Elsevier

Cortex

Volume 49, Issue 1, January 2013, Pages 120-130
Cortex

Research report
Prismatic adaptation effects on spatial representation of time in neglect patients

https://doi.org/10.1016/j.cortex.2011.11.010Get rights and content

Abstract

Processing of temporal information may require the use of spatial attention to represent time along a mental time line. We used prismatic adaptation (PA) to explore the contribution of spatial attention to the spatial representation of time in right brain damaged patients with and without neglect of left space and in age-matched healthy controls.

Right brain damaged patients presented time underestimation deficits, that were significantly greater in patients with neglect than in patients without neglect. PA inducing leftward attentional deviation reduced time underestimation deficit in patients with neglect.

The results support the hypothesis that a right hemispheric network has a role, per se, in time perception. Moreover, they suggest that right hemisphere is important in time perception for its control of spatial attention, engaged in spatial representation of time. Procedures that ameliorate left spatial deficits could also be useful for modulating temporal deficits in right brain damaged patients with neglect.

Introduction

Recent neuroscientific literature suggested the existence of a direct link between time perception and spatial attention. Based on the hypothesis that time is spatially represented (Walsh, 2003, Bueti and Walsh, 2009) onto a mental time line (MTL) oriented in ascending order from left to right (Ishihara et al., 2008, Vallesi et al., 2008), previous studies showed a lateralized distortion of time intervals following a lateralized manipulation of spatial attention (Vicario et al., 2007, Vicario et al., 2008). In a previous study, taking advantage of a procedure widely used to induce a shift of spatial attention (namely, Prismatic adaptation – PA), we demonstrated a time underestimation or overestimation following leftward and rightward attentional shifts, respectively (Frassinetti et al., 2009). In a group of young healthy subjects prisms inducing a leftward attentional shift, affected time perception toward an underestimation. Prisms inducing rightward attentional shift, caused an opposite pattern of temporal overestimation.

An interesting model to study the link between spatial attention and time representation is constituted by patients with visual spatial neglect. Indeed, neglect patients, after a lesion of the right hemisphere, show a deficit in orienting spatial attention toward the controlesional space (i.e., the left hemispace) and a severe attentional bias toward the ipsilesional space (i.e., the right hemispace) (Husain and Rorden, 2003, Mesulam, 1999, Driver and Mattingley, 1998). In addition to spatial deficits, time perception deficits have been described in neglect patients (Basso et al., 1996, Becchio and Bertone, 2006, Danckert et al., 2007, Oliveri et al., 2009). Danckert and colleagues (2007) investigated time perception in a group of neglect patients compared with a group of right brain damaged patients (RBD) without neglect (RBD-N−) and a group of healthy controls (HC). All subjects had to estimate the time of an illusionary motion stimulus presented on the center of the screen. Neglect patients showed greater underestimation of time intervals compared to both RBD patients and HC; RBD patients slightly underestimated time intervals compared with HC. However, these Authors interpreted the greater underestimation of time intervals showed by neglect patients with respect to RBD patients suggesting that time impairment is an epiphenomenon of the neglect syndrome.

The rightward bias of spatial attention in neglect patients can be reduced by means of one session of PA (Rossetti et al., 1998, Farné et al., 2002; for a review see Rode et al., 2003). Recently, the effects of prismatic lenses on time were studied in RBD-N− and in age-matched healthy controls (Magnani et al., 2011). PA inducing leftward attentional deviation biased time perception in RBD-N− patients and in controls, while PA inducing a rightward attentional deviation failed to affect time perception in either groups. However the effects of prismatic lenses on time perception in RBD patients with neglect (RBD-N+) were never investigated.

