Effects of prismatic adaptation on spatial gradients in unilateral neglect: A comparison of visual and auditory target detection with central attentional load
Introduction
Spatial neglect is a common consequence of unilateral stroke, particularly when the lesion affects the right cortical hemisphere (Driver and Mattingley, 1998, Stone et al., 1993). This syndrome is characterised by reduced awareness for stimuli arising from the contralesional side of space, despite intact sensory functioning. The deficit is thought to reflect damage to internal representations of contralesional space (Bisiach and Luzzati, 1978, Karnath et al., 1998) and a pathological ipsilesional bias in spatial attention (Kinsbourne, 1993). This lateralised impairment can affect patients’ perception of stimuli in any modality, including vision, audition (see Pavani, Husain, Ladavas, & Driver, 2004) and tactile processing (e.g., Guerrini et al., 2003, Schindler et al., 2006, Vallar et al., 1994). The presence of neglect is a major predictor of poor functional recovery; furthermore, it is accompanied by profound unawareness of the deficit, which is a major obstacle to rehabilitation and recovery (Vuilleumier, 2004). Over the past decade, prism adaptation has emerged as a potentially effective therapy for reducing neglect across a range of attentional tasks and behavioural measures, with improvements lasting several hours and, in some studies, days or weeks (Frassinetti et al., 2002, Rossetti et al., 1998, Serino et al., 2006).
Prism adaptation is achieved by a brief period of pointing to visual targets while wearing prism lenses that laterally shift the visual field towards the right side by 10–15°. Initially, the prism-induced shift in the visual field causes participants (including neglect patients) to make rightward errors in pointing to the visual target. With subsequent pointing movements, participants compensate for the shift and these errors are abolished. Once the prism lenses are removed, participants demonstrate a temporary bias (or aftereffect) in visually guided pointing, and in their proprioceptive judgement of a point straight ahead. This aftereffect is in the opposite direction to the prism-induced shift (i.e., toward the left following adaptation to right-shifting prisms). Patients with left spatial neglect following right hemisphere stroke respond only to adaptation with right-shifting prisms that induce a leftward aftereffect in pointing movements (Rossetti et al., 1998, Tilikete et al., 2001). This leftward bias in pointing appears to generalise to patients’ attentional performance, as the initial motor effect is outlasted by a reduction in patients’ ipsilesional (rightward) bias on unrelated spatial tasks such as cancellation and line bisection (e.g., Farne et al., 2002, Frassinetti et al., 2002, Rossetti et al., 1998, Sarri et al., 2008, Serino et al., 2006). Although tasks such as these involve a motor component, there is evidence from a number of studies that prism adaptation can affect patients’ attentional bias on a range of purely perceptual tasks (Berberovic et al., 2004, Striemer and Danckert, 2007) as well as on tasks of mental imagery and mental number line judgments (Rode et al., 2001, Rossetti et al., 2004). This suggests that the initial visuo-motor aftereffect induced by adaptation transfers to functions of spatial attention (Pisella et al., 2006, Redding et al., 2005). Indeed, it has been postulated that prism adaptation may act on higher spatial cognitive functions by the enlargement of contralesional spatial representations (Redding & Wallace, 2006), and ‘rebalancing’ of the pathological ipsilesional spatial gradient of attention (Pisella et al., 2006). Although there is accumulating positive evidence for the efficacy of prism adaptation, not all manifestations of neglect improve with this treatment (Ferber et al., 2003, Morris et al., 2004, Nijboer et al., 2008, Sarri et al., 2006), and there is evidence that some patients may not respond to prism adaptation (Sarri et al., 2008). In the present study we examined the effects of prism adaptation on visual and auditory spatial biases in neglect, using procedurally identical visual and auditory versions of a task that measured patients’ attentional gradient for detecting brief peripheral stimuli.
