of the metaphor.
Future studies can examine the role of the right-hemisphere motor cortex during figurative and literal action sentence comprehension. Evidence suggests that right-hemisphere action-perception areas can support action-related semantic processing via connectivity to left-hemisphere areas following disruption of the left-hemisphere (Riccardi, et al., 2020; Riccardi, et al., 2019), raising the possibility that right-hemisphere areas could compensate for the effects of left-hemisphere stimulation alone. The question of laterality is also especially relevant for figurative language comprehension, as there is an ongoing debate regarding the specialization of the right-hemisphere for figurative language (Bohrn, Altmann, & Jacobs, 2012; Kasparian, 2013; Rapp, Mutschler, & Erb, 2012). tDCS provides a unique opportunity for future investigations to stimulate a single hemisphere, or both hemispheres simultaneously, allowing for an in-depth investigation of laterality effects in language processing.
4.4. Conclusion
The present study investigated the effect of HD-tDCS over the left-hemisphere motor cortex on sensibility judgement reaction times for action and visual sentences. Action sentences as a whole were affected differentially by stimulation, suggesting a functional role of motor cortex in their processing. Metaphoric and idiomatic action sentences were also affected selectively by this stimulation relative to control sentences. This suggests that the functional link between action language and motor cortex is maintained for figurative use.
Supplementary Material
HD-tDCS applied to left motor cortex while subjects read action sentences
Action sentences showed relative facilitation with stimulation
This facilitation was also seen for metaphoric and idiomatic action
Functional role of motor cortex in action language processing
Acknowledgments
This research was supported by NIH/NIDCD grants R01 DC010783, R56DC010783, and R01DC017162 (RD).
Footnotes
Authors contributions
KJ and NR equally contributed to this work. RD designed the study. SM and NR collected the data. MM, KJ, and SM analyzed the data. KJ, NR and RD wrote the paper. All authors read and confirmed the final version of the paper.
. RT ~ Sentence type + Stimulation + Sentence type *Stimulation + (1 + Stimulation|Subject)
Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
References
- Alam M, Truong DQ, Khadka N, & Bikson M. (2016). Spatial and polarity precision of concentric high-definition transcranial direct current stimulation (HD-tDCS). Phys Med Biol, 61, 4506–4521. [DOI] [PubMed] [Google Scholar]
- Ambrus GG, Al-Moyed H, Chaieb L, Sarp L, Antal A, & Paulus W. (2012). The fade-in-short stimulation--fade out approach to sham tDCS--reliable at 1 mA for naive and experienced subjects, but not investigators. Brain Stimul, 5, 499–504. [DOI] [PubMed] [Google Scholar]
- Aziz-Zadeh L, Wilson SM, Rizzolatti G, & Iacoboni M. (2006). Congruent embodied representations for visually presented actions and linguistic phrases describing actions. Curr Biol, 16, 1818–1823. [DOI] [PubMed] [Google Scholar]
- Balota DA, Yap MJ, Cortese MJ, Hutchison KA, Kessler B, Loftis B, Neely JH, Nelson DL, Simpson GB, & Treiman R. (2007). The English Lexicon Project. Behav Res Methods, 39, 445–459. [DOI] [PubMed] [Google Scholar]
- Barr DJ, Levy R, Scheepers C, & Tily HJ (2013). Random effects structure for confirmatory hypothesis testing: Keep it maximal. J Mem Lang, 68. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Batsikadze G, Moliadze V, Paulus W, Kuo MF, & Nitsche MA (2013). Partially non-linear stimulation intensity-dependent effects of direct current stimulation on motor cortex excitability in humans. J Physiol, 591, 1987–2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Binder JR, & Desai RH (2011). The neurobiology of semantic memory. Trends Cogn Sci, 15, 527–536. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Binder JR, Desai RH, Graves WW, & Conant LL (2009). Where is the semantic system? A critical review and meta-analysis of 120 functional neuroimaging studies. Cereb Cortex, 19, 2767–2796. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bohrn IC, Altmann U, & Jacobs AM (2012). Looking at the brains behind figurative language--a quantitative meta-analysis of neuroimaging studies on metaphor, idiom, and irony processing. Neuropsychologia, 50, 2669–2683. [DOI] [PubMed] [Google Scholar]
