The coordination of bimanual prehension movements in a centrally deafferented patient

Brain (2000), 123, 380–393 The coordination of bimanual prehension movements in a centrally deafferented patient G. M. Jackson,1 S. R. Jackson,1 M. Husain,2 M. Harvey,3 T. Kramer3 and L. Dow4 1Centre for Perception, Attention and Motor Sciences, School of Psychology, University of Wales, Bangor, 2Division of Neuroscience and Psychological Medicine, Imperial College School of Medicine, Charing Cross Hospital, London, 3Department of Experimental Psychology, University of Bristol and 4Care of the Elderly, Frenchay Hospital, Bristol, UK Correspondence to: Dr Georgina M. Jackson, School of Psychology, University of Nottingham, University Park, Nottingham NG7 2RD, UK E-mail: Summary Many everyday tasks require that we use our hands cooperatively, for example, when unscrewing a jar. For tasks where both hands are required to perform the same action, a common motor programme can be used. However, where each hand needs to perform a different action, some degree of independent control of each hand is required. We examined the coordination of bimanual movement kinematics in a female patient recovering from a cerebrovascular accident involving anterior regions of the parietal lobe of the right hemisphere, which resulted in a dense hemianaesthesia of her left arm. Our results indicate that unimanual movements executed by our patient using her non-sensate hand are relatively unimpaired. In contrast, during bimanual movements, reaches executed by our patient using her non-sensate hand show gross directional errors and spatiotemporal irregularities, including the inappropriate coupling of movement velocities. These data are discussed with reference to the role played by limb proprioception in the planning and control of prehension movements. Keywords: bimanual movements; reach-to-grasp; deafferentation; hemianaesthesia; parietal cortex Abbreviations: BA ⫽ Brodmann area; BIT ⫽ Behavioural Inattention Test; MD ⫽ movement duration; PGA ⫽ peak grip aperture; SI ⫽ primary somatosensory cortex; SII ⫽ secondary somatosensory cortex; TTPGA% ⫽ time taken to reach peak grip aperture expressed as a percentage of total movement time; TTPV ⫽ time taken to reach peak movement velocity; WAIS-R ⫽ Wechsler Adult Intelligence Scale—Revised Introduction Planning and execution of bimanual movements When we execute a unimanual reaching movement to a target position, the duration of the movement is frequently found to depend on the ratio of movement amplitude to target size (a formula known as Fitts’ Law). Movement duration (MD) is shorter when the distance is small and/or the target is large (sometimes referred to as having a low index-of-difficulty), compared with when the distance is longer and/or the target object is smaller (referred to as having a high index-ofdifficulty). Bimanual movements in which both hands execute movements of the same index-of-difficulty also conform to this rule, while bimanual movements of mixed index-ofdifficulty do not (Kelso et al., 1979, 1983; Jackson et al., 1999). During bimanual movements subjects tend naturally to synchronize their hands, even when they are not explicitly instructed to do so (Keele, 1986). As a consequence, MD as well as time to movement onset are often similar for both © Oxford University Press 2000 hands. The hand reaching for the difficult target takes less time than it would when reaching to the same target under unimanual conditions, whereas the hand reaching to the easy target takes more time than it would for a unimanual reach. While it has been argued that there can be significant departures from synchrony when the limbs are moving to mixed difficulty targets (Marteniuk et al., 1984), it should be noted that the absolute differences in movement onset times and MD between the limbs is usually small (~100 ms or less). How might this degree of temporal synchronization be achieved? Two broad classes of explanation can be distinguished: one suggests that coordination of movement components is planned in advance of movement onset and based upon temporal synchronization (e.g. Jeannerod, 1981, 1984; Hoff and Arbib, 1993); the other proposes that coordination is achieved by the on-line control of movement Central deafferentation and bimanual prehension parameters based upon continuous sampling of spatial information (e.g. Bootsma and van Wieringen, 1992; Zaal et al., 1999). While these models differ quite substantially in their account of how temporal synchronization is achieved, proprioceptive signals are likely to be critical for effective synchronization in either case. Recent findings from the visual attention literature demonstrate that individuals are limited in their ability to attend to more than one object at a time (Duncan, 1984). Duncan and colleagues propose that visual information related to different objects results in competition between those objects, which is characterized as a reduction in the efficient processing of each object (Duncan et al., 1997). One obvious limiting factor during the execution of bimanual movements is the need to control and maintain the synchronicity of two actions unfolding in parallel. One possible role for proprioception in this case would be to allow bimanual movements to be executed without the need to allocate attentional resources. Proprioception and the coordination of upperlimb movements The sensorimotor system controlling upper-limb movements may use both visual and proprioceptive inputs to formulate motor commands. However, movement accuracy is maximized when both are available (Rossetti et al., 1994, 1995). Visual information can serve to calibrate proprioceptive knowledge of initial limb position (Rossetti et al., 1994, 1995) and to make on-line corrections to a kinaesthetically controlled hand path (Goodale et al., 1986). Recent evidence also suggests that proprioceptive signals can function to update ‘visual’ representations of peripersonal space (Carey and Allan, 1996). It should be noted, however, that the precise role played by both visual and proprioceptive signals may vary with task demands such as the requirement for accuracy or the need for manipulation. The role played by proprioception in limb movement control has previously been investigated by studying how movements are affected by the removal of proprioceptive signals. Studies of single joint movements have suggested that neither proprioceptive nor visual information is entirely necessary for movement initiation or for computing the final position of the limb. For example, deafferented monkeys can execute simple aimed movements with relative accuracy, even in the absence of vision (Polit and Bizzi, 1979). However, it should be noted that in this experiment the animals were highly trained and the terminal accuracy of the movements did not approach normal levels. Similar results have been obtained in human subjects with a peripheral deafferentation due to large-fibre sensory neuropathy—a condition which results in the degen (...truncated)