Perturbing the Action Observation Network During Perception and Categorization of Actions

Cerebral Cortex March 2015;25:598–608 doi:10.1093/cercor/bht242 Advance Access publication October 1, 2013 Perturbing the Action Observation Network During Perception and Categorization of Actions’ Goals and Grips: State-Dependency and Virtual Lesion TMS Effects Pierre O. Jacquet1,2 and Alessio Avenanti1,3,4 1 Department of Psychology, Alma Mater Studiorum, University of Bologna, 40127 Bologna, Italy, 2INSERM U1028, CNRS UMR5292, Lyon Neuroscience Research Center, 69676 Bron cedex, France, 3Centro studi e ricerche in Neuroscienze Cognitive, Campus di Cesena, University of Bologna, 47521 Cesena, Italy and 4Istituto di Ricovero e Cura a Carattere Scientifico Fondazione Santa Lucia, 00179 Roma, Italy Address correspondence to Alessio Avenanti, Centro studi e ricerche in Neuroscienze Cognitive, Campus di Cesena, Università di Bologna. Viale Europa 980, 47521 Cesena, Italy. Email: ; or to Pierre O. Jacquet, Université Paris-Descartes, Sorbonne Paris Cité, Laboratoire Psychologie de la Perception CNRS UMR8158, 75006 Paris, France. Email: Keywords: action observation network, action perception, somatosensory cortex, state dependency, transcranial magnetic stimulation, virtual lesion Introduction Observing another individual manipulating an object (e.g., a wine bottle) with the aim of achieving a specific purpose may involve the processing of low- and high-level components of the observed motor behavior, namely the specific grip used to grasp the object (e.g., power or precision grip) and the end-goal achieved via object manipulation (e.g., pouring a glass or placing the bottle in the ice bucket). It has been suggested that the ability to perceive and understand others’ actions depends on resonance mechanisms that map observed motor acts onto one’s own action representations (Rizzolatti and Craighero 2004; Wilson and Knoblich 2005; Keysers et al. 2010; Urgesi et al. 2010; Avenanti and Urgesi 2011; Kilner 2011; Borgomaneri et al. 2012) and are implemented in a widespread cortical network, usually referred to as the action observation network (AON). Classically, the inferior frontal cortex (IFC, including the ventral premotor cortex and the posterior part of the inferior frontal gyrus) and the anterior intraparietal cortex (AIP) have been considered important nodes of the © The Author 2013. Published by Oxford University Press. All rights reserved. For Permissions, please e-mail: AON, mediating action perception through motor simulation (di Pellegrino et al. 1992; Gallese et al. 1996; Fogassi et al. 2005; Chong et al. 2008; Etzel et al. 2008; Kilner et al. 2009; Oosterhof et al. 2010). In addition, mounting evidence suggests that the somatosensory cortices may also be involved in perceiving and internally simulating others’ behavioral states (Keysers et al. 2004; Bufalari et al. 2007; Ebisch et al. 2008; Valeriani et al. 2008; Avenanti et al. 2009; Aziz-Zadeh et al. 2012; Gazzola et al. 2012). In particular, the primary somatosensory cortex (S1) is consistently active during action perception and execution (Avikainen et al. 2002; Rossi et al. 2002; Costantini et al. 2005; Avenanti et al. 2007; Gazzola and Keysers 2009; Turella et al. 2012) and may thus be considered an additional sensorimotor node of the AON (Keysers et al. 2010). One unresolved issue is whether, and how, low- and highlevel components of actions—namely the type of hand grip and end-goals—are differentially represented in sensorimotor regions of the AON and what is the respective contribution of such regions to action perception. Imaging and neurophysiological studies have suggested that the IFC is involved in processing both low- and high-level components of seen actions, whereas parietal nodes of the AON may be more involved in processing high-level components (e.g., end-goals) (Iacoboni et al. 2005; Hamilton and Grafton 2006, 2008; Grafton and Hamilton 2007; Lestou et al. 2008; Grafton 2009; Majdandzic et al. 2009; Bonini et al. 2010, 2012; Urgesi et al. 2010). However, as AIP and S1 are often co-activated (Keysers et al. 2010), it is unclear whether these 2 regions play any differential role in action perception. Moreover, although several studies using imaging and neurophysiological techniques have suggested activation of IFC, AIP, and S1 during observation of others’ actions (Caspers et al. 2010; Molenberghs et al. 2012), it should be noted that these techniques provide correlational evidence and cannot establish a direct causal link between brain and function (Silvanto and Pascual-Leone 2012). The precise aim of the present study is to test the causal influences of IFC, AIP, and S1 in the perception of different action components. To test the hypothesis that IFC has a major role in processing grips and end-goals while parietal regions would be mainly devoted to processing goals, we used transcranial magnetic stimulation-adaptation (TMS-A). The TMS-A paradigm is based on the well-established notion of “state-dependency”, i.e. that TMS effects depend on the context and the initial state of the stimulated neurons (Lang et al. 2004; Siebner et al. 2004, 2009; Bestmann et al. 2010). Specifically, TMS is thought to differentially modulate neurons that are Watching others grasping and using objects activates an action observation network (AON), including inferior frontal (IFC), anterior intraparietal (AIP), and somatosensory cortices (S1). Yet, causal evidence of the differential involvement of such AON sensorimotor nodes in representing high- and low-level action components (i.e., end-goals and grip type) is meager. To address this issue, we used transcranial magnetic stimulation-adaptation (TMS-A) during 2 novel action perception tasks. Participants were shown adapting movies displaying a demonstrator performing goal-directed actions with a tool, using either power or precision grips. They were then asked to match the end-goal (Goal-recognition task) or the grip (Grip-recognition task) of actions shown in test pictures to the adapting movies. TMS was administered over IFC, AIP, or S1 during presentation of test pictures. Virtual lesion-like effects were found in the Grip-recognition task where IFC stimulation induced a general performance decrease, suggesting a critical role of IFC in perceiving grips. In the Goal-recognition task, IFC and S1 stimulation differently affected the processing of “adapted” and “nonadapted” goals. These “state-dependent” effects suggest that the overall goal of seen actions is encoded into functionally distinct and spatially overlapping neural populations in IFC–S1 and such encoding is critical for recognizing and understanding end-goals. power vs. precision grip) were manipulated, in such a way that either end-goal could be achieved with either grip ( presenting a “many-to-one” mapping problem). In addition, subjects had to perform 2 tasks. In the “Goal-recognition task,” participants had to provide similarity judgments on the end-goal of the action, independently of the ty (...truncated)