INTRODUCTION
Hemispatial neglect is a common symptom of right hemisphere stroke (Ringman, Saver, Woolson, Clarke, & Adams, Reference Ringman, Saver, Woolson, Clarke and Adams2004). Severe neglect becomes clinically observable, for example, in activities of daily living and in neuropsychological screening tests (Gillen, Tennen, & McKee, Reference Gillen, Tennen and Mc Kee2005; Katz, Hartman-Maeir, Ring, & Soroker, Reference Katz, Hartman-Maeir, Ring and Soroker1999). Subclinical neglect is more demanding to diagnose but can result in functional disability (Bonato, Priftis, Marenzi, Umiltá, & Zorzi, Reference Bonato, Priftis, Marenzi, Umiltà and Zorzi2012; Jehkonen et al., Reference Jehkonen, Ahonen, Dastidar, Koivisto, Laippala, Vilkki and Molnár2000).
Traditional paper-and-pencil tests are not sensitive in revealing subclinical neglect (Bonato & Deouell, Reference Bonato and Deouell2013). They have also been criticized for their poor ecological validity since stimuli are static and presented in a narrow visual space (Bonato & Deouell, Reference Bonato and Deouell2013; Hasegawa, Hirono, & Yamadori, Reference Hasegawa, Hirono and Yamadori2011; Nakatani, Notoya, Sunahara, Takahashi, & Inoue, Reference Nakatani, Notoya, Sunahara, Takahashi and Inoue2013; Ulm et al., Reference Ulm, Wohlrapp, Meinzer, Steinicke, Schatz, Denzler and Winter2013). There have been various attempts to improve traditional tests’ sensitivity. These include, for example, increasing the number or similarity of target and distractor stimuli (Aglioti, Smania, Barbieri, & Corbetta, Reference Aglioti, Smania, Barbieri and Corbetta1997; Basagni et al., Reference Basagni, De Tanti, Damora, Abbruzzese, Varalta, Antonucci and Mancuso2017; Kaplan et al., Reference Kaplan, Verfaellie, Meadows, Caplan, Pessin and DeWitt1991; Rapcsak, Verfaellie, Fleet, & Heilman, Reference Rapcsak, Verfaellie, Fleet and Heilman1989; Sarri, Greenwood, Kalra, & Driver, Reference Sarri, Greenwood, Kalra and Driver2009), using time limits in visual searching (Priftis, Di Salvo, & Zara, Reference Priftis, Di Salvo and Zara2019), or requiring counting backward while performing the task (Robertson & Frasca, Reference Robertson and Frasca1992).
The increased complexity of the test environment enhances assessment sensitivity in revealing neglect (Blini et al., Reference Blini, Romeo, Spironelli, Pitteri, Meneghello, Bonato and Zorzi2016; Bonato, Reference Bonato2012, Reference Bonato2015; Bonato, Priftis, Marenzi, Umiltá, & Zorzi, Reference Bonato, Priftis, Marenzi, Umiltá and Zorzi2010; Hasegawa et al., Reference Hasegawa, Hirono and Yamadori2011; Robertson & Manly, Reference Robertson, Manly, Karnath, Milner and Vallar2004). While a large portion of this evidence comes from observations in patients with right hemisphere strokes (Bartolomeo, Reference Bartolomeo2000; Bonato, Reference Bonato2015; Bonato et al., Reference Bonato2012; Bonato, Priftis, Umiltá, & Zorzi, Reference Bonato, Priftis, Umiltá and Zorzi2013; Deouell, Sacher, & Soroker, Reference Deouell, Sacher and Soroker2005; Eramudugolla, Boyce, Irvine, & Mattingley, Reference Eramudugolla, Boyce, Irvine and Mattingley2010; Smania et al., Reference Smania, Martini, Gambina, Tomelleri, Palamara, Natale and Marzi1998; van Kessel, van Nes, Geurts, Brouwer, & Fasotti, Reference van Kessel, van Nes, Geurts, Brouwer and Fasotti2013), there are also studies showing similar deficits in left hemisphere patients (Blini et al., Reference Blini, Romeo, Spironelli, Pitteri, Meneghello, Bonato and Zorzi2016; Bonato et al., Reference Bonato, Priftis, Marenzi, Umiltá and Zorzi2010).
