Passive limb movements improve visual neglect

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Abstract

Recent studies have reported that left neglect can be ameliorated during active movements of a contralesional limb in the contralesional space. In contrast, a passive left hand movement does not seem to induce an amelioration of neglect, at least when it is associated to simultaneous active right movement (Robertson IH, North N, Neuropsychologia 31 (1993) 293–300). In the present study, we explored the possibility that a complex passive movement, such as abduction and adduction of the arm, is able to reduce neglect also when it is associated to simultaneous active right arm movements. To test this hypothesis neglect patients were required to perform an object cancellation test and a line bisection test by using the right hand, while the left arm was passively moved. Moreover, we verified the possibility that left arm stimulation activates the peripersonal more than the extrapersonal space, with the exception of the condition in which the far space can be reached by a tool that extends peripersonal space in the far space (Farnè A, Làdavas E, Neuroreport 11 (2000) 1645–1649). For this reason, patients were required to perform the tasks in near (70 cm) and in far (140 cm) space by means of a light pen (pointing task) and of a stick (reaching task).

When the left arm was passively moved the results showed a significant reduction of neglect with respect to the baseline condition, and the improvement equally affected the near and the far space. A different effect for the near and far space was observed in relation to the task (pointing vs. reaching). In the pointing task, neglect was more severe in the far than in near space; however, this difference disappeared when the patients had to reach objects by means of a stick.

In conclusion, the present study shows that the entity of improvement of visual neglect due to a left passive movement is related to the entity of proprioceptive signals specifying left hand position.

Introduction

Unilateral visual neglect typically produces inattention for stimuli located on the left (or contralesional) side of space. The deficit has been conceived as a representational deficit due to the competition between left and right space representations [4], [9], [10], [21], [34].

The unilateral damage of a brain area with a contralateral field representation results in a reduction of competitive weights in the affected field. After a right brain damage, the activation of a contralateral space representation is weak and, as a consequence, the competition with intact ipsilesional space representation induces neglect in that sector of space. The competition might operate on a number of different topographically mapped brain areas encoding both the input and output components of responses, each of them contributing to the construction of the perceived space representation. The antagonism between left and right space representation, however, may be reduced by the activation of a spatial representation mapped in another right brain structure, which co-operates, through mutual excitation, with the damaged representation. The reduction of this antagonism will produce a better level of activation of the left-side representation of the space and, as a consequence, it will increase the level of detection for left-sided stimuli.

For example, it has been shown that the level of awareness of left-sided stimuli presented in the extrapersonal space can be increased by rendering the proprioceptive signals specifying the position of the left hand more salient [16], [21], [26]. Halligan et al. [16] showed that neglect in a line-bisection test was less severe when the left hand was used, although the effect disappeared when the subject was required to begin the task with his/her left hand positioned in the right space. Therefore, it seems that the spatial position of the hand, more than the responding hand, can be the crucial factor in determining the modulation of neglect. This conclusion has been confirmed by Robertson and North [26]. When patients with neglect were asked to make minimal finger movements in the left hemispace with either hand, a reduction of neglect was found only in the condition in which the left hand was making movements in the left hemispace. This means that, in order to obtain a reduction of neglect, the hand (left) and the spatial position of the hand (left) have to be combined: neither right hand responses in the left hemispace nor left hand responses in the right hemispace produced an amelioration of neglect.

These studies clearly show that the activation of proprioceptive information related to the position of the limb can modulate the impaired representation related to extrapersonal space. Moreover, it has been shown by Robertson and North [28] that only an active movement of the left hand is able to produce an amelioration of visual neglect, whereas a passive left hand movement in the left hemispace does not seem to reduce neglect. A possible explanation for this result is that in their study the patient had to cancel the letters ‘E’ and ‘R’, randomly distributed among five rows of letters, by using the right hand; this might have cancelled a weaker effect due to the passive left hand movement. In this case, the left-side representation, evoked by a passive movement, is weaker comparing to the right spatial representation evoked by an active right hand movement.

This interpretation has been confirmed by a study of Làdavas et al. [21] in which patients did not use the right hand to perform the task. In an experimental condition in which patients were required to name objects depicted on a sheet of paper, they found an amelioration of neglect by simply using a passive left hand movement.

A further explanation for the lack of a neglect improvement in Robertson et al.'s study is that a passive finger movement might be too weak to compete with an active right hand movement. Thus, it is possible to hypothesise that more complex passive movements, such as abduction and adduction of the arm, might activate strongly the left side of space producing a reduction of neglect. In this condition, passive movements might produce amelioration also when a simultaneous active right arm movement is performed in the right space.

In the present study the effect of a left-side passive activation was measured in a condition in which there was not a competing right-side activation (object naming task and perceptual line bisection task) and in a condition in which there was a simultaneous right-side activation (object cancellation task and motor line bisection task). If the proprioceptive activation, produced by the passive abduction and adduction of the left arm, is strong enough to compete with the activation produced by the use of the right arm, no difference between the two experimental conditions should emerge. In contrast, if a passive movement can evoke only a weak left-side space representation, a better performance is expected in the condition in which patients perform the task without a competing right-side movement, i.e. in the object naming and in the perceptual line bisection.

