Elsevier

Neuropsychologia

Volume 50, Issue 11, September 2012, Pages 2573-2576
Neuropsychologia

Testing the activation–orientation account of spatial attentional asymmetries using transcranial direct current stimulation

https://doi.org/10.1016/j.neuropsychologia.2012.07.003Get rights and content

Abstract

The general population shows an attentional bias to the left, known as pseudoneglect. This bias is thought to be driven by higher levels of activation in right parietal areas. Using transcranial direct current stimulation (tDCS) to manipulate activation, this study examined whether tDCS over the left and right posterior parietal cortices (PPC) affects pseudoneglect. Normal participants received tDCS over the left or right PPCs (15 in each group). Pseudoneglect was measured using the greyscales task, which requires a forced-choice discrimination of luminance between two opposing luminance gradients. The greyscales task was administered both before and after; (a) anodal (b) cathodal and (c) sham tDCS. Participants who received tDCS over the left PPC demonstrated pseudoneglect for the greyscales task, which was significantly reduced by anodal tDCS, but was unaffected by sham or cathodal tDCS. In contrast, for those participants who received right PPC tDCS, pseudoneglect for the greyscales task was unaffected by tDCS. Anodal tDCS, which is known to elevate neural excitation, may have overcome lower levels of activation in the left PPC, resulting in decreased pseudoneglect. These findings provide convincing evidence in support of an activation–orientation model of pseudoneglect and have implications for models of left neglect.

Highlights

► Examined if tDCS over the posterior parietal cortices (PPC) affects pseudoneglect. ► Pseudoneglect was measured before and after anodal, cathodal and sham tDCS. ► Pseudoneglect was significantly reduced by anodal tDCS over the left PPC. ► Pseudoneglect was unaffected by sham and cathodal tDCS of left PPC. ► Pseudoneglect was unaffected by anodal, sham and cathodal tDCS of right PPC. ► Findings support of an activation–orientation model of Pseudoneglect. ► Implications for models of left neglect are considered.

Introduction

Where left neglect patients demonstrate a rightward attentional bias (Heilman, Watson, & Valenstein, 1993), neurologically intact adults demonstrate a leftward attentional bias, referred to as ‘pseudoneglect’ (Nicholls et al., 1999, Nicholls and Loftus, 2007). Although less extreme than clinical neglect, Pseudoneglect is a reliable tendency to overestimate the features on the left side of a stimulus relative to the right and manifests on physical line bisection tasks (Jewell & McCourt, 2000), judgements of luminance, size and numerosity (Nicholls et al., 1999), and the mental representation of numbers (Loftus, Nicholls, Mattingley, & Bradshaw, 2008) and letters (Nicholls & Loftus, 2007).

Given the performance similarities (McCourt & Jewell, 1999) and the mutual involvement of the right posterior parietal cortex (PPC) (Foxe et al., 2003, Waberski et al., 2008), many accounts of pseudoneglect mirror models of neglect. The activation–orientation account suggests that spatial attention is biased in the direction opposite to the most activated hemisphere (Kinsbourne, 1970, Kinsbourne, 1987, Kinsbourne, 1993, Reuter-Lorenz et al., 1990). Neuroimaging studies demonstrate preferential activation of the right PPC during visuospatial tasks (Fink et al., 2002, Foxe et al., 2003, Harris and Miniussi, 2003, Göbel et al., 2006). In accord with an activation–orientation account, preferential activation of the right PPC during visuospatial tasks leads to a leftward attentional bias, which increases the salience of features in the left hemispace. In the case of physical line bisection, the left side of the line is subsequently perceived to be longer than the right, resulting in a leftward shift in the perceived midpoint of the line (Bultitude & Davies, 2006).

Siman-Tov et al. (2007) proposed a revised activation–orientation model, in which pseudoneglect and neglect are explained in terms of asymmetric interhemispheric neural activation and connectivity. Neuroimaging experiments in which participants completed visual attention tasks revealed a left visual field advantage, which Siman-Tov et al. suggested originates from two distinct neural mechanisms. First, that advantageous connectivity within the right hemisphere facilitates its dominance for spatial attention. Second, that connectivity between the two hemispheres favours the passage of information from the right to the left hemisphere. This account therefore suggests that a right hemisphere advantage for spatial attention, coupled with a strong right-to-left interhemispheric transfer of information, leads to a leftward bias of spatial attention.

