Impaired grasping in a patient with optic ataxia: Primary visuomotor deficit or secondary consequence of misreaching?
Introduction
In a pioneering series of studies, Jeannerod, 1984, Jeannerod, 1988 proposed that reach-to-grasp actions, such as picking up a desired object, can be partitioned into distinct and quasi-independent visuomotor parts. He argued that the action of moving the arm to bring the hand to the target object (the “proximal” or “transport” component) is principally influenced by visual information signaling the location of the object, whereas the concurrent anticipatory pre-shaping of the hand and fingers in readiness for the grasp (the so-called “distal” or “grip” component) is guided principally by the geometric properties of the object. Although it is accepted that the two components must be somehow mutually co-ordinated, there is now extensive evidence that the transport component and the grip component are each controlled online by dedicated visuomotor networks within the posterior parietal cortex, in association with linked systems in the premotor cortex (Castiello, 2005, Castiello and Begliomini, 2008, Jeannerod et al., 1995, Milner and Goodale, 2006, Tanné-Gariépy et al., 2002).
It has long been known that both components of prehension can be severely disrupted by lesions of the posterior parietal cortex. Damage to this region (particularly around the intraparietal sulcus) in humans is associated with optic ataxia (Karnath and Perenin, 2005, Perenin and Vighetto, 1988), classically defined as a deficit in accurate reaching for visual targets (Bálint, 1909, Harvey, 1995). In the great majority of patients with optic ataxia, grasping turns out to be impaired as well as reaching, and indeed patients will typically fumble for the target with the fingers widely spread, whatever the size of the target (Jeannerod, 1986a, Jeannerod, 1986b, Perenin and Vighetto, 1988, Jakobson et al., 1994). This stands in sharp contrast to the normal pattern in which the handgrip opens only so far as to exceed the target size by a safe margin, and then smoothly closes in (Jakobson & Goodale, 1990; Jeannerod, 1984). Such distal impairments have been associated with optic ataxia since the earliest reports of misreaching following parietal damage, in both monkeys and humans (Damasio and Benton, 1979, Faugier-Grimaud et al., 1978, Ferrier, 1886, Ferrier, 1890, Jeannerod, 1986a, Lamotte and Acuña, 1978, Perenin and Vighetto, 1988). Indeed this close association between the distal and proximal deficits led Perenin and Vighetto, 1983, Perenin and Vighetto, 1988 to follow Bálint (1909) in arguing that optic ataxia reflects a general impairment of visuomotor control rather than a deficit in visuospatial perception (as proposed by Holmes, 1918).
There is of course no necessary contradiction between this neuropsychological association between the distal and proximal deficits, and the quasi-modular visuomotor organization in the brain proposed by Jeannerod and his colleagues. It is entirely reasonable to argue that in most of the patients (and monkeys) studied, the lesions were extensive enough to have compromised both the “grasping” and the “reaching” visuomotor modules. None the less, the question does still arise as to whether an impairment in grip scaling necessarily implies that the patient has damage to such a “grasping” module. Instead, optic ataxia, by virtue of causing inaccurate reaching, might inevitably result in a maximally wide handgrip, simply in order to reduce the margin of error when the patient is trying to grasp an object.
Such an idea would not of course contradict the fact that some patients with parietal lesions misgrasp without misreaching (Binkofski et al., 1998, Jeannerod et al., 1994). These patients, who would not be considered to have optic ataxia, tend to have lesions that include anterior parts of the intraparietal sulcus, in particular the “grasp” region known as AIP or aIPS (Binkofski et al., 1998). These findings are important, because they refute the argument that misgrasping might always be a secondary side-effect of misreaching. The data also mesh nicely with research using functional MRI which has demonstrated distinct activation patterns for grasping (Binkofsky et al., 1999; Cavina-Pratesi et al., 2007, Culham et al., 2003, Frey et al., 2005), separate from those for reaching (Astafiev et al., 2003, Connolly et al., 2003, Culham et al., 2008, Prado et al., 2005). Complementary evidence also comes from nonhuman primate studies finding a clear double dissociation between proximal/arm and distal/hand errors following localized microinjections of muscimol (Gallese, Murata, Kaseda, Niki, & Sakata, 1994).
