Elsevier

Neuropsychologia

Volume 44, Issue 8, 2006, Pages 1325-1335
Neuropsychologia

Modulation of spatial bias in the dual task paradigm: Evidence from patients with unilateral parietal lesions and controls

https://doi.org/10.1016/j.neuropsychologia.2006.01.033Get rights and content

Abstract

Lateral attentional bias is common after unilateral brain damage. It has sometimes been proposed that lateral bias is increased by concurrent cognitive demands, perhaps because of lost top-down compensation. However, an important limitation of previous studies is the sole use of right hemisphere patients. Here we employed a dual task paradigm to measure spatial bias on a visual task while manipulating demands of a concurrent auditory task. Bias was examined in patients with left or right parietal lesions and controls. In Experiment 1 the addition of either a non-spatial or spatial auditory task led to a rightward shift in visual bias. This same rightward shift occurred in controls, left parietals and right parietals. Experiment 2 examined whether the participant's response hand affected their bias. In addition, it attempted to distinguish between the hypothesis that modulatory effects are strongly dependent on lateralization of the concurrent task, and the hypothesis that dual tasks cause a general rightward shift. Response hand was found to have no effect on spatial bias. In addition, bias did not differ between left hemisphere (verbal) and right hemisphere (pitch) concurrent tasks, though the trend was for a smaller rightward shift with the verbal task. Our results show that dual tasks do not exacerbate patients’ underlying deficits; instead they cause a global shift in attention to the right. This shift may resemble general rightward shifts that have previously been linked to reduced arousal.

Introduction

Attentional bias is a common consequence of unilateral damage to many cortical and subcortical brain regions (e.g. Battersby, Bender, Pollack, & Kahn, 1956; Damasio, Damasio, & Chang Chui, 1980; Karnath, Himmelbach, & Rorden, 2002). In unilateral neglect, there is a severe tendency to ignore objects appearing on the contralesional side. Manifestations include failure to eat food on the contralesional side of the plate, failure to groom the contralesional side of the body, and bumping into objects in the environment due to misjudgements of space. Unilateral neglect has been commonly reported following damage to the parietal lobes (Battersby et al., 1956, Critchley, 1949, Critchley, 1953; Driver & Mattingley, 1998; Posner, Walker, Friedrich, & Rafal, 1984).

Although there are a significant number of patients exhibiting these gross deficits, particularly in the acute phase (Stone et al., 1991), many patients with unilateral lesions exhibit much milder deficits, for example visual extinction. Visual extinction is characterised by normal recognition and report of contralesional items when they appear alone. If, however, contralesional and ipsilesional items are presented simultaneously for short exposures, and are thus in direct competition for attentional resources, patients exhibit a failure to see, or an ‘extinction’ of, items on the contralesional side. Here we examine attentional bias in patients with chronic lesions, selected on anatomical rather than behavioural criteria and showing no strong signs of neglect.

Previous studies have shed light on several potential factors which may influence spatial bias. One interesting suggestion concerns the relationship between spatial bias and general cognitive resources (Bartolomeo, 2000; Humphreys, Boucart, Datar, & Riddoch, 1996). Humphreys et al. (1996) reported a case, ARH, who showed chronic contralesional neglect on tasks such as target cancellation whilst showing a paradoxical bias to the contralesional side on extinction tasks. The authors postulate that when task demands are low (in the extinction paradigm) ARH is able to use top-down attentional control mechanisms to consciously compensate for the spatial deficit, thus forcing attention towards the poor field. However, when task demands are increased in the target cancellation task, the patient has fewer resources available and as a result is no longer able to compensate for their underlying deficit. A similar suggestion was made by Bartolomeo (2000). In his study subjects made speeded responses to stimuli appearing in either the left or right field. Subjects were right hemisphere patients with and without neglect and controls. In the baseline condition subjects made the same response to all target stimuli as soon as they appeared. In a second condition a small number of ‘catch trials’, on which a cue informed subjects to withhold responding, was added. As expected, neglect patients were slower to respond to targets appearing in the left field than non-neglecting patients and controls. Interestingly, when catch trials were added, the patients without neglect started to respond like the neglecting patients, with much slower reaction times for left stimuli. Bartolomeo suggested that, in the absence of catch trials, non-neglecting patients were able to inhibit a tendency to orient to the right. However, the addition of the catch trials acted to increase the task demands and reduce the resources available for such inhibition.

Other evidence suggests that attentional bias may be specifically influenced by a task's spatial demands (Cocchini, Cubelli, Della Sala, & Beschin, 1999; Vuilleumier & Rafal, 1999). Vuilleumier and Rafal (1999), for example, showed that spatial versus non-spatial task instructions could modulate awareness of identical stimuli in patients with right lesions. When the task was one of enumeration subjects appeared aware of contralesional stimuli, but when the task was to indicate the locations of items in the same stimulus array, items in the contralesional field were extinguished.