- Boulenger V, Hauk O, & Pulvermuller F. (2009). Grasping ideas with the motor system: semantic somatotopy in idiom comprehension. Cereb Cortex, 19, 1905–1914. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Boulenger V, Mechtouff L, Thobois S, Broussolle E, Jeannerod M, & Nazir T. (2008). Word processing in Parkinson’s disease is impaired for action verbs but not for concrete nouns. Neuropsychologia, 46, 743–756. [DOI] [PubMed] [Google Scholar]
- Boulenger V, Shtyrov Y, & Pulvermuller F. (2012). When do you grasp the idea? MEG evidence for instantaneous idiom understanding. NeuroImage, 59, 3502–3513. [DOI] [PubMed] [Google Scholar]
- Branscheidt M, Hoppe J, Freundlieb N, Zwitserlood P, & Liuzzi G. (2017). tDCS Over the Motor Cortex Shows Differential Effects on Action and Object Words in Associative Word Learning in Healthy Aging. Front Aging Neurosci, 9, 137. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Branscheidt M, Hoppe J, Zwitserlood P, & Liuzzi G. (2018). tDCS over the motor cortex improves lexical retrieval of action words in poststroke aphasia. J Neurophysiol, 119, 621–630. [DOI] [PubMed] [Google Scholar]
- Cacciari C, Bolognini N, Senna I, Pellicciari MC, Miniussi C, & Papagno C. (2011). Literal, fictive and metaphorical motion sentences preserve the motion component of the verb: a TMS study. Brain Lang, 119, 149–157. [DOI] [PubMed] [Google Scholar]
- Cacciari C, & Tabossi P. (1988). The comprehension of idioms. Journal of Memory and Language, 27, 668–683. [Google Scholar]
- DaSilva AF, Truong DQ, DosSantos MF, Toback RL, Datta A, & Bikson M. (2015). State-of-art neuroanatomical target analysis of high-definition and conventional tDCS montages used for migraine and pain control. Front Neuroanat, 9, 89. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Davis NJ, Gold E, Pascual-Leone A, & Bracewell RM (2013). Challenges of proper placebo control for non-invasive brain stimulation in clinical and experimental applications. Eur J Neurosci, 38, 2973–2977. [DOI] [PubMed] [Google Scholar]
- Desai RH, Binder JR, Conant LL, Mano QR, & Seidenberg MS (2011). The neural career of sensory-motor metaphors. J Cogn Neurosci, 23, 2376–2386. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Desai RH, Binder JR, Conant LL, & Seidenberg MS (2010). Activation of sensory-motor areas in sentence comprehension. Cereb Cortex, 20, 468–478. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Desai RH, Conant LL, Binder JR, Park H, & Seidenberg MS (2013). A piece of the action: modulation of sensory-motor regions by action idioms and metaphors. NeuroImage, 83, 862–869. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Desai RH, Herter T, Riccardi N, Rorden C, & Fridriksson J. (2015). Concepts within reach: Action performance predicts action language processing in stroke. Neuropsychologia, 71, 217–224. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dmochowski JP, Datta A, Bikson M, Su Y, & Parra LC (2011). Optimized multi-electrode stimulation increases focality and intensity at target. J Neural Eng, 8, 046011. [DOI] [PubMed] [Google Scholar]
- Fernandino L, Conant LL, Binder JR, Blindauer K, Hiner B, Spangler K, & Desai RH (2013a). Parkinson’s disease disrupts both automatic and controlled processing of action verbs. Brain Lang, 127, 65–74. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fernandino L, Conant LL, Binder JR, Blindauer K, Hiner B, Spangler K, & Desai RH (2013b). Where is the action? Action sentence processing in Parkinson’s disease. Neuropsychologia, 51, 1510–1517. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fernandino L, Humphries CJ, Conant LL, Seidenberg MS, & Binder JR (2016). Heteromodal Cortical Areas Encode Sensory-Motor Features of Word Meaning. J Neurosci, 36, 9763–9769. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Filmer HL, Dux PE, & Mattingley JB (2014). Applications of transcranial direct current stimulation for understanding brain function. Trends Neurosci, 37, 742–753. [DOI] [PubMed] [Google Scholar]
- Frisson S, & Pickering MJ (2001). Obtaining a Figurative Interpretation of a Word: Support for Underspecification. Metaphor and Symbol, 16, 149–171. [Google Scholar]
- Furubayashi T, Terao Y, Arai N, Okabe S, Mochizuki H, Hanajima R, Hamada M, Yugeta A, Inomata-Terada S, & Ugawa Y. (2008). Short and long duration transcranial direct current stimulation (tDCS) over the human hand motor area. Exp Brain Res, 185, 279–286. [DOI] [PubMed] [Google Scholar]
