Reaching with a tool extends visual–tactile interactions into far space: evidence from cross-modal extinction

Abstract

Several recent studies have shown cross-modal visual–tactile extinction in patients with right hemisphere lesions. In the present case, patient BV, a visual stimulus close to the right hand extinguished awareness of a touch on the left hand that would otherwise have been felt. Such extinction was reduced if the right visual stimulus was placed more distant from the patient's hand in the radial plane. However, when the patient held sticks in both hands, so that a far right visual stimulus was now at the end of the “tool” in his right hand, cross-modal extinction from this far stimulus increased. This effect depended on the patient holding a stick that reached to the position of the far visual stimulus; a similar large stick, but not connected with the patient's hand and laying passively on the right, had no effect. Wielding the stick induced a re-mapping of space, so that the far light became treated as near (and reachable by) the hand, thus modifying the spatial nature of cross-modal extinction. This may relate to the properties of multimodal neurons as found in the monkey intraparietal sulcus.

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].