It remains controversial as to whether prism adaptation directly influences the spatial bias (or gradient) in attention underlying neglect (Newport and Jackson, 2006, Pisella et al., 2006, Redding and Wallace, 2006), or whether it acts on related aspects of neglect behaviour, such as exploratory eye movements (Angeli et al., 2004, Ferber et al., 2003, Serino et al., 2006). Unilateral spatial neglect is not a hemifield-based deficit, but instead reflects increasingly reduced awareness for stimuli that are positioned at relatively more contralesional locations in space (Bartolomeo et al., 2004, Halligan and Marshall, 1991, Kinsbourne, 1993; although see Karnath et al., 1998). Thus, patients show a spatial gradient in their visual awareness, with latency and accuracy for detecting visual stimuli worsening as a function of the target's eccentricity towards the contralesional side. This graded performance of neglect patients is exacerbated by increasing the attentional demands of a visual search task (e.g., Eglin et al., 1989, Riddoch and Humphreys, 1987), and also when patients have to perform a secondary attentional load task at fixation while monitoring peripheral space for brief visual targets (Mattingley, Berberovic, Rorden, & Driver, 2003).
Empirical evidence for the effect of prism adaptation on tasks that explicitly assess biases in spatial attention has been somewhat mixed. Morris et al. (2004) examined the effects of prism adaptation on a speeded visual search task that excluded any manual component typical of cancellation tasks. In this task, participants reported the presence or absence of a single target in an array of distractors, within a limited time period. Neglect patients demonstrated a significant spatial gradient of performance on this task. Following prism adaptation, patients demonstrated significant leftward aftereffects on their proprioceptive judgment of straight ahead, and most showed changes in their performance on a line bisection task, but there was no change in their spatial gradient of attention on the visual search task. It was suggested that the effects of prism adaptation on neglect might not reflect changes in the spatial attention bias underlying the disorder. A similar finding was reported for speeded visual search in a recent study (Saevarsson, Kristjansson, Hildebrandt, & Halsband, 2009). However, in a follow-up experiment involving different patients and a visual search task that was not time limited and did not include feedback about performance, significant increases in left sided target detections were found post-prism adaptation. The authors suggest that the provision of feedback may lead to ‘de-adaptation’. Another possibility is that extended search time may have allowed ocular exploration to contribute more to search performance.
Neglect is also associated with deficits in re-orienting or disengaging attention from ipsilesional stimuli (Posner, 1980). Studies that have investigated the effect of prisms on reflexive re-orienting to peripheral stimuli have produced conflicting results. Striemer and Danckert (2007) reported that right brain damaged patients with right disengage deficits on a Posner cueing task (using exogenous cueing), were faster to reorient from a right cue to a left target following a single session of prism adaptation. In contrast, a recent study that also investigated prism effects on the exogenous cueing version of the Posner task, found improvements across two baseline testing sessions but not following prism adaptation (Nijboer et al., 2008). Interestingly, the same patients demonstrated prism-induced improvements on the Posner task with endogenous cueing. The authors suggested that the effect of prism adaptation on neglect symptoms might occur primarily through improvements in voluntary orienting, rather than by influencing patients’ automatic orienting to peripheral onsets. Certainly, the majority of positive prism effects have been seen in non time-limited tasks, including paper-and-pencil tests, which might allow voluntary exploratory behaviours to compensate for attentional biases. Also, several studies have reported that neglect patients’ ipsilesional bias in ocular exploratory movements shifts to the neglected side following prism adaptation, and that such oculo-motor changes correlate with improvements on clinical neglect tasks following prism adaptation (Angeli et al., 2004, Serino et al., 2006). Nevertheless, patients may continue to show deficits on some attentional tasks, such as the judgement of chimeric faces, despite a leftward shift in exploratory eye movements (Ferber et al., 2003).
As previously mentioned, neglect can affect patients’ perception of stimuli in any sensory modality (e.g., Guerrini et al., 2003, Pavani et al., 2004, Schindler et al., 2006, Vallar et al., 1994). Although prism adaptation is known to influence a variety of different spatial processing tasks, the generality of its effect on spatial processing is not clear because most of the tasks used to date have concerned visual (e.g., Berberovic et al., 2004, Bultitude et al., 2009, Farne et al., 2002, Frassinetti et al., 2002, Nijboer et al., 2008, Rossetti et al., 1998, Saevarsson et al., 2009, Serino et al., 2006, Striemer and Danckert, 2007), proprioceptive (Tilikete et al., 2001) or tactile modalities (Dijkerman et al., 2004, Maravita et al., 2003, McIntosh et al., 2002) – which are directly involved in the visuo-manual procedure required for adaptation. To determine whether prism effects are restricted to the visual and somatosensory systems, or whether they reflect higher-level changes in spatial attention, it is necessary to determine whether prism adaptation can ameliorate spatial neglect symptoms in a sensory system that is not directly involved in adaptation – in this case, audition. Auditory symptoms of neglect can manifest in a number of ways, such as auditory extinction (De Renzi et al., 1984, Deouell and Soroker, 2000, Karnath et al., 2002, Shisler et al., 2004), contralesional deficits in sound lateralization or localisation (Bisiach et al., 1984, Pavani et al., 2001, Pavani et al., 2002, Pavani et al., 2004), and biased judgment of the temporal order of auditory stimuli (Karnath et al., 2002). Also, we have previously demonstrated that neglect can manifest as an ipsilesional attentional gradient on both auditory and visual search tasks (Eramudugolla & Mattingley, 2009).