An important limitation of previous studies is the sole use of right hemisphere patients. The greater incidence of chronic neglect following lesions to the right hemisphere (Stone et al., 1991; Stone, Patel, Greenwood, & Halligan, 1992), has suggested that the right hemisphere may be especially important in spatial attention (Heilman, Watson, & Valenstein, 1993). At the same time, significant attentional biases can also follow left hemisphere lesions (Peers et al., 2005). In the present study we examine bias in right parietal patients, left parietal patients and controls. We employ a dual task paradigm to investigate how bias is affected by concurrent task demands. In all conditions the bias is measured by the ability to report targets in a visual task, whilst task demands are varied by changing a concurrent auditory task. The comparison of bias on the visual task alone with bias when the task is paired with a concurrent auditory task examines general effects of increasing task demands. A comparison of bias with spatial and non-spatial auditory tasks examines the specific influence of spatial demands.

Previous data from right hemisphere patients suggest that increasing task demands may simply exaggerate an underlying spatial bias. If this is the case, the addition of a concurrent auditory task in our group (regardless of whether that task is spatial or non-spatial) should increase bias to the right in right hemisphere patients, increase bias to the left in left hemisphere patients and produce no effect in healthy controls. If spatial demands are especially important, then these effects should be particularly marked with the spatial concurrent task.

It is, however, possible to imagine two further scenarios which would predict different patterns of results. Firstly, the effect of a concurrent task may be highly dependent upon its exact nature. The ‘functional distance model’ (see Kinsbourne & Hicks, 1978) suggests that the amount of interference in a dual task situation is dependent upon the distance between the control centres involved in the two tasks. Thus, tasks which are processed by the same or anatomically close regions of the brain (such as speaking and the use of the right hand) are harder to perform together than those which are processed by anatomically distant areas of the brain (such as speaking and the use of the left hand) (Kinsbourne & Cook, 1971). In the present experiment, therefore, if the auditory task recruits the left hemisphere we may expect to see a bias to the left (weaker attention to the right), whilst an auditory task that requires right hemisphere processing would be expected to shift the bias on the visual task to the right (weaker attention to the left). If this is the case then any concurrent task might produce similar effects in all our groups, but the effects would depend on the exact content of the concurrent task.

The final possibility is that dual tasks cause a global bias to the right. As only right hemisphere patients have been tested in previous studies (Bartolomeo, 2000, Humphreys et al., 1996), it is logically possible that rightward shift produced by concurrent tasks could be a general finding, not restricted to this patient group. The use of patients with left hemisphere damage is crucial to test this hypothesis. To anticipate, it is this final possibility that our results support. In Section 4 we suggest a possible analogy to general rightward shifts produced by low arousal (Manly, Dobler, Dodds, & George, 2005).

Section snippets

Participants

The total study sample comprised 24 participants, 13 with parietal lesions and 11 controls (Table 1). Participants were paid a small honorarium and gave full written informed consent prior to each testing session. The study was approved by the Cambridge local research ethics committee. The patient group comprised eight patients with left lesions and five with right lesions, all with lesions centred on the parietal lobe. In some patients lesions extended into temporal and occipital regions (see

Non-spatial dual task

Accuracy on the sound tasks was measured with d′. For the non-spatial task, average d′ values for controls, left parietals and right parietals were 2.18, 1.92 and 0.74, respectively. An analysis of variance (ANOVA) showed a significant main effect of group F(1,21) = 10.93, p < 0.01, with only right parietals significantly impaired compared to both controls (p < 0.01) and left parietals (p < 0.01). The difficulty manipulation on the sound task had the desired effect, with reduced accuracy on the harder

Discussion

Experiment 1 aimed to examine the effects of the addition of a concurrent non-spatial or spatial task on spatial bias in controls, and patients with either left or right parietal lesions. Overall accuracy on both the visual and auditory tasks differed between the three groups. Interestingly, however, the addition of a concurrent task had the same effect in all three groups. Whilst patients with right hemisphere lesions showed the expected exacerbation of their spatial bias, both controls and

Participants

All the participants from Experiment 1 took part in Experiment 2.

Methods

The methods were broadly similar to those from Experiment 1. On this occasion just two blocks of trials were run, the visual task plus an auditory verbal task and the visual task plus a pitch judgement task. The order of completing the two tasks was counterbalanced across participants. Subjects completed 10 trials of practice on the visual task and were presented with examples of each of the sound tasks prior to data collection.

Verbal dual task

Mean d′ values for controls, left parietals and right parietals were 3.43, 3.10 and 2.59, respectively. An ANOVA showed no evidence of differences between the three groups, F(2,21) = 1.31.

Pitch dual task

Mean d′ values on the pitch task were 3.05, 2.84 and 2.15 for controls, left parietals and right parietals, respectively. As with the verbal task, the difference between groups was not significant, F(2,21) = 1.95.

Visual task

Bias scores (Eq. (1)) were calculated for each response hand for each task for all individuals. Data

Discussion

The aim of Experiment 2 was to examine the effects of lateralized motor responses and simpler lateralized auditory tasks on spatial bias in the three groups of participants. The manipulation of response hand had no significant effect on bias. Overall performance on the auditory tasks was much improved in comparison to the performance on the non-spatial and spatial tasks used in Experiment 1, and no significant differences were seen between groups. Spatial bias was seen to be significantly

Acknowledgements

We would like to thank Nagui Antoun for assistance with anatomical selection of patients and Facundo Manes for normalising patients’ MRI scans and tracing their lesions. This work was supported by a Human Frontier Science Program grant (RGP0022/2001-B).

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