There are some evidence showing that neglect can be reduced by increasing the level of arousal [12], [31]. Therefore, a speculative explanation of the expected neglect amelioration can rely on a non-specific increase in arousal caused by an arm passive movement. To check for this possibility, patients performed the perceptual tasks (object naming task and perceptual line bisection task) also during passive right limb activation. Naturally, in this experimental condition, patients could not perform motor tasks (cancellation task and line motor bisection task) due to their severe left motor impairment. If the amelioration of neglect is due to a general alertness effect, then the beneficial effect should be present also during right limb activation.

In selecting repeated measure of spatial behaviour sensitive to neglect, we attempted to sample from three theoretically and empirically distinct domains of space representation. It is now clearly established that neglect for personal, peripersonal, and extrapersonal space can be dissociated from each other [15], [17], [25]. Personal space is usually referred to a body space, peripersonal space is that immediately surrounding the body and reachable by an arm movement and extrapersonal space is that outside a direct manual reaching. In the present study, we also have explored the possibility that the amelioration of neglect induced by the limb activation might be specific for peripersonal space. For this reason, the experimental material was presented at a distance of 70 cm (near space) or at a distance of 140 cm (far space). If left arm stimulation selectively activates the peripersonal space, i.e. the space reachable by the hand, then a better performance is expected, during left limb activation, in the near than in the far space.

Moreover, neurophysiological and neuropsychological findings showed that peripersonal space has important dynamic properties: it can be expanded and contracted depending upon tool use [2], [11], [19]. Iriki et al. [19] found, in the monkey parietal lobe, bimodal neurons that coded the schema of the hand. These neurons fired when a tactile stimulus was delivered to the monkey's hand and when visual objects were presented near the hand tactile receptive field. The most striking characteristic of these neurons was that their visual receptive field was modified during a reaching movement performed with a rake up to include its entire length and to cover the expanded accessible space. Moreover, the bimodal neurons’ visual receptive field was modified only when the monkey reached for an object with a rake and not when the monkey just held the rake.

A single case study by Berti and Frassinetti [2] showed that the use of a stick influenced the computation of far space also in human. They described a patient P.P. who had neglect in near, but not in far space, when she had to bisect a line by means of a light pen. In contrast, when the patient had to reach the line located in the far space by means of the stick, the left part of the line was misperceived, as it was in near space. The reaching to ‘far’ space with a tool caused an expansion of the impaired near space into the far space. Similar results were found by Farné and Làdavas [11], who investigated this phenomenon in patients with tactile extinction, by using a cross-modal visuo-tactile paradigm well suited to reveal visual peripersonal space near patient's hand. Cross-modal visuo-tactile extinction was assessed far from the hand, at the distal edge of a hand-held rake. They found that cross-modal extinction was more severe after patients used the rake to retrieve distant objects with respect to a condition in which the rake was not used. These results clearly show that the use of a tool increases the spatial extent of the representation of peri-hand visual space to incorporate the tool.

For this reason, patients were required to perform the experimental motor tasks in the near and in the far space by means of a light pen (pointing task) and of a stick (reaching task). In patients with neglect, far space is usually more impaired than near space [6]; however, the use of a stick might reduce the severity of neglect in far space which, due to the stick-use, becomes in effect near space. If this is the case, a better performance is expected for the far space when patients use a stick compared to a light pen. In contrast, patients’ performance on the near space should be independent of the use of a light pen or a finger movement response.

Section snippets

Subjects

Subjects were eight patients with right brain damage and left visual neglect, recruited from ‘Don Gnocchi’ Hospital in Parma. All had unilateral lesions due to cerebrovascular accidents. Lesion sites were confirmed by CT scans and are reported in Table 1. All patients were right handed. Gender, age and length of illness are reported in Table 1. They were fully oriented in time and place. Motor, somatosensory and visual deficits were assessed through a neurological examination. All patients were

Results

Three different ANOVAs were performed, one for each hypothesis put forward in the present study. One aim was to verify the effect of left and right-side passive activation on visual neglect. For this reason, two 2×3 ANOVAs were performed, one on the results obtained in object naming task and the other in perceptual line bisection task, with the following main effects: space (near and far) and condition (baseline, left stimulation, right stimulation). Besides the analysis of variance, pairwise

Discussion

Unilateral left neglect is one of the best predictors of poor functional recovery following stroke [7], [14], [20], [32]. A temporary recovery of neglect can be induced through a neurophysiological manipulation [3], or through a specific manipulation of the experimental tasks, aimed at producing an activation of the damaged space representation.

One of this manipulation can be that of limb activation, i.e. to induce patients to make even small movements with some part of the left side of their

Acknowledgements

We wish to thank Dr. Paola Affanni for the discussion of clinical cases. This work was supported by grants from MURST and Mc Donnell Foundation.

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