Research ReportAction-related semantic content and negation polarity modulate motor areas during sentence reading: An event-related desynchronization study
Highlights
► A greater mu ERD was found over motor areas for action vs. abstract sentences reading. ► Mu ERD was greater and delayed for negative vs. positive action sentences. ► Mu ERD analysis is useful to detect sensorimotor changes in linguistic processing.
Introduction
The neural basis of language is a central topic of cognitive neuroscience. In particular, knowing how the brain represents words' meaning is a fascinating question mark for both philosophers and scientists.
According to classical cognitive theories, concepts are represented amodally as abstract symbols, with purely arbitrary associations between concepts, and are largely unrelated to the sensorimotor experience of the concepts that are expressed (Pylyshin, 1984, Shallice, 1988). An alternative view is proposed by the Embodied Semantic Theory (see, for example, Barsalou, 2008). According to the latter perspective, the meaning of a spoken or read word, corresponding to a concept, is represented in the brain by the same neural networks that underlie the perceptual and motor experiences that have been associated when experiencing its referent. In the case of words referring to actions, some studies have suggested a possible role of the mirror neuron system (Gallese et al., 1996, Gallese and Lakoff, 2005). Over the last two decades, neuroimaging and neurophysiological studies have provided a growing number of evidences in line with the so-called embodied or grounded cognition framework, with important implications for current views on concepts understanding (Fernandino and Iacoboni, 2010).
Although the involvement of the mirror neurons system in language processing remains highly speculative, at a macro-anatomical level the processing of action-related words has been shown to induce functional activation of the motor and premotor areas (Pulvermüller and Fadiga, 2010). Indeed, several neuroimaging studies have investigated the representation of action-related concepts in the human brain, showing activations in the left premotor cortex when subjects read or listened to verbs or sentences describing actions (Hauk et al., 2004, Tettamanti et al., 2005). These cerebral activations were reported to be effector-specific (e.g., mouth, hand, foot), following a roughly somatotopic distribution. Oliveri et al. (2004), using transcranial magnetic stimulation (TMS), reported an enhancement of the left primary motor cortex (M1) excitability for action verb processing compared to abstract verbs during a linguistic task. Contrasting results have been reported by Buccino et al. (2005) who showed a decreased corticospinal excitability of hand or foot motor cortical areas during passive listening of action sentences involving the hand or leg. Recently, Papeo et al. (2009) demonstrated an increased excitability of the left M1 during hand-action verbs reading, compared to non-action verbs. This increased excitability was absent during reading of action verbs related to other body parts. Analogous TMS-induced corticospinal effects of hand-action verbs reading were also found by Candidi et al. (2010).
Despite growing evidence suggesting that motor circuits are involved in language understanding, more information is needed in order to better understand the cerebral mechanisms responsible for such processing. Cortical activity related to sensorimotor control can be easily studied with electroencephalography (EEG) using the event-related desynchronization/ synchronization (ERD/ERS) method (Pfurtscheller and Lopes da Silva, 1999). Mu ERD, usually observed before and during self-paced voluntary movements (Pfurtscheller and Neuper, 1992, Leocani et al., 1997, Pfurtscheller et al., 2000), as well as during reaction time paradigms (Leocani et al., 2001), passive movements (Cassim et al., 2001, Alegre et al., 2004, Houdayer et al., 2011) or motor imagery (Pfurtscheller et al., 2006), reflects the cortical activation of motor and premotor areas involved in movement preparation and execution. A desynchronization is considered to reflect the activation of cortico-thalamo-cortical neuronal circuits (Steriade and Llinas, 1988, Pfurtscheller and Berghold, 1989, Neuper and Pfurtcheller, 1999). Mu ERD has also been widely used to study cortical activation during cognitive performances (Boiten et al., 1992, Klimesch et al., 1993, Dujardin et al., 1995, Stipacek et al., 2003). These authors demonstrated that the alpha power (particularly in the upper alpha band) decreases with increasingly demanding tasks (Stipacek et al., 2003). EEG power measures are highly reliable within individuals (Neuper et al., 2005), and alpha band appears to be the most sensitive indicator of differences among individuals, probably due to its higher inter-individuals variance as compared to other frequency bands (van Dis et al., 1979). As a consequence, mu ERD analyses may constitute a powerful tool to study the cerebral activity involved in action-related sentence processing.
