Pseudoneglect in line bisection judgement is associated with a modulation of right hemispheric spatial attention dominance in right-handers
Introduction
Hemispheric specialization (HS) is a fundamental principle in the functional organization of the human brain (Hervé et al., 2013). In most humans, the left hemisphere is specialized for language, praxis and motor control of the dominant hand, whereas the right hemisphere is more dedicated to the control of visuospatial skills and spatial attention (Heilman et al., 1993, Karnath and Rorden, 2012, Kinsbourne, 1970a, Mazoyer et al., 2014, Mesulam, 1999). However, this is not an invariable principle. For example, there are occasional patients with aphasia after right hemispheric lesions or with neglect after left hemispheric lesions (Coppens et al., 2002, Dronkers and Knight, 1989, Suchan and Karnath, 2011). Although the variability of cerebral lateralization for language has been extensively studied in healthy participants (Josse and Tzourio-Mazoyer, 2004, Tzourio et al., 1998), right hemispheric dominance has been considered a poor relation of hemispheric specialization. To our knowledge, there is no “gold standard” for assessing hemispheric spatial dominance, such as the Wada test (Wada and Rasmussen, 1960) that remains the gold standard for assessing individual language lateralization in preoperative patients. More recently, functional magnetic resonance imaging (fMRI) has been shown to be a valid non-invasive alternative to Wada testing to assess functional language lateralization (see for reviews Binder, 2011; Dym et al., 2011). Regarding the cerebral dominance of spatial attention, studies are scarce. Jansen et al. (2004) compared functional transcranial Doppler sonography (fTCD) to fMRI measures during a landmark task in which subjects judged the accuracy of line bisections and demonstrated that both techniques were able to concordantly determine visuospatial hemispheric lateralization in healthy participants (Jansen et al., 2004).
To explore the factors that could explain the variability of spatial cerebral lateralization with fMRI, it is important to first verify whether the spatial attentional task fulfils several conditions in a sample of right-handed healthy participants.
A first condition that must be fulfilled is that the spatial attention task that is used to investigate spatial cerebral lateralization should elicit behavioural asymmetry. An example of a task that induces free-viewing behavioural asymmetries is the well-known “paper and pencil” line bisection task. This task requires the subject to mark the apparent midpoint of a long horizontal line drawn on a sheet of paper. Whereas some right hemispheric brain-injured patients bisect lines far to the right of the true midline (Doricchi and Angelelli, 1999, Sperber and Karnath, 2016), neurologically intact subjects tend to systematically err to the left of centre, a phenomenon first referred by Bowers and Heilman as pseudoneglect (Bowers and Heilman, 1980). The misbisection to the left, although not as pronounced as the rightward bias observed in patients, appears to be a reliable phenomenon (Jewell and McCourt, 2000, see however Manning et al., 1990 for a report of important between-subjects variations in the direction of pseudoneglect). One hypothesis is that this leftward asymmetry may be the result of an attentional bias directed towards the left hemispace, arising from asymmetries in hemispheric activation, with a right hemisphere involvement in visuospatial attention (Kinsbourne, 1970a, Mesulam, 1999, Nicholls and Roberts, 2002). Due to the constraint that the subject must remain still during fMRI scanning, the classical “paper and pencil” line bisection task is difficult to set up, so usually a perceptual variant, called the landmark task is used, where the subjects decide the accuracy of line bisections (Fink et al., 2002). In a previous study, we designed a line bisection judgement (LBJ) task during which the participant was asked to judge if a bisection mark was located at the centre of a horizontal line or if it slightly deviated to the left or right of the midline. A spatial deviation bias based on the errors was computed for each individual, and the results demonstrated that the subjects more frequently erroneously judged that the vertical segment was deviated to the left of the true bisection, consistent with pseudoneglect (Zago et al., 2015). In the present experiment, we modified both the stimuli and design to verify whether this error bias was robust and not linked to the experimental parameters.
Another point that needs to be investigated is whether the LBJ attentional bias is specific to the task or related to other attentional biases in healthy participants. For example, the cancellation task, where the participant is asked to mark target items in a cluttered array of distractors, is another popular paper-and-pencil method for assessing spatial neglect (Weintraub and Mesulam, 1985). Although this task also elicits a rightward behavioural bias in neglect patients, some studies have shown that these two biases may dissociate, with patients showing specific deficits in line bisection but not in cancellation and vice versa (Binder et al., 1992, Ferber and Karnath, 2001). In addition, some of the regions critical for accurate cancellation performance are not required for unbiased bisection (Rorden et al., 2006; but see Molenberghs and Sale, 2011). This dissociation has been confirmed in healthy people, with the engagement of different neural networks according to the type of attentional task (visual search vs. bisection) (Revill et al., 2011). Here, we used the “paper and pencil” symbol cancellation task (SCT) to evaluate the cancellation bias based on the centre of cancellation score (CoC, Rorden and Karnath, 2010) and investigated the relationship between both biases.
