The Right Anterior Intraparietal Sulcus Is Critical for Bimanual Grasping: A TMS Study

Cerebral Cortex October 2014;24:2591–2603 doi:10.1093/cercor/bht115 Advance Access publication May 3, 2013 The Right Anterior Intraparietal Sulcus Is Critical for Bimanual Grasping: A TMS Study Ada Le1, Michael Vesia2,4, Xiaogang Yan2, Matthias Niemeier1,2 and J. Douglas Crawford2,3,5 1 Department of Psychology, University of Toronto Scarborough, Toronto, ON, Canada, 2Centre for Vision Research, 3Neuroscience Graduate Diploma Program, Departments Psychology, Biology, and Kinesiology and Health Sciences, York University, Toronto, ON, Canada, 4Division of Neurology and Krembil Neuroscience Centre, Toronto Western Research Institute, University of Toronto, Toronto, ON, Canada and 5Canadian Action and Perception Network, Toronto, ON, Canada Address correspondence to Dr Matthias Niemeier, Department of Psychology, University of Toronto Scarborough, 1265 Military Trail, Toronto, Ontario, Canada M1C 1A4. Email: Keywords: aIPS, bimanual, grasping, right hemisphere, transcranial magnetic stimulation Introduction Grasping an object requires that forces be applied in opposition. In many cases, these oppositional forces may arise from the digits of one hand; for example, when we use the thumb in opposition to the index finger. However, we are also capable of picking up an object, either by using the palms or the digits of 2 hands in opposition. Such bimanual grasping is actually more ubiquitous in the animal kingdom than the hand (Whishaw and Coles 1996), but its neural correlates remain poorly understood. Nevertheless, it poses some important questions about how the brain extracts visual object information to guide and coordinate the control of 2 hands (Rochat 1989; Siddiqui 1995; Tresilian and Stelmach 1997; Smeets and Brenner 2001) compared to one (Jeannerod 1981; Blake 1992; Smeets and Brenner 1999; Castiello 2005; Grafton 2010). For both unimanual and bimanual grasps, vision needs to guide the hand or hands to the specific sets of grasp points on opposite sides of the object to achieve stable grasps, especially when the minimum number of contact points is used (Lederman and Wing 2003), and of course, unimanual and bimanual grasps are governed by the same external mechanical forces (Tresilian and Stelmach 1997). Further, similar visual computations are required because stable grasp points can only be found “holistically,” in sets (e.g., Fig. 1A), so that the © The Author 2013. Published by Oxford University Press. All rights reserved. For Permissions, please e-mail: search for grasp points requires matching numerous points against many other possible points (Blake et al. 1993; Vahrenkamp et al. 2011). Given that this is computationally expensive (Blake 1992; Vahrenkamp et al. 2011), it makes sense for the visual signals required in such a search to converge in a single area or a small network of highly interconnected areas. The network that controls unimanual grasps involves areas in both inferior frontal and intraparietal cortex (for reviews see Castiello and Begliomini 2008; Grafton 2010; Davare et al. 2011). Within that network, the anterior intraparietal sulcus (aIPS) has been implicated in visually guided grasping (Binkofski et al. 1998; Culham et al. 2003; Frey et al. 2005; Tunik et al. 2005, 2008; Culham and Valyear 2006; Davare et al. 2007; Castiello and Begliomini 2008; Cohen et al. 2009; CavinaPratesi et al. 2010; Davare et al. 2010; Grafton 2010; Koch et al. 2010). It is assumed to constitute the initial step of visual analysis of grasp computations (Castiello and Begliomini 2008; Rizzolatti and Luppino 2001) and appears to integrate visual information about the grasp-relevant dimension of an object as well as other aspects, such as object size (Monaco et al. 2013). Disrupting the aIPS with transcranial magnetic stimulation (TMS) primarily impairs unimanual grasp movements in a contralateral manner: TMS of the left aIPS impairs grip formation with the right hand and vice versa (Rice et al. 2007; note, though, that Davare et al. 2007 found a left brain dominance for grip force control). Despite considerable evidence for a critical role of the aIPS in the control of unimanual grasping, it remains to be shown whether bimanual grasp movements also share similar neural correlates. In agreement with this possibility, some parietal functions appear to be effector independent with regard to different skeletomotor subsystems (Arbib 1981; Hoff and Arbib 1993; Tresilian and Stelmach 1997; Park and Shea 2002; Vangheluwe et al. 2006; Heed et al. 2011) perhaps to use neural resources efficiently (see Walsh et al. 2008). This suggests that the aIPS should be involved in unimanual grasping as well as in bimanual grasping. Furthermore, it might be computationally more efficient if the aIPS in one hemisphere was dominant to avoid costly 2-way information transfer across the corpus callosum (Braun 1992). Consistent with such hemispheric dominance, we recently found that people are faster and more accurate at grasping objects bimanually in the left visual field compared to grasping in the right visual field, which suggests a right-hemispheric dominance for bimanual grasps (Le and Niemeier 2013). This is surprising given that unimanual grasps are assumed to be left-hemisphere dominant (e.g. Gonzalez et al. 2006; Davare et al. 2007; Gonzalez and Goodale 2009; Martin et al. 2011). However, behavioral visual-field effects provide only indirect evidence for hemisphere dominance and cannot specify the Grasping with 2 limbs in opposition to one another is older than the hand, yet the neural mechanisms for bimanual grasps remain unclear. Similar to unimanual grasping, bimanual grasping may require regions in the parietal cortex that use visual object-feature information to find matching stable grasp points on the object. The localization of matching points is computationally expensive, so it might make sense for the signals to converge in a single cortical area. To examine this, we use transcranial magnetic stimulation (TMS) to probe the contribution of cortical areas known to be associated with unimanual grasping, while participants performed bimanual grasps. We applied TMS to the anterior and caudal portion of the intra-parietal sulcus (aIPS and cIPS) in each hemisphere during a size-perturbation task using the index fingers of both hands to grasp an object whose orientation might or might not change. We found significant interaction effects between TMS and perturbation of the grasp-relevant object dimension that increased grip aperture only for the right aIPS. These results indicate that the aIPS is involved not only in unimanual, but also bimanual grasping, and the right aIPS is critically involved in bimanual grasps. This suggests that information from both hemispheres converges in the right hemisphere to achieve bimanual grasps.  Figure 1. (A) Algorithms for grasp point selection (regardless of the effectors) need to search the surface of an object for any combination of 2 points to i (...truncated)