Angelo Maravita

Multisensory integration and the body schema: close to hand and within reach

There has been a recent and dramatic growth of interest in the psychological and neural mechanisms of multisensory integration between different sensory modalities. Much of this recent research has focused specifically on how multisensory representations of body parts and of the peripersonal space immediately around them, are constructed. Research has also focused on how this may lead to multisensorially determined perceptions of body parts, to action execution, and even to attributions of agency and self-ownership for the body parts in question. Converging evidence from animal and human studies suggests that the primate brain constructs various body-part-centred representations of space, based on the integration of visual, tactile and proprioceptive information. These representations can plastically change following active tool-use that extends reachable space and also modifies the representation of peripersonal space. These new results indicate that a modern cognitive neuroscience approach to the classical concept of the body schema may now be within reach.

Tool-use changes multimodal spatial interactions between vision and touch in normal humans

In a visual-tactile interference paradigm, subjects judged whether tactile vibrations arose on a finger or thumb (upper vs. lower locations), while ignoring distant visual distractor lights that also appeared in upper or lower locations. Incongruent visual distractors (e.g. a lower light combined with upper touch) disrupt such tactile judgements, particularly when appearing near the tactile stimulus (e.g. on the same side of space as the stimulated hand). Here we show that actively wielding tools can change this pattern of crossmodal interference. When such tools were held in crossed positions (connecting the left hand to the right visual field, and vice-versa), the spatial constraints on crossmodal interference reversed, so that visual distractors in the other visual field now disrupted tactile judgements most for a particular hand. This phenomenon depended on active tool-use, developing with increased experience in using the tool. We relate these results to recent physiological and neuropsychological findings.

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

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 patients 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 patients 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.

Prism adaptation can improve contralesional tactile perception in neglect

The authors show that prismatic adaptation can reduce tactile inattention in stroke patients with unilateral neglect. Four patients with visuospatial neglect and tactile extinction underwent 10-minute application of 20° right-shifting prismatic lenses during pointing. This improved contralesional tactile perception in all patients, even for a task requiring no exploration or spatial motor responses. This finding suggests a potential role for prismatic adaptation in the rehabilitation of multiple sensory modalities in patients with neglect.

Multisensory contributions to the 3-D representation of visuotactile peripersonal space in humans: evidence from the crossmodal congruency task

In order to determine precisely the location of a tactile stimulus presented to the hand it is necessary to know not only which part of the body has been stimulated, but also where that part of the body lies in space. This involves the multisensory integration of visual, tactile, proprioceptive, and even auditory cues regarding limb position. In recent years, researchers have become increasingly interested in the question of how these various sensory cues are weighted and integrated in order to enable people to localize tactile stimuli, as well as to give rise to the felt position of our limbs, and ultimately the multisensory representation of 3-D peripersonal space. We highlight recent research on this topic using the crossmodal congruency task, in which participants make speeded elevation discrimination responses to vibrotactile targets presented to the thumb or index finger, while simultaneously trying to ignore irrelevant visual distractors presented from either the same (i.e., congruent) or a different (i.e., incongruent) elevation. Crossmodal congruency effects (calculated as performance on incongruent-congruent trials) are greatest when visual and vibrotactile stimuli are presented from the same azimuthal location, thus providing an index of common position across different sensory modalities. The crossmodal congruency task has been used to investigate a number of questions related to the representation of space in both normal participants and brain-damaged patients. In this review, we detail the major findings from this research, and highlight areas of convergence with other cognitive neuroscience disciplines.

Electrophysiological Correlates of Conscious Vision: Evidence from Unilateral Extinction

To study the electrophysiological correlates of conscious vision, we recorded event-related potentials (ERPs) in a patient with partial unilateral visual extinction as a result of right-hemisphere damage. When, following bilateral presentations, contralesional stimuli were not perceived, there was an absence of the early attention-sensitive P1 (80-120 msec) and N1 (140-180 msec) components of the ERP response. In contrast, following unilateral presentations, or in those bilateral presentations in which contralesional stimuli were perceived (about 60), these ERP components were present. These results provide novel evidence that extinction involves the stage of early focusing of attention and that the P1 and N1 components of visual ERPs are reliable physiological correlates of conscious vision.

Active tool use with the contralesional hand can reduce cross-modal extinction of touch on that hand.

After a unilateral brain lesion, patients may show cross-modal, visual-tactile extinction. Such patients may fail to report tactile stimuli on the contralesional hand when presented together with competing visual stimuli near the ipsilesional hand. In this work we tested the hypothesis that this cross-modal extinction may be reduced when a patient has used a tool with the contralesional hand to reach for objects in the ipsilesional visual field. Consistent with previous work, we hypothesize that active use of a tool may extend cross-modal interactions between visual stimuli at the tip of the tool and tactile stimuli on the hand wielding the tool. In the new situation of a tool connecting the contralesional hand with ipsilesional visual space, competition between stimuli on these opposite sides may be reduced, so that extinction decreases. We studied patient BV, who showed reliable cross-modal, visual-tactile extinction after right-hemisphere stroke. In two separate sessions we showed that prolonged tool use (10-20 min) with the contralesional hand in ipsilesional space reduced cross-modal extinction for up to 60-90 min post-training. We propose that an actively used tool may be effective in linking cross-modal stimuli presented along its extension. This can then overcome competition between stimuli presented on opposite sides of the body midline, thus modulating extinction.

The electrophysiology of tactile extinction: ERP correlates of unconscious somatosensory processing

We examined the electrophysiological correlates of left-sided tactile extinction in a patient with right-hemisphere damage. Computer-controlled punctate touch was presented to the left, right or both index fingers in an unpredictable sequence. The patient reported his conscious tactile percept (left, right or both). He showed extinction on 75% of bilateral trials, reporting only right stimulation for these. Somatosensory evoked potentials for unilateral stimulation showed early components over contralateral somatosensory areas (P60 and N110) for either hand. In contrast to the results observed for age-matched controls, the patients P60 was smaller in amplitude for left-hand touch over the right hemisphere than for right-hand touch over the intact hemisphere. Bilateral trials with extinction revealed residual P60 and N110 components over the right hemisphere in response to the extinguished left touch. These results demonstrate residual unconscious somatosensory processing of extinguished touch. They also suggest that tactile extinction can be caused by attenuation rather than elimination of somatosensory responses in the damaged hemisphere, with an underlying deficit even on unilateral trials.