New computerized assessment methods requiring divided attention and reacting to dynamic stimuli offer benefits over traditional tests (Bonato et al., Reference Bonato, Priftis, Marenzi, Umiltá and Zorzi2010; van Kessel, van Nes, Brouwer, Geurts, & Fasotti, Reference van Kessel, van Nes, Brouwer, Geurts and Fasotti2010; van Kessel et al., Reference van Kessel, van Nes, Geurts, Brouwer and Fasotti2013). Variations in task complexity hinder the use of compensatory strategies, and reaction time measurements enhance precision (Bonato & Deouell, Reference Bonato and Deouell2013). Traditional tests do not reach similar sensitivity (Deouell et al., Reference Deouell, Sacher and Soroker2005; Kim et al., Reference Kim, Ku, Chang, Park, Lim, Han and Kim2010; Tanaka, Sugihara, Nara, Ino, & Ifukube, Reference Tanaka, Sugihara, Nara, Ino and Ifukube2005; Tsirlin, Dupierrix, Chokron, Coquillart, & Ohlmann, Reference Tsirlin, Dupierrix, Chokron, Coquillart and Ohlmann2009; Ulm et al., Reference Ulm, Wohlrapp, Meinzer, Steinicke, Schatz, Denzler and Winter2013; van Kessel et al., Reference van Kessel, van Nes, Brouwer, Geurts and Fasotti2010, Reference van Kessel, van Nes, Geurts, Brouwer and Fasotti2013) even if factors increasing discernment are introduced (Bonato et al., Reference Bonato2012).
Various studies have compared new assessment methods with traditional tests (e.g. Deouell et al., Reference Deouell, Sacher and Soroker2005; Kim et al., Reference Kim, Ku, Chang, Park, Lim, Han and Kim2010; Tanaka et al., Reference Tanaka, Sugihara, Nara, Ino and Ifukube2005; Ulm et al., Reference Ulm, Wohlrapp, Meinzer, Steinicke, Schatz, Denzler and Winter2013; van Kessel et al., Reference van Kessel, van Nes, Brouwer, Geurts and Fasotti2010), and computerized dual-tasks with single tasks (Andres et al., Reference Andres, Geers, Marnette, Coyette, Bonato, Priftis and Masson2019; Blini et al., Reference Blini, Romeo, Spironelli, Pitteri, Meneghello, Bonato and Zorzi2016; Bonato, Reference Bonato2015; Bonato et al., Reference Bonato, Priftis, Marenzi, Umiltá and Zorzi2010, Reference Bonato2012; van Kessel et al. Reference van Kessel, van Nes, Geurts, Brouwer and Fasotti2013). However, to our knowledge, there is only limited research comparing different computerized dual-tasks. Some of these studies have reported different versions of the dual-task as being sensitive (Blini et al., Reference Blini, Romeo, Spironelli, Pitteri, Meneghello, Bonato and Zorzi2016; Bonato et al., Reference Bonato, Priftis, Marenzi, Umiltá and Zorzi2010, Reference Bonato2012; Peers, Ludwig, Cusack, & Duncan, Reference Peers, Ludwig, Cusack and Duncan2006). It has also been shown that low complexity in the primary central task does not reveal neglect in secondary peripheral visual processing, but high complexity does (Vuilleumier & Driver, Reference Vuilleumier and Driver2007). None of these dual-task studies has utilized large screens.
The aim of the present study was to examine whether varying the complexity of the dual-task would improve the sensitivity of the assessment and enable the identification of subclinical neglect. More specifically, we investigated whether a computerized dual-task paradigm and the use of a large perceptual field would yield sufficient complexity in order to differentiate the findings obtained through a traditional paper-and-pencil cancellation test, or whether additional factors increasing task demands would be required. To answer the research problem, we developed and compared two computerized dual tasks: one simpler and the other more complex. The tasks were presented on a 173 cm × 277 cm screen to enhance ecological validity. The Bells Test was used as a traditional cancellation test to assess neglect. While neglect may occur in different sensory modalities, this study focuses solely on the visual form.
