Elsevier

Cortex

Volume 45, Issue 4, April 2009, Pages 537-543
Cortex

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Prism adaptation overcomes pseudoneglect for the greyscales task

https://doi.org/10.1016/j.cortex.2007.12.011Get rights and content

Abstract

Visuomotor adaptation to left-shifting prisms can affect performance for a variety of tasks in neurologically intact (normal) participants. This study examined whether visuomotor adaptation affects performance on the greyscales task in normal participants. Forty-two normal participants completed a greyscales task before and after adaptation to either: left-shifting prisms, right-shifting prisms or control spectacles that did not shift the visual scene. Participants demonstrated a leftward bias (i.e., selected the stimulus that was darker on the left as being darker overall) that was reversed by a short period of visuomotor adaptation to left-shifting prisms. In contrast, this bias was unaffected by adaptation to right-shifting prisms and control spectacles. The findings demonstrate that a simple visuomotor task can alter the distribution of spatial attention for the greyscales task in normal participants.

Introduction

Left neglect is an inability to orient toward, explore and respond to stimuli located in the contralesional side of space (Heilman et al., 1993). Patients with left neglect demonstrate a perceptual deficit toward the left side of space, including an unawareness of the left side of space (Rapcsak et al., 1987), a tendency to over-attend to the right-most words on a page (De Renzi et al., 1989), and a distortion of personal space (Guariglia and Antonucci, 1992). This deficit is particularly evident in line bisection tasks, where left neglect patients bisect a line to the right of its veridical midpoint. Neglect is not restricted to stimuli that are physically present, but has also been observed in mental imagery tasks (Bartolomeo et al., 2005) and mental number line bisection tasks (Zorzi et al., 2002).

Despite significant advances in understanding the cognitive and neural bases of neglect, an effective rehabilitation intervention remains elusive. Some methods improve the clinical symptoms of neglect (for example; vestibular stimulation, optokinetic stimulation and attention retraining), but these therapies involve intensive training regimes and their effects are transient. In contrast, a short period of adaptation to right-shifting prisms ameliorates the clinical and everyday symptoms of left neglect for hours to days (Pisella et al., 2006, Frassinetti et al., 2002, Rossetti et al., 1998). Adaptation to right-shifting prisms improves left neglect for explicitly spatial tasks (i.e., tasks with an observable spatial response or coding of stimuli) such as physical line bisection (Rossetti et al., 1998) and for non-explicitly spatial tasks such as mental imagery (Rode et al., 2001), temporal order judgements (Berberovic et al., 2004) and mental number line bisection (Rossetti et al., 2004). Adaptation to right-shifting prisms also ameliorates left neglect for visual-verbal tasks that do not involve a manual response of the limb used during adaptation (Farnè et al., 2002). Neglect is a chronic condition that is difficult to treat and understanding the effects of adaptation is important in the move toward a non-invasive, stable rehabilitation intervention.

Wearing right-shifting prisms causes objects to appear to the right of where they actually are, so that when the wearer first points to an object they miss to the right. Subsequent movements must be adapted if they are to be accurate. Prism adaptation involves two key mechanisms – ‘strategic control’ and ‘spatial realignment’ (Redding et al., 2005). Strategic control is a short-term process whereby initial reaching errors are rapidly detected and reduced. Spatial realignment involves a shift of sensory-motor reference frames so that the felt and seen positions of the moving limb are congruous (Redding and Wallace, 1997). Negative aftereffects (i.e., pointing errors in the direction opposite to the prismatic shift following removal of the prisms) are thought to reflect the amount of spatial realignment that has occurred (Redding and Wallace, 2006), and can be observed within a 5-min adaptation session (Pisella et al., 2006).

It remains unclear how prism adaptation ameliorates left neglect. It has been suggested that the adaptive process promotes the realignment of dysfunctional spatial maps. Adaptation to right-shifting prisms shifts biased egocentric spatial reference frames to the neglected side, correcting the dysfunctional calibration of the task-work space (Rossetti et al., 1998, Redding et al., 2005, Redding and Wallace, 2006). It has also been suggested that adaptation to right-shifting prisms ameliorates left neglect by re-setting ocular scanning behaviour toward the left (neglected) side (Angeli et al., 2004, Serino et al., 2006). Neglect patients demonstrate a rightward ocular-motor orienting bias (compared to normal participants), which is corrected by adaptation to right-shifting prisms (Angeli et al., 2004). The leftward ocular-motor bias following adaptation to right-shifting prisms cannot be explained by visual aftereffects (for a review, see Michel, 2006). Indeed, visual aftereffects occur in the direction of prismatic displacement (for a review, see Kornheiser, 1976), suggesting that changes in ocular pattern cannot be explained by sensorimotor aftereffects, but rather in terms of the reorganization of visuospatial functions.

Where left neglect patients misbisect mental and physical lines to the right, normal participants demonstrate a leftward bias (Nicholls and Loftus, 2007, Nicholls et al., 1999). This leftward bias reflects pseudoneglect, a phenomenon that causes the properties on the left side of a stimulus to be overestimated relative to those on the right (Bowers and Heilman, 1980). Pseudoneglect manifests itself on physical line bisection tasks, where the perceived midpoint of a line is shifted left of the true midpoint (Jewell and McCourt, 2000), but is also observed for judgements of luminance, size, and numerosity (Nicholls et al., 1999) and for mental alphabet lines (Nicholls and Loftus, 2007).