The effect of prism adaptation on auditory processing was recently examined for the first time (Jacquin-Courtois et al., 2010). In this study, the authors found that neglect patients who received prism adaptation significantly improved performance on a dichotic listening task compared with patients who underwent sham treatment with non-prismatic lenses. The dichotic listening task in their study involved patients listening to simultaneous pairs of spoken words, with each word presented monaurally to either the left or right ear. On each trial, patients were required to divide their attention between the left and right stimuli and to repeat both words. Neglect patients in both the control and experimental groups showed reduced accuracy for repeating contralesional relative to ipsilesional words. A single session of prism adaptation increased the accuracy of contralesional compared to ipsilesional word repetition, showing that visuo-motor adaptation ameliorates auditory extinction in neglect. However, the dichotic task employed by Jacquin-Courtois et al. (2010) differs from the typical extinction paradigm in which unilateral trials, bilateral trials and catch trials are intermingled, making the stimulus location unpredictable. Although extinction occurs in the context of attentional competition created by simultaneous bilateral stimulation (Driver, Mattingley, Rorden, & Davis, 1997), the spatial locations of stimuli in the Jacquin-Courtois et al. task were always bilateral and hence predictable, so in this context, extinction may be overcome by a strategic or voluntary shift in attention to the contralesional ear. If prism adaptation largely affects patients’ voluntary orienting of spatial attention on visual tasks (e.g., Angeli et al., 2004, Ferber et al., 2003, Nijboer et al., 2008, Serino et al., 2006), then it is plausible that it might also increase patients’ voluntary orienting to the contralesional ear during dichotic listening. Whether the effects observed by Jacquin-Courtois et al. were multimodal in nature is difficult to ascertain from their study, because they did not assess their patients for equivalent improvements in visual spatial attention. It is possible that prism adaptation improves voluntary orienting to sounds as well as visual stimuli, but whether it also influences auditory spatial biases in stimulus-driven orienting is not known. This distinction is an important one in understanding the locus of prism effects on neglect symptoms (Corbetta and Shulman, 2002, Corbetta et al., 2008, Karnath et al., 2003).
In the present study, we examined whether prism adaptation can influence neglect patients’ attentional gradient for detecting brief peripheral stimuli, and whether this effect generalises across sensory modalities. To test patients’ spatial gradient of attention, we used visual and auditory versions of a dual task in which patients had to monitor a central stream of stimuli for a target while responding to brief peripheral stimuli presented at varying locations within the left and right hemifield in an unpredictable fashion. In the auditory version of the task, we presented binaural stimuli over headphones; the stimuli were spatialised using head-related transfer functions (HRTF), such that participants perceived the sounds as emanating from locations in extrapersonal space. Unlike dichotic stimulus presentation (which is a non-optimal method of assessing auditory spatial attention because it confounds ear of presentation with spatial hemifield (Beaton and McCarthy, 1993, Beaton and McCarthy, 1995, Hugdahl et al., 1991, Spierer et al., 2007)), our stimuli were not restricted to one or the other ear but to either the left or right hemifield, similar to free-field sound presentation. Because prism adaptation directly induces a lateral bias in arm and eye movements (Angeli et al., 2004, Ferber et al., 2003, Redding et al., 2005, Redding and Wallace, 2006), these motor biases alone may explain neglect improvements on spatial tasks that require manual or ocular exploration (Angeli et al., 2004, Serino et al., 2006). Thus, to ensure that any prism effects reflect attentional changes, and are independent of changes to motor behaviour following adaptation, we employed auditory and visual tasks that did not require a manual localisation response, required central fixation of gaze, and that explicitly examined neglect patients’ spatial gradient of attention.