In the present study, mu ERD analysis was used to address two questions. First, does motor cortex activation occur automatically when participants perform a sentence-reading task involving hand action verbs, even when the task does not require an explicit retrieval of the motor content? Second, does this cortical motor activation occur also during the reading of action verbs presented with sentential negation? Sentential negation is a universal syntactic feature of human language that reverses the truth value of any given sentence by using lexical morphemes such as “not”; e.g. “John has left” and “John has not left” (Klima, 1964, Laka, 1990, Haegeman, 1997, Zanuttini, 1997). Several recent psycholinguistic studies have investigated the influence of sentential negation on language processing, but the neurophysiological evidence is limited. Tettamanti et al. (2008) used fMRI to show that action-related sentences, compared to abstract ones, activated the left premotor and fronto-parietal areas involved in action representation. The same authors found a reduced BOLD signal activity for negative versus affirmative action-related sentences. Liuzza et al. (2011), applying paired-pulse TMS over the left M1 during passive reading of hand-action and abstract sentences, showed a difference in cortico-spinal excitability for positive and negative polarity hand-action sentences.
In the present study, EEG was recorded in young healthy volunteers during a sentence-reading task. Subjects were asked to read silently affirmative or negative short sentences, with hand-action or abstract content. When the sentence disappeared from the screen, subjects had to decide whether the verb contained in the sentence was represented in the Italian language with high, medium or low frequency (Fig. 1). We hypothesized that reading sentences referring to hand-action compared to abstract verbs would be associated to motor cortex involvement as measured by mu ERD. We also hypothesized that sentence polarity would modulate mu ERD, possibly leading to a lower amplitude of mu ERD during negative hand-action sentences reading.
Section snippets
Results
All the subjects could perform the task correctly. We found a significant correlation (ρ=0.87; p=0.001) between the CoLFIS lexical frequency and the perceived verb's frequency expressed by the subjects. A mu ERD was induced by the different conditions in all but one subject. This finding is coherent with the literature, reporting that not every subjects present with significant ERDs (Pfurtscheller and Lopes da Silva, 1999). Since the aim of the study was to compare mu ERD induced by the
Discussion
The main results of the present study are that hand-action related sentences reading is accompanied by a desynchronization of the mu rhythm over the left motor and pre-motor areas, and that this mu ERD is delayed and of greater amplitude during negative hand-action sentence reading. These results demonstrate that mu ERD analysis is a suitable method for studying cortical activation involved in the processing of linguistic stimuli.
Participants
Eleven right-handed native Italian speakers (7 females; mean age=21.61±2.75 years) of comparable education levels (Graduate level) participated in the experiment. All subjects had normal visual acuity. All participants reported no history of psychiatric, neurological disorders, drug abuse or current use of psychoactive medications. Subjects signed a written informed consent before participating to the study, which was approved by our local Ethics Committee and carried out in accordance with the
Acknowledgments
This work was supported by the Institute of Experimental Neurology (INSPE) of IRCCS San Raffaele Hospital, Milan and by the Vita-Salute San Raffaele University of Milan. Dr. Federica Alemanno conducted this study as partial fulfillment of her Ph.D. in Molecular Medicine, Program in Experimental Neurology, San Raffaele University, Milan, Italy. We would like to thank Dr. Pasquale Anthony Della Rosa for helpful comments on English language editing of the manuscript.
References (78)
- et al.
Alpha and beta oscillatory activity during a sequence of two movements
Clin. Neurophysiol.
(2004) - et al.
Congruent embodied representations for visually presented actions and linguistic phrases describing actions
Curr. Biol.
(2006) - et al.
Embodied semantics for actions: findings from functional brain imaging
J. Physiol. Paris
(2008) - et al.
Martin A. Parallel visual motion processing streams for manipulable objects and human movements
Neuron
(2002) - et al.
Event-related desynchronization: the effects of energetic and computational demands
Electroencephalogr. Clin. Neurophysiol.
(1992) - et al.
Listening to action-related sentences modulates the activity of the motor system: a combined TMS and behavioral study
Cogn. Brain. Res.
(2005) - et al.
The effects of semantic category and knowledge type on lexical-semantic access: a PET study
Neuroimage
(1998) - et al.
Time course of fMRI-activation in language and spatial networks during sentence comprehension
Neuroimage
(1999) - et al.
Brief and sustained movements: differences in event-related (de)synchronization (ERD/ERS) patterns
Clin. Neurophysiol.
(2000) - et al.
Event-related desynchronization (ERD) patterns during memory processes: effects of aging and task difficulty
Electroencephalogr. Clin. Neurophysiol.
(1995)
Are cortical motor maps based on body parts or coordinated actions? Implications for embodied semantics
Brain Lang.
Somatotopic representation of action words in human motor and premotor cortex
Neuron
The time course of action and action-word comprehension in the human brain as revealed by neurophysiology
J. Physiol. Paris
Reference-free identification of components of checkerboard-evoked multichannel potential fields
Electroencephalogr. Clin. Neurophysiol.