A variety of cognitive and neural mechanisms have been proposed to explain pseudoneglect. Some researchers have focused on the effect of asymmetrical eye movements whereby scans starting on the left lead to an overestimation of the leftward features of the stimulus (Manning et al., 1990). While asymmetries in scanning could be derived from reading habits (Chokron et al., 1998), the evidence appears to favour an attentional account (Manning et al., 1990). Indeed, the fact that pseudoneglect occurs for physical line bisection when overt (McCourt and Olafson, 1997) or covert (McCourt and Jewell, 1999) scanning behaviour is controlled suggests an underlying attentional mechanism (Nicholls and Roberts, 2002). Right hemisphere dominance for attention (Heilman et al., 1987, Mattingley et al., 1992, Spiers et al., 1990) may generate a contralateral attentional bias (see Kinsbourne, 1970) increasing the salience of features in the left hemispace.

Neglect and pseudoneglect are thought to reflect the operation of a common set of cognitive and neural mechanisms (McCourt and Jewell, 1999, Nicholls et al., 2004) and are moderated by similar variables (McCourt, 2001, Nicholls et al., 1999). With this in mind, we explored whether pseudoneglect is affected by prism adaptation in a manner that is analogous to neglect. By demonstrating such an effect, we would establish that the remedial effects of prism adaptation extend beyond disordered maps of attention and also affect spatial mapping in a normally functioning brain.

Pseudoneglect was assessed in the present study using the greyscales task, which requires a forced choice luminance judgement between two mirror-reversed luminance gradients. Normal participants usually select the stimulus that is darker on the left – despite the fact that both stimuli are equiluminant (Nicholls et al., 1999, Okubo and Nicholls, 2006). The greyscales task is highly sensitive to lateral asymmetries in attention and allows us to examine the effects of adaptation on a purely perceptual task where there is no manual response and where the coding of the stimuli (upper/lower) is orthogonal to the dimension of interest (left/right). Therefore, if an effect of adaptation is observed, it must relate to a remapping of the stimulus rather than the required response. That is, since the greyscales task does not require any manual response, any effects of prism adaptation must go beyond relatively low-level congruencies in the mapping of the stimulus with reference to body coordinates and/or the response. The present study also sought to control eye scanning by presenting greyscales stimuli for 200 msec and requiring central fixation in between trials.

Previous research has revealed an asymmetric effect of prismatic adaptation in both normal participants and left neglect patients. Left-shifting prisms do not affect bisection judgements in left neglect (Rossetti et al., 1998, Rossetti et al., 2004) and right-shifting prisms do not affect bisection judgements in normal participants (Berberovic and Mattingley, 2003, Colent et al., 2000). This suggests that there is an inherent asymmetry in the mechanisms that link adaptation and spatial cognition, causing the two hemispheres to be differentially engaged during adaptation (Colent et al., 2000, Vallar et al., 1999). In light of these findings, we predicted that pseudoneglect would be corrected by 15° left-shifting prisms, but not by right-shifting prisms.

Section snippets

Participants

Forty-two neurologically intact, right-handed undergraduate students participated in the study (8 male, mean age 21 years). Fourteen participants were adapted to left-shifting prisms (3 male, mean age 20.71 years, SD = 2.46), 14 to right-shifting prisms (3 male, mean age 20.64 years, SD = 2.82) and 14 participants were exposed to control spectacles with no lateral shift (2 male, mean age 20.36 years, SD = 2.79). All had normal vision or corrected to normal vision. The study was approved by the

Negative aftereffects

All participants successfully adapted within 50 pointing trials. Inspection of the relative data (where direction is coded) demonstrated rightward negative aftereffects (M = 4.67°, SE = .41) for the left-shifting group and leftward negative aftereffects (M = 2.71°, SE = .74) for the right-shifting group. The control group was consistently accurate in their pointing (i.e., 0° from both targets). A t-test comparing negative aftereffects with zero (no negative aftereffects) revealed a significant

Discussion

Participants demonstrated pseudoneglect for the greyscales task by selecting the greyscale that was darker on the left as being darker overall. This leftward bias was reversed by adaptation to left-shifting prisms, but was unaffected by the same level of adaptation to right-shifting prisms. The asymmetric effect of prisms is consistent with previous studies with normal participants (Michel et al., 2003;, Berberovic and Mattingley, 2003, Colent et al., 2000) and in neglect populations (

Conclusion

In conclusion, the current study demonstrates that the leftward attentional bias that occurs in the normally functioning brain can be overcome by left-shifting prisms. The effect of prismatic adaptation on pseudoneglect appears to be a mirror analogue of what occurs in neglect populations (e.g., Rossetti et al., 1998, Rossetti et al., 2004). This research therefore supports the suggestion that neglect and pseudoneglect are twin manifestations of a common set of cognitive and neural mechanisms (

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