Section snippets
Participants
A group of twelve individuals with recent right hemisphere stroke (see Fig. 1), all of whom demonstrated left neglect on clinical tests, were recruited from stroke units in Brisbane (mean age = 66 years (SD = 14.85)). Although participants had varying degrees of hearing loss as measured by pure-tone audiometry (frequency range: 0.25–8 kHz), none had an asymmetric hearing loss (difference between thresholds >20 dB) (see Table 1). Approval was obtained from The University of Queensland and hospital
Left inattention and stability of symptoms over baseline sessions
Performance on each of the four tasks (line bisection, cancellation, visual and auditory dual tasks) during the baseline sessions was assessed. The patient group demonstrated significant asymmetries in performance on all four tasks, and these deficits were stable across the first and second baseline administrations.
Cancellation task. On both versions of the Balloons test (A and B), patients showed reduced cancellation of targets located within the left hemifield relative to targets located
Discussion
We investigated whether the effects of prism adaptation on spatial neglect are evident as a change in patients’ spatial gradient of attention, and whether this generalises to attention biases in the auditory modality. We found that patients demonstrated significant aftereffects of prism adaptation as measured by leftward shifts in their SSA, and that this effect generalised to patients’ neglect symptoms on a cancellation task, in the context of unchanged baseline performance over the previous
Conclusions
In a sample of 12 neglect patients who underwent prism adaptation, we found that the majority of patients did not show any changes in their spatial bias in exogenous attention to either visual or auditory stimuli, despite demonstrating significant visuo-motor aftereffects of adaptation and reduced neglect behaviour on traditional pen-and-paper tasks. Individual patients, however, did show changes in their visual spatial gradient of attention. No such effects were apparent on an analogous
Acknowledgement
This research was supported by a project grant from the National Health and Medical Research Council (Australia) awarded to JBM, DRFI and RE.
References (78)
- et al.
Recovery of oculo-motor bias in neglect patients after prism adaptation
Neuropsychologia
(2004) - et al.
Neglected attention in apparent spatial compression
Neuropsychologia
(2004) - et al.
Auditory neglect after right frontal lobe and right pulvinar thalamic lesions: Comments on Hugdahl, Wester and Asbjornsen (1991) and some preliminary findings
Brain and Language
(1993) - et al.
On the nature of auditory neglect: A reply to Hugdahl and Wester
Brain and Language
(1995) - et al.
Unilateral neglect of representational space
Cortex
(1978) - et al.
The reorienting system of the human brain: From environment to theory of mind
Neuron
(2008) - et al.
Eye position and cross-sensory learning both contribute to prism adaptation of auditory space
Progress in Brain Research
(2008) - et al.
A long-lasting improvement of somatosensory function after prism adaptation, a case study
Neuropsychologia
(2004) - et al.
Ameliorating neglect with prism adaptation: Visuo-manual and visuo-verbal measures
Neuropsychologia
(2002) - et al.
Spatial compression in visual neglect: A case study
Cortex
(1991)
Auditory neglect after right frontal lobe and right pulvinar thalamic lesions
Brain and Language
Impaired perception of temporal order in auditory extinction
Neuropsychologia
Displacement of the egocentric visual midline in altitudinal postchiasmatic scotomata
Neuropsychologia
Prism adaptation improved chronic visual and haptic neglect: A single case study
Cortex
Prism adaptation and spatial attention: A study of visual search in normals and patients with unilateral neglect
Cortex
Auditory deficits in visuospatial neglect patients
Cortex
Selective deficit of auditory localisation in patients with visuospatial neglect
Neuropsychologia
Deficit of auditory space perception in patients with visuospatial neglect
Neuropsychologia
Applications of prism adaptation: A tutorial in theory and method
Neuroscience and Biobehavioural Reviews
Prism adaptation and unilateral neglect: Review and analysis
Neuropsychologia
The effect of cueing on unilateral neglect
Neuropsychologia
Auditory sustained attention is a marker of unilateral spatial neglect
Neuropsychologia
Prism adaptation improves representational neglect
Neuropsychologia
Prism adaptation improves visual search in hemispatial neglect
Neuropsychologia
Prism adaptation aftereffects in stroke patients with spatial neglect: Pathological effects on subjective straight ahead but not visual open-loop pointing
Neuropsychologia
A common basis for visual and tactile exploration deficits in spatial neglect?
