Zones of bimanual and unimanual preference within human primary sensorimotor cortex during object manipulation

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Abstract

We asked which brain areas are engaged in the coordination of our hands in dexterous object manipulations where they cooperate for achieving a common goal. Well-trained right-handers steered a cursor on a screen to hit successively displayed targets by applying isometric forces and torques to a rigid tool. In two bimanual conditions, the object was held freely in the air and the hands thus generated coupled opposing forces. Yet, depending on the mapping rule linking hand forces and cursor movements, all subjects selected either the left or the right hand as prime actor. In two unimanual conditions, the subjects performed the same task with either the left or the right hand operating on a fixed tool. Functional magnetic resonance imaging revealed common activation across all four conditions in a dorsal fronto-parietal network biased to the left hemisphere and in bilateral occipitotemporal cortex. Contrary to the notion that medial wall premotor areas are especially active in complex bimanual actions, their activation depended on acting hand (left, right) rather than on grip type (bimanual, unimanual). We observed effects of grip type only in the primary sensorimotor cortex (SMC). In particular, with either hand as prime actor, bimanual actions preferentially activated subregions of the SMC contralateral to the acting hand. A sizeable subregion with preference for unimanual activity was found only in the left SMC in our right-handed subjects. Collectively, these results indicate a hemispheric asymmetry for the SMC and that partially different neural populations support the control of bimanual versus unimanual object manipulations.

Introduction

Most previous researches on cerebral control of bimanual actions have addressed situations where the two hands simultaneously perform independent tasks, typically involving finger tapping or other gestures (see Swinnen, 2002, Wiesendanger and Serrien, 2004 for reviews). Mesial wall premotor areas (supplementary and cingulate motor areas) together with lateral premotor areas, parietal cortex and cerebellum typically show higher or more extensive activation during bimanual as compared to unimanual movements (Goerres et al., 1998, Jäncke et al., 1998, Tracy et al., 2001, Toyokura et al., 2002, Nair et al., 2003, Debaere et al., 2004). Furthermore, these brain regions tend to be more engaged during asymmetric or out-of-phase bimanual movements than in mirror-symmetric or in-phase movements (Sadato et al., 1997, Goerres et al., 1998, Stephan et al., 1999a, Stephan et al., 1999b, Toyokura et al., 1999, Immisch et al., 2001, Serrien et al., 2001, Meyer-Lindenberg et al., 2002, Ullén et al., 2003, Debaere et al., 2004, Wenderoth et al., 2005). Given that the hands have greater difficulties acting independently under asymmetric gestures (Swinnen, 2002), this increase in brain activity is thought to reflect an ‘additional coordination effort’ required to overcome difficulties in interhemispheric spatiotemporal integration (Debaere et al., 2004, Wenderoth et al., 2005). Natural object-oriented bimanual activities, however, run apparently effortlessly although they commonly involve coordinated action patterns with complex mixtures of mirror-symmetric and asymmetric components. In such activities, the two hands are functionally bound together in time and space for attaining a common goal, such as when opening bottles and jars, buttoning a shirt and playing a violin. Thus, rather than simultaneously performing separate tasks, the hands play complementary roles where one in each instance serves as prime actor while the other has a stabilizing or assisting function (Guiard, 1987, MacNeilage, 1987, Viallet et al., 1992, Johansson et al., 2006).

To learn about neural mechanisms that support bimanual coordination during object manipulations, we used functional magnetic resonance imaging (fMRI) to compare brain activity while well-trained right-handers completed the same task under comparable bimanual and unimanual conditions. In the bimanual conditions, the subjects applied longitudinal and twist forces to a tool held freely between the hands to control a cursor for hitting targets on a computer screen. Based on converging evidence from correlations between applied forces and tool movements, neurophysiological (electromyography, transcranial magnetic brain stimulation) and fMRI data, we have previously demonstrated that the brain in such situations flexibly assigns as prime actor the hand (left or right) whose forces are directionally most spatially congruent with the movement goal (Johansson et al., 2006). The accompanying hand, bound to generate forces directed opposite to the goal motion, is assigned an assisting, or postural, role. By applying different mapping rules between hand forces and cursor movements, we created two bimanual conditions where either the left or the right hand functioned as prime actor. In both condition, the two hands generated complex combinations of coordinated mirror-symmetric and anti-symmetric actions. In the unimanual conditions, the tool was fixated and the subjects performed the same task by applying forces by either the left or the right hand. The forces generated by a single hand were virtually identical to those applied by the same hand in the bimanual conditions. In a factorial analysis, we examined the effect of grip type (unimanual, bimanual) and acting hand (left, right) on blood oxygen level-dependent (BOLD) signals recorded from the whole brain as well as possible interaction effects between these factors. Our results, based on object manipulation, challenge the generality of the notion that tasks requiring complex coordinated bimanual actions employ more neural resources than used when the corresponding action components are performed unimanually. For premotor areas, our results suggest that their engagement rather depends on primarily acting hand (left or right) than on whether a task is performed unimanually or bimanually. Finally, we submit that the control of bimanual and unimanual object manipulations use partially different hand representations in the primary sensorimotor cortex.

Section snippets

Materials and methods

The present results are based on the same brain scanning experiment as reported on in a previous study that concerned hand assignments in the bimanual conditions (Johansson et al., 2006).

Results

We present the results in three main sections. First, we address the subjects’ behavior in the fMRI scanner. Second, based on the factorial design of the experiment (Fig. 1B), we examine main effects of acting hand (left, right) and grip type (unimanual, bimanual) and interactions between these factors on the BOLD signals. For the bimanual conditions, the term acting hand refers to the hand functioning as prime actor. Finally, based on the conjunction analysis we examine BOLD activity that was

Discussion

We have examined brain activity in healthy right-handers while they through tool manipulation accomplished the same task under unimanual and bimanual conditions. A single hand performed virtually identical actions whether the task was unimanually or bimanually performed. Furthermore, in contrast to previous studies comparing neural control mechanisms in bimanual and unimanual actions, the acting hand was factored into the present analysis not only for unimanual but also for bimanual actions.

Acknowledgments

We thank Micael Andersson, Anders Bäckström and Göran Westling for their technical support, and Lars Nyberg for the valuable comments on the manuscript. This work was supported by the Swedish Research Council (project 08667) and the 6th Framework Program of the EU (project IST-001917, IST-028056).

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