The present study tested the effect of unilateral hemispheric activation proposed in the models by Kinsbourne, 1970, Kinsbourne, 1987, Kinsbourne, 1993 and Siman-Tov et al. (2007) using transcranial direct current stimulation (tDCS). This relatively recent technique is a non-invasive method of brain stimulation that can be used to modulate cortical excitability. When applied to the skull, tDCS penetrates the underlying cortex and increases (anodal) or decreases (cathodal) cortical excitability in that area (Lang et al., 2011, Nitsche and Paulus, 2000, Zaghi et al., 2010).

Studies using tDCS have shown altered visual detection in healthy controls and left neglect patients (Sparing et al., 2009). In healthy controls, anodal tDCS over the PPC improved visual detection in the contralateral visual field and cathodal tDCS over the PPC improved performance in the ipsilateral visual field. For left neglect patients, anodal tDCS over the lesioned PPC and cathodal tDCS over the unlesioned PPC reduced left neglect on a physical line bisection task. Based on these findings, the authors suggested that tDCS modulates visual attention by reducing interhemispheric imbalance.

In the present study, pseudoneglect was assessed using the greyscales task, which requires a forced choice luminance judgement between two mirror-reversed luminance gradients. Neurologically intact participants typically select the stimulus that is darker on the left (Nicholls et al., 1999, Okubo and Nicholls, 2006). The greyscales task is highly sensitive to spatial biases of attention and allows us to examine the effects of tDCS on a purely perceptual task. The techniques associated with tDCS are still a developing science (Jacobson, Koslowsky, & Lavidor, 2012) and exact predictions are difficult to make. It is possible that tDCS will have symmetrical effects on the hemispheres. That is, cathodal and anodal stimulation will excite and inhibit (respectively) neural activity—resulting in systematic increases and decreases in pseudoneglect for left and right tDCS. However, given that activation techniques, such as visual spatial cueing (Nicholls and Roberts, 2002, Sosa et al., 2011) and prismatic adaptation (Loftus et al., 2008) often only affect left hemisphere activity, we predicted that stimulation over the left PPC was more likely to have an effect than stimulation over the right PPC. In addition, tDCS itself appears to have differential effects, with anodal (excitatory) stimulation more likely to yield an effect on cognitive tasks than cathodal (inhibitory) stimulation (Jaconson et al., 2012). Therefore, if unilateral activation affects asymmetries in attention, we predicted that increased excitation of the left PPC (using anodal tDCS) should equalise hemispheric activation and reduce pseudoneglect for the greyscales task.

Section snippets

Participants

Thirty neurologically intact, right-handed (in accord with the Edinburgh Handedness Inventory, Oldfield, 1971) undergraduate students took part in the study (6 males, mean age 26 years). All participants had normal or corrected to normal vision. The study was approved by a University human ethics committee and was performed in accord with the 1964 Declaration of Helsinki.

Materials and methods

Participants were randomly assigned to one of two stimulation groups: (i) left PPC or (ii) right PPC (15 each group). All

Results

All participants successfully completed the experiment and there were no missing data. For each trial, participants selected the stimulus that was darker on the left or the right, classified as ‘left’ and ‘right’ responses, respectively. A measure of bias for the greyscales task was calculated by subtracting the number of left responses from the number of right responses and converting the result into a percentage. Bias scores could therefore range from −100% to +100% with negative and positive

Discussion

Participants demonstrated pseudoneglect for the greyscales task by selecting the greyscale that was darker on the left as being darker overall, regardless of group inclusion. This leftward bias is consistent with other studies using the greyscales task (Nicholls et al., 1999, Okubo and Nicholls, 2006). Pseudoneglect was significantly reduced following 20 min of anodal tDCS over the left PPC, but remained unaffected by cathodal or sham tDCS over the left PPC. This leftward bias was also

References (29)

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