Event-related coherence and event-related desynchronization/synchronization in the 10 Hz and 20 Hz EEG during self-paced movements
Electroencephalogr. Clin. Neurophysiol.
Event-related desynchronization in reaction time paradigms: a comparison with event-related potentials and corticospinal excitability
Clin. Neurophysiol.
A critical look at the embodied cognition hypothesis and a new proposal for grounding conceptual content
J. Physiol. Paris
Electroencephalographic analysis of cortico-muscular coherence: reference effect, volume conduction and generator mechanism
Clin Neurophysiol.
Event-related beta EEG-changes during passive and attempted foot movements in paraplegic patients
Brain Res
Sensitivity of alpha band ERD to individual differences in cognition
Prog. Brain. Res.
Long-term stability and consistency of EEG event-related (de-)synchronization across different cognitive task
Clin. Neurophysiol.
ERD/ERS patterns reflecting sensorimotor activation and deactivation
Prog. Brain. Res.
Motor imagery and action observation: modulation of sensorimotor brain rhythms during mental control of a brain-computer interface
Clin. Neurophysiol.
Evaluation of event-related desynchronization (ERD) preceding and following voluntary self-paced movement
Electroencephalogr. Clin. Neurophysiol.
Patterns of cortical activation during planning of voluntary movement
Electroencephalogr. Clin. Neurophysiol.
Event-related EEG/MEG synchronization and desynchronization: basic principles
Clin. Neurophysiol.
Mu rhythm (de)synchronization and EEG single-trial classification of different motor imagery tasks
Neuroimage
Functional dissociation of lower and upper frequency mu rhythms in relation to voluntary limb movement
Clin. Neurophysiol.
Central beta rhythm during sensorimotor activities in man. Electroenceph
Clin. Neurophysiol.
Sensitivity of human EEG alpha band desynchronization to different working memory components and increasing levels of memory load
Neurosci. Lett.
Three-dimensional tomography of event-related potentials during response inhibition: evidence for phasic frontal lobe activation
Evoked Potential
Negation in the brain: modulating action representations
Neuroimage
To move or not to move: imperatives modulate action-related verb processing in the motor system
Neuroscience
Individual differences in the human electroencephalogram during quiet wakefulness
Electroencephalogr. Clin. Neurophysiol.
The functional role of motor activation in language processing: motor cortical oscillations support lexical-semantic retrieval
Neuroimage
EEG power changes during a multiple level memory retention task
Int. J. Psychophysiol.
Grounded cognition
Annu. Rev. Psychol.
Cross-talk between language processes and overt motor behavior in the first 200 ms of processing
J. Cogn. Neurosci
Hands on the future: facilitation of cortico-spinal hand-representation when reading the future tense of hand-related action verbs
Eur. J. Neurosci.
Cited by (27)
Embodiment of action-related language in the native and a late foreign language – An fMRI-study
2023, Brain and LanguageMotor resonance during linguistic processing as shown by EEG in a naturalistic VR environment
2019, Brain and CognitionCitation Excerpt :Reading single verbs related to the body caused soma topical µ ERD (von Nicolai et al., 2014). Moreover, greater µ rhythm suppression has been observed for action language compared to abstract language (Alemanno et al., 2012; Moreno et al., 2015). To examine how the acquisition of lexical items might be directly influenced by the motor system, Fargier et al. (2012) conducted a learning paradigm using EEG.
Negation markers inhibit motor routines during typing of manual action verbs
2019, CognitionCitation Excerpt :More particularly, recent evidence indicates that negation may be neurocognitively rooted in mechanisms specialized for response inhibition (Beltrán, Muñetón-Ayala & de Vega, 2018; de Vega et al., 2016; García et al., 2016; Papeo, Hochmann, & Battelli, 2016). For instance, relative to their affirmative counterparts, negative action sentences (e.g., Now you will not cut the bread) involve reduced fronto-central theta power –a robust index of brain motor inhibition (de Vega et al., 2016)–, larger amplitude of the inhibition-related N1 component (Beltrán et al., 2018), greater and delayed event-related desynchronization of the mu rhythm –another classical marker of motor simulation (Alemanno et al., 2012)–, and hypoactivation of putative motor hubs (Tettamanti et al., 2008). Compatibly, single-pulse transcranial magnetic stimulation over the left precentral gyrus increases the amplitude of motor-evoked potentials for action relative to state verbs in affirmative sentences, but no such modulation occurs in negative contexts (Papeo et al., 2016).