Neuropsychologia
Mechanisms underlying neglect recovery after prism adaptation
Neuropsychologia
Auditory extinction: The effect of stimulus similarity and task requirements
Neuropsychologia
Extinction of auditory stimuli in hemineglect: Space versus ear
Neuropsychologia
Prism adaptation to rightward optical deviation improves postural imbalance in left hemiparetic patients
Current Biology
A feature-integration theory of attention
Cognitive Psychology
Anosognosia: The neurology of beliefs and uncertainties
Cortex
Abnormal attentional modulation of retinotopic cortex in parietal patients with spatial neglect
Current Biology
Prismatic adaptation reduces biased temporal order judgments in spatial neglect
Neuroreport
Disorders of perceived auditory lateralization after lesions of the right hemisphere
Brain
Prism adaptation reverses the local processing bias in patients with right temporo-parietal junction lesions
Brain
Control of goal-directed and stimulus-driven attention in the brain
Nature Reviews Neuroscience
Auditory extinction following hemisphere damage
Neuropsychologia
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2019, CortexCitation Excerpt :In keeping with the hypothesis of a spatial representation of temporal information, shifting attentive focus along the mental time line can bias time processing in a flexible manner. According to observations from literature in the spatial domain, showing that PA extends its effects to sensory modalities not directly implicated in visuo-motor coordination, such as auditory modality (Eramudugolla, Boyce, Irvine, & Mattingley, 2010; Jacquin-Courtois et al., 2010), Magnani, Pavani, and Frassinetti (2012) demonstrated the effects of PA on auditory time. Participants were instructed to classify sound durations as “short” or “long”, only when the stimulus occupied a pre-determined location in space (left or right), regardless of its pitch (spatial experiment), or only when the stimulus was of a pre-determined pitch (high-frequency or low-frequency), regardless of its spatial location (tonal experiment).
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2015, Research in Developmental DisabilitiesCitation Excerpt :PA has been shown to modify performances in a variety of spatial tasks in adults: both in healthy individuals and in patients with unilateral neglect after stroke (Serino, Bonifazi, Pierfederici, & Làdavas, 2007). Due to its long-lasting effect, PA is regarded as an effective procedure for rehabilitating unilateral spatial neglect by bringing the neglected hemispace into the task-work space (Facchin, Beschin, Toraldo, Cisari, & Daini, 2013; Rusconi & Carelli, 2012; Làdavas, Bonifazi, Catena, & Serino, 2011; Eramudugolla, Boyce, Irvine, & Mattingley, 2010; Turton, O’Leary, Gabb, Woodward, & Gilchrist, 2010; Serino et al., 2007). Indeed, this rehabilitation method elicits a shift of the visual field towards the non-neglected ipsilesional side during the execution of pointing or reaching tasks, forcing subjects to compensate and to re-orient movements in the direction of the neglected contralesional side (Rossetti et al., 1998).
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2015, Handbook of Clinical NeurologyCitation Excerpt :One study found that prism adaptation significantly reduces auditory extinction as measured in a dichotic speech test (Jacquin-Courtois et al., 2010). The other study used a target detection task and found improvement in both visual and auditory target detection that was similar for ipsi- and contralesional stimuli (Eramudugolla et al., 2010). The effect of prism adaptation on auditory extinction lasted for 2 hours (Jacquin-Courtois et al., 2010).
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2013, Neuroscience and Biobehavioral ReviewsCitation Excerpt :Tasks used in these cases do neither include visual components or explicitly spatial parameters. Moreover, clear dissociations have been demonstrated in neglect patients between improvement of oculo-motor exploration without clinical beneficial effects (Dijkerman et al., 2003; Ferber et al., 2003), or visuo-motor effects without improvement of pathological gradient of spatial attention (Eramudugolla et al., 2010). Amelioration of unilateral neglect following PA thus cannot be mediated only by an adaptive redistribution of oculo-motor exploration or spatial attention.
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