Reaching with a tool extends visual–tactile interactions into far space: evidence from cross-modal extinction
Introduction
Extinction is a common sign after unilateral brain damage, especially following right-hemisphere lesions [5], [22]. The patient can perceive a contralesional stimulus in isolation, yet fails to perceive the same stimulus when delivered together with an ipsilesional one. Such extinction can arise cross-modally. For example, in patients with right-hemisphere lesions, a visual stimulus near the right hand may prevent awareness of a touch on the left hand that would otherwise be felt (e.g. [4], [15], [16], [18]). Recent studies show that such cross-modal extinction is reduced by moving the right visual stimulus away from the right hand [4], [15], [16], so that it no longer falls in the ‘peripersonal’ space [20] immediately around that hand. This may relate to multimodal neurons found in several areas of monkey cortex, responding to both vision and touch with spatially corresponding receptive fields in the two modalities [2], [8], [9], [10], [11]. For such cells, if the tactile receptive field is on one hand, the visual receptive field will fall in the peripersonal space around that hand, and indeed will shift along with postural changes of the hand [10], [11]. If similar cell populations exist in humans, a visual stimulus near one hand might thereby boost the representation of that hand [6], to compete [5] with the activity produced by touch on the other hand, thus producing cross-modal extinction when the other hand has been disadvantaged by a unilateral lesion [4], [15].
Here we tested whether cross-modal extinction of left touch in a right-hemisphere patient could be increased for a visual stimulus that is far from the right hand, when connected to that hand by a stick which the patient holds (see [19] for a related stick manipulation in normals). This situation tests whether the critical factor determining cross-modal extinction is the physical distance between a visual stimulus and the hand (as might be expected on simple ‘spotlight’ models; [6]), or instead whether the visual stimulus falls within the possible action-space of the hand, which is extended by holding a stick [1], [7]. Increased extinction when wielding the stick could be predicted on the basis of recent physiological results from multimodal neurons in the intraparietal sulcus [13].
Section snippets
Patient
BV was a 67 yr-old right-handed male who suffered a right hemisphere ischaemic stroke in the territory of the posterior cerebral artery (Fig. 1).
On neurological assessment five weeks later, he showed a left homonymous hemianopia plus a mild distal motor and proprioceptive impairment for the left limbs. He also showed left neglect in daily life and formal testing (Behavioural Inattention Test [23] score was 31; cut-off is 129). On confrontation with light touch, tactile sensitivity appeared
Results
E1: The percentage of correct responses on unilateral and bilateral trials is shown in Fig. 3 (Leftmost graph, E1) for each condition. BV's performance for unilateral trials was virtually errorless. By contrast, performance on bilateral trials showed many errors, all taking the form of missing the left touch while reporting only the right visual stimulus. Extinction rate depended on condition. The most severe extinction was in the Near Hand condition (6% bilateral correct), followed by the Far
Discussion
The results from both experiments show that cross-modal extinction was modulated not only by the physical distance of the right visual stimulus from the right hand (cf. [4], [15], [16]), but also by the patient wielding a stick in the right hand which reached to that far visual stimulus. The latter condition increased the cross-modal extinction produced by the far visual stimulus. Adding a long stick, which rested on the table without connecting the hand to the far visual stimulus (Gap
Acknowledgements
This work was supported by an MRC Programme grant and a McDonnel Pew project grant to J.D. Thanks to Chris Rorden, Steffan Kennett and Giacomo Giampieri for technical help and to Elisabetta Ladavas for discussions of her related work with Alessandro Farnè, which was conducted independently of the present study at around the same time. Thanks also to Professor Alan Thompson and staff of the Rehabilitation unit at the National Hospital for Neurology and Neurosurgery and to BV for his cheerful
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