Applauding with Closed Hands: Neural Signature of Action-Sentence Compatibility Effects

Abstract

BackgroundBehavioral studies have provided evidence for an action–sentence compatibility effect (ACE) that suggests a coupling of motor mechanisms and action-sentence comprehension. When both processes are concurrent, the action sentence primes the actual movement, and simultaneously, the action affects comprehension. The aim of the present study was to investigate brain markers of bidirectional impact of language comprehension and motor processes.Methodology/Principal FindingsParticipants listened to sentences describing an action that involved an open hand, a closed hand, or no manual action. Each participant was asked to press a button to indicate his/her understanding of the sentence. Each participant was assigned a hand-shape, either closed or open, which had to be used to activate the button. There were two groups (depending on the assigned hand-shape) and three categories (compatible, incompatible and neutral) defined according to the compatibility between the response and the sentence. ACEs were found in both groups. Brain markers of semantic processing exhibited an N400-like component around the Cz electrode position. This component distinguishes between compatible and incompatible, with a greater negative deflection for incompatible. Motor response elicited a motor potential (MP) and a re-afferent potential (RAP), which are both enhanced in the compatible condition.Conclusions/SignificanceThe present findings provide the first ACE cortical measurements of semantic processing and the motor response. N400-like effects suggest that incompatibility with motor processes interferes in sentence comprehension in a semantic fashion. Modulation of motor potentials (MP and RAP) revealed a multimodal semantic facilitation of the motor response. Both results provide neural evidence of an action-sentence bidirectional relationship. Our results suggest that ACE is not an epiphenomenal post-sentence comprehension process. In contrast, motor-language integration occurring during the verb onset supports a genuine and ongoing brain motor-language interaction.

Event-Related Potential Studies of Cognitive and Social Neuroscience

“…Although this component was first studied in the linguistic field, recent studies have extended previous results to richer action sequences and pictorial stimuli (sometimes called N350 or N400-like), such as congruent-incongruent pictures or videos of gestures, actions and motor events (Aravena et al, 2010;Cornejo et al, 2009;Proverbio et al, 2010;Ibañez et al, 2010bIbañez et al, , 2011Guerra et al, 2009;Sitnikova et al, 2003). Although spatial resolution provided by ERP does not allow a precise localization of N400 neural generators, evidence from lesion studies, MEG and intracranial recordings converge to implicate temporal areas (left superior/middle temporal gyrus, the anterior-medial temporal lobe, the PHC and anterior fusiform gyrus) as the possible sources of N400 (Van Petten and Luka, 2006).…”

“…The lateralized readiness potential (LRP) is a particular form of RP in response to certain movements of one side (left or right) of the body. Being related to RP, another negativity measured over Cz beginning shortly before the response onset (-90 ms) has been named the motor potential (MP) or late motor-related potential (late MRP; Aravena et al, 2010). The MP is likely to represent pyramidal neuron activity in the primary cortex (M1) at motor execution.…”

“…ERPs studies of early (N170 and ELAN) and late components (N400, LPC, LPP) have provided important insights about the temporal brain dynamics of contextual effects in language. For instance, important issues, such as automaticity of contextual effects, multimodal blending of meanings, action-sentence coupling, language-like gesture processing, language and social information coupling, and early emotional word processing have been demonstrated within ERP research (Aravena et al, 2010;Cornejo et al, 2009;Hagoort, 2008;Ibanez et al, 2006Ibanez et al, , 2009Ibanez et al, , 2010bIbanez et al, , 2010cIbanez et al, , 2011b2011c, 2011d, 2011e, Van Petten and Luka, 2006. Contextual effects in language assessed with ERPs is a relevant topic in diverse areas of neuropsychiatric research, such as schizophrenia (Guerra et al, 2009;Ibanez et al, 2011c), Alzheimer's disease and mild cognitive impairment (Schwartz et al, 2003;Taylor and Olichney, 2007), focal basal ganglia lesions (Paulmann, Pell and Kotz, 2008) alcoholism (Roopesh et al, 2009) and aphasia (Wassenaar and Hagoort, 2005), among other conditions.…”

Attention to body-parts varies with visual preference and verb–effector associations

“…English and Cantonese speakers also show slower judgments when evaluating matches between verbs and line drawings that involve the same body-effector, which has been suggested to be due to inhibitory effects from the activation of effector-specific memory circuits (Bergen et al 2010). Even an implicit relationship between the body, action, visual attention, and language is shown by a faster arm contraction than arm expansion response to hearing ''open the drawer'' (Glenberg and Kaschak 2002), by the role of context in studies of language comprehension (e.g., Barsalou 2008;Kemmerer 2015), and different response times and patterns of neural activation when action sentences and responses to them are compatible versus incompatible (Aravena et al 2010).…”

Theories and Theorizers: A Contextual Approach to Theories of Cognition

“…Cognition might be explained in many ways, including mechanical, reductionist, and physical methods, and even teleological and emergentist explanations (see for example, Barutta et al 2010a). Finally, alternative approaches (Barutta et al 2010b) to orthodox computationalism, such as connectionism (Leech et al 2008), embodied, distributed and situated cognition (Anderson 2003;Smith and Collins 2009;Dufey et al 2010), social neuroscience (Decety and Lamm 2006), the contextual approach to cognition (Aravena et al 2010;Baker and Moya 1998;Cornejo et al 2009;Hurtado et al 2009;Guerra et al 2009;Ibáñez et al 2006;Ibáñez et al 2009a, b;Ibánez et al 2010a, b, c, d;Riveros et al 2010;San Martín et al 2010), ecological cognition (Turvey 2007), and dynamical approaches (Breakspear and Stam 2005), amongst others, are increasingly well known today in cognitive science (Cosmelli and Ibanez 2008). For these reasons, it is essential for meta-theoretical analysis to be sensitive both to the components of a theory that it is most possible to formalize and to the contextual framework of that theory.…”