Furthermore, in accordance with the hypothesis that pseudoneglect is associated with a right hemispheric dominance for spatial attention (Bowers and Heilman, 1980), the behavioural bias might be related to the cerebral asymmetry found during the LBJ task. For example, Szczepanski and Kastner (2013) demonstrated brain-behaviour correlation such that an individual's behavioural spatial bias, as measured using the landmark task, can be predicted by the degree of lateralization of the frontoparietal cortex (Szczepanski and Kastner, 2013). We also found such a relation between the LBJ bias and hemispheric lateralization in right- and left-handers (Zago et al., 2015). In the present study, we verified whether this association was also found in our sample of right-handers and whether it was specific to LBJ or related to the CoC measured during the “paper and pencil” cancellation task. In addition, one of the critical questions in cognitive neuroscience is how the variability in the functional organization of the human brain affects cognitive performance. In the language domain, it has been shown that, although healthy adults weakly lateralized for language performed lower on language or visuospatial tests than typical left-lateralized subjects, no correlation existed between the cerebral lateralization for language and performance (Mellet et al., 2014). In contrast, in children, some studies have demonstrated an association between the strength of cerebral lateralization and performance in language and visuospatial domains (Everts et al., 2009, Groen et al., 2012). Here, we assessed whether spatial cerebral lateralization could be linked to visuospatial skills in adults.
The spatial attention task should produce functional asymmetries linked to spatial attention processes involved in the task and should not be driven by other parameters that are known to elicit asymmetries, such as motoric responses, eye movement activity and visual attention shifting (Petit et al., 2014; Petit et al., 2009; Shulman et al., 2010). Consequently, the spatial attentional task should be compared to a control task that controls for low level perceptual activities and eye and hand motor activities performed during the attentional task. In addition, these functional asymmetries should be evaluated by statistical methods, using the reliable laterality index (LI) that provides quantitative information about hemispheric lateralization (Wilke et al., 2007) and voxel-wise comparisons of the magnitude of activation in the two hemispheres to yield a statistically valid regional asymmetric pattern (Liégeois et al., 2002, Stevens et al., 2005, Zago et al., 2015). Although they did not include such analyses, the first studies that used the landmark task in right-handers evidenced the involvement of a large network, including the frontal, parietal, temporal and occipital areas, in which activation tended to be predominant in the right hemisphere (Ciçek et al., 2009, Fink et al., 2000, Fink et al., 2001).
Finally, another important condition that the spatial task should fulfil is that the pattern of regional fMRI asymmetry observed during LBJ in healthy participants should be consistent with the pattern of lesions of neurological stroke patients who exhibit bisection bias (Corbetta et al., 2005; Rorden et al., 2006). Here, we investigated this issue by comparing the asymmetric brain regions of healthy participants to the brain lesions of stroke patients showing line bisection deficits, as reported by Rorden et al. (2006).
The aim of the present study was to validate the use of the LBJ task to adequately investigate the lateralized cerebral bases of spatial attention. We assessed 1) whether the LBJ task elicited a behavioural spatial attention bias and whether this relationship was observed with another attentional deviation bias, such as cancellation bias; 2) whether the LBJ task produced reliable cerebral functional asymmetries related to LBJ mechanisms, as assessed by the hemispheric lateralization index (HFLI) and regional functional asymmetry analyses computed from BOLD-fMRI images acquired during a LBJ task compared to a visuomotor control task; 3) whether the spatial cerebral asymmetry was related to the LBJ behavioural bias and whether this relationship was specific to LBJ or also found with cancellation bias, and we also explored the association between LBJ cerebral lateralization and visuospatial skills; 4) and whether the functional asymmetry pattern measured during the LBJ task was consistent with the lesion map of neurological stroke patients showing deficits regarding line bisection compared to patients without such a deficit (Rorden et al., 2006).
A second objective of this study was to re-test the absence of the association between the cerebral lateralization for language and for spatial processing that we previously reported in right-handers who performed a language production task and LBJ task (Zago et al., 2015). Here, we verified whether this absence of a relation between cerebral lateralization was also observed with another component of language, such as speech listening (Tzourio et al., 1998), which, as the LBJ task, puts more demand on perceptual processing within each domain.
Section snippets
Participants
Fifty-one right-handed healthy volunteers (25 women, 26 men) as assessed using the Edinburgh handedness questionnaire (+90±15; mean±SD; Oldfield, 1971) were included in the present study. The mean age of the entire sample was 28 years (SD=7 years). All gave their informed, written consent and received an allowance for their participation. A local Ethics Committee (CCPRB Basse-Normandie, France) approved the experimental protocol. All subjects were free of brain abnormalities, which were
Line Bisection Judgement
Performance was high during LBJ (76.9±7.6% correct), and participants responded within an average of 1.0 s (±0.1 s). The error spatial attentional bias was negative on average (mean: −2.6; SD: 6.1, one sample t-test: t(50)=−3.09, p=0.003), indicating that participants produced more errors deviated to the left, consistent with a “pseudoneglect effect” (Bowers and Heilman, 1980). For the leftward errors, the condition that gathered most of the errors was when the subjects answered ‘middle’ for
Discussion
The aim of the present study was to investigate whether the LBJ task met the conditions required to adequately investigate the lateralized cerebral bases of spatial attention and to be afterwards used to determine the factors of variability of spatial cerebral lateralization.
First, the LBJ task designed in the present experiment allowed for the assessment of behavioural attentional bias based on the errors that participants made to judge of the position of the vertical segment. Globally,
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Now at Laboratory for the Psychology of Child Development and Education, CNRS Unit 8240, Paris-Descartes University and Caen University, F-75005, Paris, France.