Functional Magnetic Resonance Imaging Adaptation Reveals the Cortical Networks for Processing Grasp-Relevant Object Properties

Cerebral Cortex, Jun 2014

Grasping behaviors require the selection of grasp-relevant object dimensions, independent of overall object size. Previous neuroimaging studies found that the intraparietal cortex processes object size, but it is unknown whether the graspable dimension (i.e., grasp axis between selected points on the object) or the overall size of objects triggers activation in that region. We used functional magnetic resonance imaging adaptation to investigate human brain areas involved in processing the grasp-relevant dimension of real 3-dimensional objects in grasping and viewing tasks. Trials consisted of 2 sequential stimuli in which the object's grasp-relevant dimension, its global size, or both were novel or repeated. We found that calcarine and extrastriate visual areas adapted to object size regardless of the grasp-relevant dimension during viewing tasks. In contrast, the superior parietal occipital cortex (SPOC) and lateral occipital complex of the left hemisphere adapted to the grasp-relevant dimension regardless of object size and task. Finally, the dorsal premotor cortex adapted to the grasp-relevant dimension in grasping, but not in viewing, tasks, suggesting that motor processing was complete at this stage. Taken together, our results provide a complete cortical circuit for progressive transformation of general object properties into grasp-related responses.

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Functional Magnetic Resonance Imaging Adaptation Reveals the Cortical Networks for Processing Grasp-Relevant Object Properties

Cerebral Cortex June Functional Magnetic Resonance Imaging Adaptation Reveals the Cortical Networks for Processing Grasp-Relevant Object Properties Simona Monaco 1 2 3 Ying Chen 1 2 3 W.P. Medendorp 0 2 J.D. Crawford 1 2 3 5 6 Katja Fiehler 2 4 Denise Y.P. Henriques 1 2 3 6 0 Radboud University Nijmegen, Donders Institute for Brain , Cognition and Behaviour, Nijmegen 6500HB , The Netherlands 1 Canadian Action and Perception Network (CAPnet) 2 The Author 2013. Published by Oxford University Press. All rights reserved. For Permissions , please 3 York University, Centre for Vision Research , Toronto, ON , Canada 4 University of Giessen , Experimental Psychology, Giessen , Germany 5 Department of Biology, York University , Toronto, ON , Canada 6 Departments of Psychology, Kinesiology, Health Sciences, and Neuroscience Graduate Diploma Program, York University , Toronto, ON , Canada Grasping behaviors require the selection of grasp-relevant object dimensions, independent of overall object size. Previous neuroimaging studies found that the intraparietal cortex processes object size, but it is unknown whether the graspable dimension (i.e., grasp axis between selected points on the object) or the overall size of objects triggers activation in that region. We used functional magnetic resonance imaging adaptation to investigate human brain areas involved in processing the grasp-relevant dimension of real 3-dimensional objects in grasping and viewing tasks. Trials consisted of 2 sequential stimuli in which the object's grasp-relevant dimension, its global size, or both were novel or repeated. We found that calcarine and extrastriate visual areas adapted to object size regardless of the grasp-relevant dimension during viewing tasks. In contrast, the superior parietal occipital cortex (SPOC) and lateral occipital complex of the left hemisphere adapted to the grasp-relevant dimension regardless of object size and task. Finally, the dorsal premotor cortex adapted to the grasp-relevant dimension in grasping, but not in viewing, tasks, suggesting that motor processing was complete at this stage. Taken together, our results provide a complete cortical circuit for progressive transformation of general object properties into grasp-related responses. functional magnetic resonance imaging adaptation; grasping; grasp-relevant dimension; object size Introduction The properties of an object are processed not only based on its physical appearance, like the surface and shape, but also on the possible actions that it could afford depending on our motor capabilities (Gibson 1979). For instance, if the intent is to grasp an object, then the graspable dimension becomes the most relevant property (Ganel and Goodale 2003). In fact, planning a precision grip requires the selection of the grasp axis on the object (distance between selected locations for index finger and thumb), which will determine the grip aperture. We will refer to this axis as the graspable or grasp-relevant dimension of an object. Usually, an object has several potential graspable dimensions that depend on general object properties, and that become evident after a quick initial analysis of the object. However, very little is known about the cortical mechanisms that derive the graspable dimension from more general object properties, and the degree to which these processes might be separated at the neural level is not yet understood. Both primate electrophysiology and human neuroimaging studies have implicated several cortical areas in coding object properties, like size and shape. For example, it has been shown that dorsal stream areas, such as the anterior intraparietal area (AIP), process size, and shape of objects for grasping actions (macaques: Murata et al. 2000; Asher et al. 2007; Gardner et al. 2007; humans: Cavina-Pratesi et al. 2007; Kroliczak et al. 2008; Chouinard et al. 2009; Monaco et al. 2010). In addition, an area in the superior parietal occipital cortex of humans (SPOC) and macaques (V6A) is involved in processing and coordinating several components of grasping actions (humans: Cavina-Pratesi et al. 2010; Gallivan et al. 2011, Monaco et al. 2011; macaques: Fattori et al. 2009, 2010, 2012). Other areas in the intraparietal sulcus process object size and shape during passive viewing, that is, irrespective of a pending grasping movement (macaques: Sereno and Maunsell 1998; Sereno et al. 2002; Sawamura et al. 2005; Lehky and Sereno 2007; humans: Sawamura et al. 2005; Konen and Kastner 2008; Monaco et al. 2010). Similarly, several human imaging studies have shown that the lateral occipital complex (LOC), a ventral stream area, is involved in processing object properties for grasping movements (Culham et al. 2003; Singhal et al. 2006; Monaco et al. 2010) as well as in viewing tasks (for reviews see Grill-Spector et al. 2001; Kourtzi and Connor 2011). Given the well-established involvement of the dorsal stream in object-directed actions and the ventral s (...truncated)


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Simona Monaco, Ying Chen, W.P. Medendorp, J.D. Crawford, Katja Fiehler, Denise Y.P. Henriques. Functional Magnetic Resonance Imaging Adaptation Reveals the Cortical Networks for Processing Grasp-Relevant Object Properties, Cerebral Cortex, 2014, pp. 1540-1554, 24/6, DOI: 10.1093/cercor/bht006