- Garnett EO, & den Ouden DB (2015). Validating a Sham Condition for Use in High Definition Transcranial Direct Current Stimulation. Brain Stimul, 8, 551–554. [DOI] [PubMed] [Google Scholar]
- Garnett EO, Malyutina S, Datta A, & den Ouden DB (2015). On the Use of the Terms Anodal and Cathodal in High-Definition Transcranial Direct Current Stimulation: A Technical Note. Neuromodulation, 18, 705–713. [DOI] [PubMed] [Google Scholar]
- Gibbs R. (1994a). The poetics of mind : figurative thought, language, and understanding. Cambridge [England] ; New York, NY, USA: Cambridge University Press. [Google Scholar]
- Gibbs R. (1994b). The Poetics of Mind: Figurative Thought, Language, and Understanding. Cambridge, UK: Cambridge University Press. [Google Scholar]
- Gijssels T, Ivry RB, & Casasanto D. (2018). tDCS to premotor cortex changes action verb understanding: Complementary effects of inhibitory and excitatory stimulation. Sci Rep, 8, 11452. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Glucksberg S. (2008). How metphors create categories-quickly. In Gibbs J, Raymond W (Ed.), The cambridge handbook of metaphor and thought (pp. 109–128). New York, NY: Cambridge University Press. [Google Scholar]
- Hamblin JL, & Gibbs RW Jr. (1999). Why you can’t kick the bucket as you slowly die: Verbs in idiom comprehension. Journal of Psycholinguistic Research, 28, 25–39. [Google Scholar]
- Ho KA, Taylor JL, Chew T, Galvez V, Alonzo A, Bai S, Dokos S, & Loo CK (2016). The Effect of Transcranial Direct Current Stimulation (tDCS) Electrode Size and Current Intensity on Motor Cortical Excitability: Evidence From Single and Repeated Sessions. Brain Stimul, 9, 1–7. [DOI] [PubMed] [Google Scholar]
- Howell DC (2012). Statistical methods for psychology (8 ed.): Wadsworth Publishing Company. [Google Scholar]
- Janus RA, & Bever TG (1985). Processing of Metaphoric Language - an Investigation of the 3-Stage Model of Metaphor Comprehension. Journal of Psycholinguistic Research, 14, 473–487. [Google Scholar]
- Johari K, Walenski M, Reifegerste J, Ashrafi F, Behroozmand R, Daemi M, & Ullman MT (2019). A dissociation between syntactic and lexical processing in Parkinson’s disease. Journal of Neurolinguistics, 51, 221–235. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kasparian K. (2013). Hemispheric differences in figurative language processing: Contributions of neuroimaging methods and challenges in reconciling current empirical findings. Journal of Neurolinguistics, 26, 1–21. [Google Scholar]
- Kemmerer D, Rudrauf D, Manzel K, & Tranel D. (2012). Behavioral patterns and lesion sites associated with impaired processing of lexical and conceptual knowledge of actions. Cortex, 48, 826–848. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kessler SK, Turkeltaub PE, Benson JG, & Hamilton RH (2012). Differences in the experience of active and sham transcranial direct current stimulation. Brain Stimul, 5, 155–162. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kiefer M, Trumpp N, Herrnberger B, Sim E-J, Hoenig K, & Pulvermüller F. (2012). Dissociating the representation of action- and sound-related concepts in middle temporal cortex. Brain and Language, 122, 120–125. [DOI] [PubMed] [Google Scholar]
- Kuo HI, Bikson M, Datta A, Minhas P, Paulus W, Kuo MF, & Nitsche MA (2013). Comparing cortical plasticity induced by conventional and high-definition 4 × 1 ring tDCS: a neurophysiological study. Brain Stimul, 6, 644–648. [DOI] [PubMed] [Google Scholar]
- Lacey S, Stilla R, Deshpande G, Zhao S, Stephens C, McCormick K, Kemmerer D, & Sathian K. (2017). Engagement of the left extrastriate body area during body-part metaphor comprehension. Brain Lang, 166, 1–18. [DOI] [PubMed] [Google Scholar]
- Lacey S, Stilla R, & Sathian K. (2012). Metaphorically feeling: comprehending textural metaphors activates somatosensory cortex. Brain Lang, 120, 416–421. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lai VT, van Dam W, Conant LL, Binder JR, & Desai RH (2015). Familiarity differentially affects right hemisphere contributions to processing metaphors and literals. Front Hum Neurosci, 9, 44. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Liuzzi G, Freundlieb N, Ridder V, Hoppe J, Heise K, Zimerman M, Dobel C, Enriquez-Geppert S, Gerloff C, Zwitserlood P, & Hummel FC (2010). The involvement of the left motor cortex in learning of a novel action word lexicon. Curr Biol, 20, 17451751. [DOI] [PubMed] [Google Scholar]
