Applauding with Closed Hands: Neural Signature of Action-Sentence Compatibility Effects Pia Aravena1,2, Esteban Hurtado 3 , Rodrigo Riveros2, Juan Felipe Cardona1, Facundo Manes1,4, Agustı´n Iba´ n˜ ez1,2,4,5* 1 Laboratory of Experimental Psychology & Neuroscience, Institute of Cognitive Neurology (INECO), Buenos Aires, Capital Federal, Argentina, 2 Laboratory of Cognitive Neuroscience, Universidad Diego Portales, Santiago, Chile, 3 Doctoral Program, Psychology School, Pontificia Universidad Cato´ lica de Chile, Santiago, Chile, 4 Institute of Neuroscience, Favaloro University, Buenos Aires, Capital Federal, Argentina, 5 National Scientific and Technical Research Council (CONICET), Buenos Aires, Capital Federal, Argentina Abstract Background: Behavioral 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 Findings: Participants 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/Significance: The 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. Citation: Aravena P, Hurtado E, Riveros R, Cardona JF, Manes F, et al. (2010) Applauding with Closed Hands: Neural Signature of Action-Sentence Compatibility Effects. PLoS ONE 5(7): e11751. doi:10.1371/journal.pone.0011751 Editor: Paul L. Gribble, The University of Western Ontario, Canada Received March 20, 2010; Accepted June 25, 2010; Published July 28, 2010 Copyright: 2010 Aravena et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: This research was supported by CONICET (The National Scientific and Technical Research Council) and FINECO (Foundation for Research in Cognitive Neurosciences). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * E-mail: aibanez@neurologiacognitiva.org Introduction Bodily actions, such as gestures or emotional body language, are finely intertwined with language during natural speech. For example, when the president of a country is talking about the big steps on the road to consolidation, he/she is likely to automatically and without effort extend his/her hands in a big step gesture. But if the opposite gesture is performed (e.g., stretched the hands) during the same sentence, the overall meaning of the speech may appear incongruent. It appears that our brains couple motor and semantic processes together towards a specific significance. How does the brain produce such interactions? Moreover, do subtle aspects of movement, such as hand-shape in a limb action (e.g., open or closed) during language processing, also imply motor- language interactions in the brain? Our study looked for specific action-sentence compatibility effect (ACE) by examining motor and semantic processes indexed by Event Related Potentials (ERPs). Given the systematic involvement of the motor system in language processing as shown by neurophysiological and behav- ioral studies (for reviews, see, [1,2]), the coupling of neural networks between language understanding and action is no longer a matter of debate. However, the interpretation of this claim still confronts theoretical postures about the role of the motor system in language. More specifically, current research is still evaluating the sufficient and necessary implication of motor systems for language understanding opposed to debating their facilitation or coopera- tion. In addition, mutually bidirectional implications between language and motor processing are not well described. The idea that conceptual knowledge is mapped onto sensory- motor systems (see for example [3]) comes from a series of neuropsychological studies. The groundwork of this hypothesis PLoS ONE | www.plosone.org 1 July 2010 | Volume 5 | Issue 7 | e11751