Although misgrasping can clearly arise in the absence of misreaching, it remains uncertain that the converse dissociation holds true in patients with optic ataxia. That is, it remains possible that in many such patients impaired grasping arises purely as a secondary consequence of misreaching, and not as the result of disruption of the “grasp” module.
Flesh can be put on the bones of these doubts. Numerous visuomotor studies show a tendency in healthy subjects to increase the size of their anticipatory grip aperture to compensate for factors that increase transport inaccuracy during reaching toward the object to be grasped. In one such study, maximum grip aperture (MGA) was found to be significantly greater during reaching movements that were performed faster than normal, and also during reaching with the eyes closed (Wing, Turton, & Fraser, 1986). In both cases, this wider hand aperture was accompanied by less accurate transport of the hand toward the target location. It is reasonable to infer that in these circumstances anticipatory grip aperture was enlarged to give a wider margin of error for achieving a successful capture of the object, thereby compensating for the spatial inaccuracy associated with speeded movements. Similar findings of an increased maximum grip aperture during reaching have been reported in cases where the stimulus uncertainty is increased in other ways, for example when visual target size is reduced (Berthier, Clifton, Gullapalli, McCall, & Robin, 1996), when the field of view is restricted (González-Alvarez, Subramanian, & Pardhan, 2007), or when the target eccentricity is increased (Goodale and Murphy, 1997, Schlicht and Schrater, 2007).
In the present paper we aimed to test whether deficits in grip calibration can be separated from deficits in reaching accuracy in optic ataxia, by the use of a task requiring grasping without arm transport. Such a task was developed by Cavina-Pratesi et al. (2006; see also Culham et al., 2008) in order to achieve a clean contrast between ‘pure grasping’ and ‘pure reaching’ in a functional MRI study.1 We adopted this methodology in the present experiment in an attempt to tease apart the transport from the grasp impairment in a patient with optic ataxia (M.H.). Our specific intention was to establish whether his grasping difficulties were primary, or secondary to poor reaching; but at the same time we wished to validate our method so that it might be used for making unambiguous assessments of other such patients in the future.
Section snippets
Subjects
Patient M.H. had suffered an anoxic episode 8 years prior to the current testing. Structural MRI carried out in 2006 revealed disseminated damage in posterior parietal and frontal regions, concentrated particularly in the vicinity of the intraparietal sulcus of the left hemisphere, with some extension onto the medial aspect and into the inferior parietal lobule. Some atrophy was visible in the left hemisphere both cortically (within the posterior parietal, fronto-temporal and frontal regions)
Transport component
Analysis of the mean reaching error (or transport error, TE) revealed a significant interaction of viewing condition × distance (F(1,6) = 10.90, p = 0.016) with the mean TE for the far reaches being higher (9.82 mm) than for close ones (8.99 mm) during central fixation only. Analysis of the variability of TE showed a significant main effect of movement direction (F(1,6) = 11.96, p = 0.014) with inward movements (22.4) being less variable than outward (27.6) ones. In addition, an interaction of hand × space (F
Discussion
Our aim in this study was to tease apart the reaching and grasping impairments in a patient with optic ataxia (M.H.), by varying the proximal and distal requirements of a prehensive action. We manipulated the proximal component (arm transport) by asking our participants to grasp objects either at a close location adjacent to the hand (arm transport not required), or at a far location within reach of the hand but not immediately adjacent to it (arm transport required). We manipulated the distal
Acknowledgements
The authors are grateful to Dr Robert McIntosh and Dr Thomas Schenk for their comments on the first draft of the manuscript and to Isabella Curti for helping during data collection. Most of all, the authors wish to thank M.H. for his kindness and endless patience. The research was funded by the Medical Research Council (grant no. G0401090).
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