METHOD
Participants
A total of 58 potentially eligible consecutive stroke patients receiving rehabilitation at the Neurology Outpatient Clinic of Helsinki University Hospital were selected for recruitment. Recruitment and data collection were carried out between June 2016 and February 2019. The inclusion criteria were native Finnish speakers with first-ever CT (computed tomography) or MRI (magnetic resonance imaging)-verified stroke; no prior neurological diagnosis or bilateral stroke; no visual field defect according to clinical neurological or neuro-ophthalmological evaluation; no primary impairment in hearing or sight (other than myopia or hyperopia corrected with glasses); no substance abuse; no severe aphasia or other significant cognitive or similar symptom preventing participation; and no severe hemiparesis or other significant motor symptom or psychiatric disease, which would complicate the cooperation. Altogether, 18 patients were excluded because of prior or bilateral stroke, visual field defect, or severe neglect, preventing cooperation. The patients included in the study comprised 20 right hemisphere (RH patient group, 9 men, mean age 53 SD ± 8 years) and 20 left hemisphere (LH patient group, 15 men, mean age 51 SD ± 9 years) stroke patients. Fourteen of the RH patients and 10 of the LH patients received multiprofessional neurological outpatient rehabilitation, while the rest of the patients received only neuropsychological outpatient rehabilitation.
Control participants included 20 healthy volunteers (8 men, mean age 46 SD ± 15 years) matched with the patient groups in age, gender, and education. The characteristics of the patients and controls are shown in Table 1.
Characteristics of the patients and controls
Note. LH = left hemisphere stroke; RH = right hemisphere stroke.
a Mean (SD), Mann–Whitney U- or Kruskal–Wallis Tests (U/X2).
b Frequency, Pearson Chi-Square Test (χ2).
The study protocol was approved by the Ethics Committee of Helsinki University Hospital. All participants gave written informed consent for participation. The data included in the study were obtained in compliance with the Helsinki Declaration.
Procedure
Comprehensive neuropsychological assessment
The comprehensive neuropsychological assessment consisted of tests covering multiple cognitive domains. Visual attention was examined with the Bells Test to assess neglect (Gauthier, Dehaut, & Joanette, Reference Gauthier, Dehaut and Joanette1989). Executive functions and processing speed were examined with the Trail Making Test, parts A and B (Reitan, Reference Reitan1958), the Brixton Spatial Anticipation Test (Burgess & Shallice, Reference Burgess and Shallice1997), design, phonetic and semantic fluency (Jones-Gotman & Milner, Reference Jones-Gotman and Milner1977; Miller, Reference Miller1984), and a dual-task modification of the Bourdon–Wiersma Test, including counting numbers backwards and visual dot cancellation (Vilkki, Virtanen, Surma-aho, & Servo, Reference Vilkki, Virtanen, Surma-aho and Servo1996). Memory was examined with working memory distraction, word list learning, and delayed recall (Christensen, Reference Christensen1979), and with subtests of the Wechsler Memory Scale, third edition (WMS-III): Letter-Number Sequencing and Visual Memory Span (Wechsler, Reference Wechsler1997, Reference Wechsler2008). Depression was evaluated with the Depression Scale, which consists of 10 items with scores ranging from 0 to 30 (Salokangas, Poutanen, & Stengard, Reference Salokangas, Poutanen and Stengård1995).
Large-screen tasks
Apparatus
A new computer-based method, the Active Space, was developed based on near-field imaging technology (Linnavuo, Kovalev, & Sepponen, Reference Linnavuo, Kovalev and Sepponen2010; Rimminen, Lindström, Linnavuo, & Sepponen, Reference Rimminen, Lindström, Linnavuo and Sepponen2010). The Active Space includes several means of generating visual stimuli and measuring reaction times. The main visual stimuli generator is a short throw video projector (Epson EB-680, Seiko EPSON Corporation, Suwa, Japan) producing a display of height 173 cm and a width of 277 cm on the wall. The midpoint of the screen is located 120 cm from the floor. The pixel size of the display is 1.9 mm. Control of the Active Space and the task applications are implemented using LabVIEW™ systems engineering software (National Instruments, Austin, TX, USA).
In the research setting, the participant was seated in a chair facing the screen at a 180-cm distance. Thus, the display appeared at an angle of approximately 75° horizontally and 51° vertically. The participants performed two distinct dual-tasks. In both, a peripheral visual field task was presented simultaneously with a numeric central task. A short training, including verbal guidance, preceded the actual test session.
Tasks
The main technical parameters of the large-screen tasks are listed in Table 2.
Main technical parameters of detection and crash tasks
Note. RGB = red, green, blue color space; ISI = interstimulus interval; ITI = intertarget interval.
Detection task
In the peripheral visual field task, the participants were instructed to observe and react to a red sphere flashing among other colored ones, with all spheres appearing one at a time. For the central task, numbers appeared in the center of the screen. Participants were instructed to observe the continuously changing numbers and react only to the number 2. As part of the dual-task paradigm, subjects performed the peripheral visual field task and the central task simultaneously, but peripheral and central targets never appeared at the same time.
