Inter- and Intrahemispheric Dissociations in Ideomotor Apraxia: A Large-Scale Lesion–Symptom Mapping Study in Subacute Brain-Damaged Patients

Cerebral Cortex December 2013;23:2781–2789 doi:10.1093/cercor/bhs280 Advance Access publication September 17, 2012 FEATURE ARTICLE Inter- and Intrahemispheric Dissociations in Ideomotor Apraxia: A Large-Scale Lesion–Symptom Mapping Study in Subacute Brain-Damaged Patients Aurelie L. Manuel1, Narges Radman2, Delphine Mesot1, Leila Chouiter2, Stephanie Clarke1, Jean-Marie Annoni2 and Lucas Spierer1,2 1 Department of Clinical Neurosciences, Neuropsychology and Neurorehabilitation Service, Vaudois University Hospital Center and University of Lausanne, 1011 Lausanne, Switzerland and 2Department of Medicine, Neurology Unit, University of Fribourg, 1700 Fribourg, Switzerland Pantomimes of object use require accurate representations of movements and a selection of the most task-relevant gestures. Prominent models of praxis, corroborated by functional neuroimaging studies, predict a critical role for left parietal cortices in pantomime and advance that these areas store representations of tool use. In contrast, lesion data points to the involvement of left inferior frontal areas, suggesting that defective selection of movement features is the cause of pantomime errors. We conducted a large-scale voxelbased lesion–symptom mapping analyses with configural/spatial (CS) and body-part-as-object (BPO) pantomime errors of 150 left and right brain-damaged patients. Our results confirm the left hemisphere dominance in pantomime. Both types of error were associated with damage to left inferior frontal regions in tumor and stroke patients. While CS pantomime errors were associated with left temporoparietal lesions in both stroke and tumor patients, these errors appeared less associated with parietal areas in stroke than in tumor patients and less associated with temporal in tumor than stroke patients. BPO errors were associated with left inferior frontal lesions in both tumor and stroke patients. Collectively, our results reveal a left intrahemispheric dissociation for various aspects of pantomime, but with an unspecific role for inferior frontal regions. Keywords: frontal, ideomotor apraxia, lesion, pantomime, parietal, voxel-based lesion–symptom mapping Introduction Pantomime of object or tool use is the act of pretending to use an object by adopting the same limb configurations and producing the same sequences of movements as if the object were actually held and used. Pantomime of object or tool use is the act of pretending to use an object by adopting the same limb configurations and producing the same sequences of movements as if the object were actually held and used. Within the model of praxis by Rothi et al. (1991, 1997), pantomime to verbal command is distinguished from other types of motor productions based on the fact that it neither requires a visual analysis of the gesture to be produced nor a comparison between the visual input with a lexicon of action (as would be the case for, e.g., imitation of new or familiar gestures). Rather, the analysis of the auditory/verbal command is directly followed by the selection of the spatiotemporal attributes of the gesture to be performed from an action output lexicon and the programming and implementation of the motor action (see also Peigneux and Van der Linden 2000). Because the production of pantomimes involve semantic, executive, and spatial/configural level of motor processing © The Author 2012. Published by Oxford University Press. All rights reserved. For Permissions, please e-mail: (to respectively understand the gestures, select the relevant movements representing the action, and represent accurately the relationships between the body parts involved in the movement and of how they interact with the object (Goldenberg 2009)), pantomime constitutes a sensitive task to detect ideomotor apraxia following a brain lesion (Heilman and Rothi 1993). In the current article, we refer to “ideomotor apraxia” using the definition proposed by Rothi et al. (1991, 1997): “an impairment in the timing, sequencing, and spatial organization of gestural movements” (Rothi et al. 1991). Starting from the seminal hypotheses of Liepmann (1908) in stroke patients, most prominent models of praxia advance that left parietal areas store the motor representations of tool use guiding action and therefore predict that these structures play a central role in pantomime (Moll et al. 2000; Peigneux et al. 2004). Functional neuroimaging studies corroborate these models by consistently observing correlations between left parietal areas activity and pantomiming (Vingerhoets, Acke et al. 2012, Vingerhoets, Vandekerckhove et al. 2011; see Lewis (2006) for a meta-analysis of activation studies). In contrast, lesion studies report that accurate pantomime depends on the integrity of left inferior frontal areas (Goldenberg et al. 2007) and less consistently of parietal areas (Kertesz and Ferro 1984; Goldenberg and Hagmann 1997; Peigneux et al. 2000). Although not directly for pantomimes, parietal areas have been involved in ideomotor apraxia (Basso et al. 1985; Haaland et al. 2000; Buxbaum et al. 2007) or coordination of arm movements in ideomotor apraxia (Mutha et al. 2010). Therefore, lesion studies conclude that pantomime critically depends on the selection of a limited, task-relevant set of features among the many features involved in the actual tool use to be mimed (Goldenberg et al. 2007; Goldenberg 2009; Bohlhalter et al. 2011). The disparity between the findings of neuroimaging and lesion approaches about the involvement of parietal regions has been hypothesized to follow from the pantomimes being realized under different conditions in each type of study. Because of the constraints induced by the scanner on participant’s movements, the pantomimes require additional spatial transformations of movements to unusual reference frames, which in turn increase the involvement of parietal structures (Andersen et al., 1997; Goldenberg et al., 2007). Rumiati et al. (2004), however, reported an involvement of left parietal areas for the pantomiming of visually presented objects in patients with deficit in the organization of sequences relative to tool use (ideational apraxia), suggesting that these structures might trigger tool use-related motor programs. Pantomime are Address correspondence to Aurelie Manuel, Faculty of Biology and Medicine–UNIL, Neuropsychology and Neurorehabilitation Service–CHUV, av. Pierre-Decker 5 1011, Lausanne, Switzerland. Email: 2782 Neural correlates of pantomime • Manuel et al. (VLSM; Bates et al. 2003) on a group of subacute, unselected, hemispheric brain-damaged patients and pantomime scores differentiating the typical spatial/configural (CS) and BPO pantomime error types. We used highly selective inferential statistical analyses of lesion–symptom mapping based on continuous scores rather than descriptive comparisons between lesion patterns of patients’ groups defined by behavioral cutoffs (i.e., with or without apraxia). Because the inclusion (...truncated)