Left hand movements and right hemisphere activation in unilateral spatial neglect: a test of the interhemispheric imbalance hypothesis
Introduction
Unilateral spatial neglect (USN) can be considered the most frequent and dramatic behavioral defect of patients with right hemisphere damage [8], [10] and as a major factor in poor recovery after stroke [7]. Therefore, several authors have tried to develop rehabilitation techniques or to search for experimental conditions that can temporarily or persistently reduce hemineglect. The best known and most effective experimental condition which can transiently reduce USN is caloric vestibular stimulation, proposed by Rubens [37] and developed by Cappa et al. [4], Vallar et al. [39], [41], and Rode et al. [36]. Rubens reasoned that if unilateral neglect is partly due to a gaze and postural turning bias, then caloric vestibular stimulation, producing eye deviation and past-pointing in the direction opposite to this bias, should reduce the tendency to neglect stimuli in the contralateral half space. His results strongly supported the hypothesis since, even in patients with severe neglect, vestibular stimulation markedly improved performance on tests of visual neglect. Effects similar to those observed after caloric vestibular stimulation have since been obtained using other techniques such as optokinetic stimulation [29], [38], trunk midline orientation [23], neck muscle vibration [21], [23] and transcutaneous electrical nervous stimulation [22], [40].
However, the interpretation of these well-established findings remains controversial. Some authors maintain that the structures recruited during caloric vestibular stimulation and other facilitatory techniques contribute to the generation of a body centered spatial map for directing attention and movements toward extrapersonal space. According to this interpretation, USN should be considered as an orienting bias produced by defects in a central reference system, and all the above mentioned techniques could contribute to restoring this spatial map, thus reducing the imbalance in the system [23], [29], [38].
An alternative interpretation, more in line with the ‘peripheral’ hypothesis that prompted Rubens’ seminal experiment, assumes that all these manoeuvres act on the output systems of this integrated reference frame, thus reducing the consequences of its imbalance. For example, by provoking a forced automatic gaze displacement, caloric vestibular stimulation and optokinetic stimulation could prompt a correlative automatic displacement of attention, since direction of eye movements and direction of attention are closely related in spontaneous and uncontrolled conditions [18]. Similar reasoning could be applied to other techniques which influence the severity of neglect by manipulating other components of the spatial orienting apparatus (see [10], [11] for a more thorough discussion of this issue).
An important contribution to clarifying this issue could come from the study of other facilitatory techniques based on the activation of body parts, such as the limbs, which should be less critically involved in the construction of the body reference frame. However, it must be noted that even if several authors have shown through the use of different experimental paradigms that active movements of the left hand can improve the severity of USN, the mechanism underlying this improvement is still controversial.
Joanette and coworkers [19], [20] and Robertson and coworkers [32], [33], [34], [35] attributed the improvement of neglect observed after left hand movements to the activation of the right hemisphere premotor systems associated with the use of the left hand. This interpretation, which is based on ‘premotor’ model of neglect of Rizzolatti and coworkers [30], [31], assumes that since attentional and motor circuits are intimately linked in the brain, the activation of the right hemisphere motor circuits should lead to a recruitment of the associated attentional mechanisms, thus improving attention for the left side of space. On the other hand, Halligan and coworkers [14], [16] showed that the left hand advantage for line bisection performance is reduced when this hand starts from the right extremity of the line. These authors proposed that the left hand acts as a cue enhancing attention to the left side of space. Still other authors (e.g. [25], [27]) proposed that by increasing the activity of the right hemisphere, left hand movements may counteract the interhemispheric imbalance which, according to Kinsbourne [24], [25], subserves the clinical manifestations of neglect. In fact, Kinsbourne’s influential model assumes: (a) that attention may be directed along a vector resulting from the interaction of paired opponents processors controlled, respectively by the right and left hemisphere and (b) that neglect resulting from right hemisphere damage may be modified by reducing (or increasing) the interhemispheric imbalance via activation of the right (or respectively of the left) hemisphere.