A first aim of this study is to investigate the impact of a spatial attention deficit following a right hemispheric stroke on the spatial representation of time. A second aim is to assess if a reduction of the spatial attention deficit by means of PA is able to ameliorate the spatial representation of time in RBD patients with neglect (RBD-N+). RBD-N+, RBD-N− and age-matched healthy controls, were submitted to a time bisection task, before and after a single session of PA. PA inducing a leftward attentional shift was chosen for two reasons: first, according to the side of PA used for the rehabilitation of spatial deficit in neglect patients; second, considering the lack of effect of PA inducing a rightward attentional shift on time in brain damaged patients in our previous study (Magnani et al., 2011). Since RBD patients, regardless of the presence of neglect, are often impaired in temporal tasks (Basso et al., 1996, Danckert et al., 2007, Koch et al., 2002), we expect to replicate the result of a compromised performance of both RBD-N+ and RBD-N− (i.e., underestimation of time) in the time task compared to HC. Indeed, a crucial involvement of the right, rather than the left, hemisphere in controlling time perception is well established in the literature (Harrington et al., 1998, Koch et al., 2002, Koch et al., 2003, Lewis and Miall, 2006, Oliveri et al., 2009). In a pioneer neuropsychological work, Harrington and colleagues (1998), showed that right- but not left brain damaged patients had time perception deficits. Moreover, by analyzing patients’ lesions, authors found an involvement of a fronto-parietal network suggesting that this circuit of the right hemisphere is the locus of timekeeping operations. Following studies corroborated this suggestion. Koch and colleagues (2002), described a patient with a right prefrontal lesion presenting an underestimation of time compared to a group of healthy controls. They also found a similar result of an underestimation of time after disruption of the right, but not the left, dorsolateral prefrontal cortex by using TMS in a group of healthy subjects. Similarly, Oliveri and colleagues (2009) showed a significant underestimation of time in patients with right brain damage and in healthy subjects after the inhibition by TMS of the right, but not the left, posterior parietal cortex. Such results suggest that a right fronto-parietal network is directly involved in timekeeping functions and it is probably connected with the internal pacemaker system with the role of creating and processing the cognitive representation of time. However, the attempt of the present study is to go beyond the general role of the right hemisphere in time, focusing on the possible and peculiar influence of spatial attention on the representation of time. In this regard, if spatial attention actually plays a role in shaping the spatial representation of time, RBD-N+ are expected to be more impaired on the time task compared to RBD-N− and HC. Concerning the effects of PA on time perception deficit in neglect patients, if PA can actually ameliorate spatial representations, we expected a reduction of the impairment in the spatial representation of time in RBD-N+ patients after PA (A-PA) compared to before PA (B-PA) in the time bisection task.

Section snippets

Participants and neuropsychological assessment

Twenty patients with unilateral right brain damage, ten with neglect (RBD-N+, 3 male; mean age = 69.8 years; SD = 8.3 years; mean education = 7 years) and ten without neglect (RBD-N−, 7 male; mean age = 71.1 years; SD = 8.3 years; mean education = 8.5 years) and ten participants without history of neurological or psychiatric disease (3 male, mean age = 60.7 years; SD = 7.8 years; mean education = 9.1 years) gave their informed consent to participate in the study, which was approved by the local

Time bisection task

Performance in the time bisection task was calculated for each subject. First, how HC, RBD-N− and RBD-N+ patients performed the temporal task B-PA was verified (see Supplementary Materials). Second, performance B-PA and A-PA was compared in order to investigate the effects of PA on time bisection task in each group. The dependent measure was the mean (in milliseconds) of reproduced intervals. Reproduced time intervals longer than the encoded ones were interpreted as time underestimation;

Discussion

There are two aspects to the main results of the present study. The first concerns the consequence of a deficit of spatial attention following a brain lesion on the spatial representation of time; the second concerns the effects of PA on spatial representation of time. About the first point, the presence of a spatial attention deficit worsens the temporal deficit emerging following right brain damage. Indeed, RBD-N− patients underestimated time with respect to healthy controls. Moreover, RBD-N+

Acknowledgments

This work was supported by grants from RFO (Ministry of University and Research) to Francesca Frassinetti.

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