- Martin A. (2016). GRAPES-Grounding representations in action, perception, and emotion systems: How object properties and categories are represented in the human brain. Psychon Bull Rev, 23, 979–990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mashal N, & Faust M. (2008). Right hemisphere sensitivity to novel metaphoric relations: application of the signal detection theory. Brain Lang, 104, 103–112. [DOI] [PubMed] [Google Scholar]
- Mashal N, & Faust M. (2009). Conventionalisation of novel metaphors: a shift in hemispheric asymmetry. Laterality, 14, 573–589. [DOI] [PubMed] [Google Scholar]
- Medeiros LF, de Souza IC, Vidor LP, de Souza A, Deitos A, Volz MS, Fregni F, Caumo W, & Torres IL (2012). Neurobiological effects of transcranial direct current stimulation: a review. Front Psychiatry, 3, 110. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pulvermuller F, Hauk O, Nikulin VV, & Ilmoniemi RJ (2005). Functional links between motor and language systems. Eur J Neurosci, 21, 793–797. [DOI] [PubMed] [Google Scholar]
- R-Core-Team. (2014). R: A language and environment for statistical computing. In. Vienna, Austria: R Foundation for Statistical Computing. [Google Scholar]
- Rapp AM, Mutschler DE, & Erb M. (2012). Where in the brain is nonliteral language? A coordinate-based meta-analysis of functional magnetic resonance imaging studies. NeuroImage, 63, 600–610. [DOI] [PubMed] [Google Scholar]
- Rawji V, Ciocca M, Zacharia A, Soares D, Truong D, Bikson M, Rothwell J, & Bestmann S. (2018). tDCS changes in motor excitability are specific to orientation of current flow. Brain Stimul, 11, 289–298. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Reilly M, Howerton O, & Desai RH (2019). Time-Course of Motor Involvement in Literal and Metaphoric Action Sentence Processing: A TMS Study. Front Psychol, 10, 371. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Riccardi N, Yourganov G, Rorden C, Fridriksson J, & Desai R. (2020). Degradation of Praxis Brain Networks and Impaired Comprehension of Manipulable Nouns in Stroke. J Cogn Neurosci, 32, 467–483. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Riccardi N, Yourganov G, Rorden C, Fridriksson J, & Desai RH (2019). Dissociating action and abstract verb comprehension post-stroke. Cortex, 120, 131–146. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Richardson J, Datta A, Dmochowski J, Parra LC, & Fridriksson J. (2015). Feasibility of using high-definition transcranial direct current stimulation (HD-tDCS) to enhance treatment outcomes in persons with aphasia. NeuroRehabilitation, 36, 115–126. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Richardson JD, Fillmore P, Datta A, Truong D, Bikson M, & Fridriksson J. (2014). Toward Development of Sham Protocols for High-Definition Transcranial Direct Current Stimulation (HD-tDCS). NeuroRegulation, 1, 62–72. [Google Scholar]
- Searle J. (1979). Metaphor. In Ortony A (Ed.), Metaphor and Thought: Cambridge University Press. [Google Scholar]
- Swinney D, & Cutler A. (1979). The access and processing of idiomatic expressions. Journal of Verbal Learning and Verbal Behavior, 18, 523–534. [Google Scholar]
- Titone DA, & Connine CM (1999). On the compositional and noncompositional nature of idiomatic expressions. Journal of Pragmatics, 31, 1655–1674. [Google Scholar]
- Vukovic N, Feurra M, Shpektor A, Myachykov A, & Shtyrov Y. (2017). Primary motor cortex functionally contributes to language comprehension: An online rTMS study. Neuropsychologia, 96, 222–229. [DOI] [PubMed] [Google Scholar]
- Vukovic N, & Shtyrov Y. (2019). Learning with the wave of the hand: Kinematic and TMS evidence of primary motor cortex role in category-specific encoding of word meaning. NeuroImage, 202, 116179. [DOI] [PubMed] [Google Scholar]
- Wang J, Conder JA, Blitzer DN, & Shinkareva SV (2010). Neural representation of abstract and concrete concepts: a meta-analysis of neuroimaging studies. Hum Brain Mapp, 31, 1459–1468. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Willems RM, Labruna L, D’Esposito M, Ivry R, & Casasanto D. (2011). A functional role for the motor system in language understanding: evidence from theta-burst transcranial magnetic stimulation. Psychol Sci, 22, 849–854. [DOI] [PubMed] [Google Scholar]
- Yang J. (2014). The role of the right hemisphere in metaphor comprehension: a meta-analysis of functional magnetic resonance imaging studies. Hum Brain Mapp, 35, 107–122. [DOI] [PMC free article] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.