The aim of the present research was to try to check this last hypothesis by means of a slightly modified version of the ‘limb activation technique’ proposed by Robertson and North [32], [33], [34]. In their basic experiment, conducted on patient TD, these authors showed that a reduction of left-sided neglect can be observed when the patient voluntarily moves the fingers of his left hand in the left half space. This effect, evaluated by using the total number of omissions made on the letter cancellation sub-test of the Behavioural Inattention Test [42] as a measure of neglect, was not dependent on the patient’s limb being in view, was not obtained when the left hand moved in the right half space and was not produced by a passive movement of the same hand. Robertson and North’s study was criticized on methodological grounds by Cubelli et al. [6], and only in part confirmed by Ladavas and coworkers [9], [26]. Cubelli et al. [6] argued that, since patients with USN usually also have a generalized attentional impairment in addition to a lateralized defect of space exploration, it is possible that left hand movements, by improving the level of arousal, may reduce the total number of omissions without reducing the right–left asymmetry that is the hallmark of USN. Ladavas and coworkers [9], [26], on the other hand, showed that the severity of neglect can be reduced not only by active, but also by passive movements of the left hand. In spite of these minor objections, several studies confirmed that active movements of the left hand can reduce the severity of neglect [2], [5] or of visual extinction [28].
In our study, we intended to replicate this experiment in an unselected group of neglect patients by keeping under control two variables which (according to the ‘interhemispheric imbalance hypothesis’) should influence the severity of neglect in a predictable way. These variables are the following: the (right or left) half space where the left hand moves and the (verbal or visual–spatial) nature of the material used to measure the severity of neglect. We predicted that if left hand movements reduce the severity of neglect by activating the right hemisphere, then: (a) these movements should improve the severity of USN, irrespectively of the half space where the left hand moves since, in any case, the left hand movements should activate the right hemisphere; (b) neglect should be more severe with visual–spatial stimuli, which activate the right hemisphere, than with verbal stimuli, which activate the left hemisphere. This last prediction had been previously checked with conflicting results by other authors [3], [5], [17], but perhaps these contrasting results could be explained by methodological considerations. One of these could be the measures used to evaluate the severity of neglect since, according to Kinsbourne [24], [25], in USN the attentional defect is not limited to the left half space, but shifts along a continuum from the extreme right to the extreme left half space. Now, since the standard measures used to evaluate the severity of neglect on a cancellation task are substantially based on the number of omissions made on the right and left half sheet, they are probably inappropriate for testing the interhemispheric imbalance hypothesis and it was necessary to find a more appropriate measure of neglect to test this dynamic model.
Therefore, in our study we used a new method, labeled the center of the ‘attentional field’, devised to evaluate the spatial distribution of the patient’s attention, in keeping with Kinsbourne’s construct of neglect, in addition to three traditional measures of the severity of neglect. The latter were based on the total number of omissions made on the cancellation sheet, the number of omissions made on the left half sheet and on the difference between the omissions made on the right and left half sheet.
Section snippets
Patients
Data used to check our working hypothesis were gathered on seven right brain-damaged patients with clinical evidence of left neglect, but spared ability to move the left hand, at least in part.
These patients were selected from a consecutive series of patients who had been referred to the Policlinico Gemelli in Rome over a 2-year-period (from June 1997 to June 1999) due to a recent stroke. The main selection criteria were the following: (a) a single right hemisphere lesion due to a recent
The influence movements of the left hand on the right and left sides of space can have on severity of neglect
Due to the small size of our experimental sample, the influence movements of the left hand on the right and left sides of space can have on the severity of neglect was studied by pooling together results obtained with verbal and visual–spatial stimuli. Data necessary for this analysis were obtained by computing four kinds of measures (namely, total number of omissions, left-sided omissions, left minus right-sided omissions and center of attentional field) for each patient in three experimental
Discussion
The aim of the present research was to check the basic prediction of Kinsbourne’s ‘interhemispheric imbalance hypothesis’, which assumes that conditions leading to an activation of the right hemisphere should reduce the severity of contralateral neglect. This prediction was checked in a group of neglect patients with a slightly modified version of the ‘limb activation technique’ [32], [33], [34] by considering the following critical variables: (1) the (verbal or visual–spatial) nature of the
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