The duration of the Detection task was 2 min, and it was preceded by three trial runs of 30 s: first, both individual tasks were practiced separately, and finally, in the third trial run, the combined dual-task was practiced.
Correct reactions and reaction times, as well as missed stimuli, were extracted. A response was interpreted as “missed” if the participant failed to respond within the allowed temporal window of 1000 ms. If the participant responded before the target appeared or earlier than 250 ms after target onset, the reactions were excluded as anticipatory errors. Reactions deviating more than 2.5 SD from the mean were also excluded as outliers. This was done separately for each participant and condition. A total of 2% of all reactions were excluded. A visualization of the Detection task is presented in Figure 1.
Visualization of the Detection task. Initially, no targets are visible (top), then a central target appears (middle), and last, a red peripheral target sphere flashes in the left hemifield (bottom).
Crash task
The peripheral visual field task was to observe and react to a collision of two moving gray spheres, resulting in a white flash appearing on the screen. In the central task, numbers appeared at the center of the display. The participants were instructed to follow the continuously changing numbers and react by saying the word “hep” into a lavalier microphone any time a number presented on the screen was exactly twice as high as the immediately preceding figure (alternatives: 1 → 2, 2 → 4, 3 → 6, 4 → 8). As part of the dual-task paradigm, subjects performed the peripheral visual field task and the central task simultaneously, but peripheral and central targets never appeared at the same time.
The duration of the Crash task was 4 min and was preceded by three trial runs of 30 s: first, both individual tasks were practiced separately, and finally, in the third trial run, the combined dual-task was practiced.
Correct reactions and reaction times, as well as missed stimuli, were extracted. A response was interpreted as “missed” if the participant failed to respond within the allowed temporal window of 1500 ms. If the participant responded before the target appeared, or earlier than 250 ms after target onset, the reactions were excluded as anticipatory errors. Also, reactions deviating more than 2.5 SD from the mean were excluded as outliers. This was done separately for each participant and condition. A total of 3% of all reactions were excluded. The visualization of the Crash task is presented in Figure 2.
Visualization of the Crash task. A collision is just happening (top), resulting in a white flash in the left hemifield (bottom).
The Crash task was the more complex of the two dual-tasks. Compared to Detection, Crash introduced additional task demands through (1) increased arithmetic demands of the central task, (2) required different reactions in the central and peripheral tasks, (3) doubled the task duration, and (4) decreased the prominence of the targets from the background. All participants performed the Detection task first.
Data Analysis
The Statistical Package for the Social Sciences (Version 25.0, IBM Corporation, Armonk, NY, USA) was used for statistical analyses. Large-screen task variables were created by calculating the average hit rates and reaction times separately for the left and right peripheral targets. Demographics, clinical and neuropsychological data, and the hit rates of the large-screen tasks were analyzed by using nonparametric methods due to the skewed distribution of the variables. Analyses were performed by using the Mann–Whitney U- or Kruskal–Wallis Tests (U/X2) for continuous variables and the Pearson’s Chi-Square Test (χ2) for categorical variables. Dunn’s Test was used for post hoc analyses. Within-group analyses (hit rate differences between the two hemifields) were performed using the Wilcoxon Signed-Rank Test. Reaction times were analyzed by using mixed analysis of variance (ANOVA) with Group (RH patients vs. LH patients vs. controls) as the between-participants factor and Hemifield (left vs. right) as well as Task (Crash task vs. Detection task) as within-participants factors. For multiple pairwise comparisons, the p values were adjusted using the Bonferroni correction in all post hoc analyses. Effect sizes were calculated by computing eta squared (η 2) for the Kruskal–Wallis Test, r for the Mann–Whitney U, Wilcoxon Signed-Rank, and Dunn’s Tests, Cramer’s V for Pearson’s Chi-Square Test, and partial eta squared (η 2 partial) for mixed ANOVA (Tomczak & Tomczak, Reference Tomczak and Tomczak2014). For significant group differences, Cohen’s descriptions for η 2 (partial) (large effect: .14, medium effect: .06, small effect: .01) and for r (large effect: .5, medium effect: .3, small effect: 1) were used (Cohen, Reference Cohen1988, pp. 79–80, 283–287, 366–368). The level of statistical significance was set at .05.
RESULTS
Patient and Control Characteristics
No significant differences were observed between the patient and control groups in demographic or clinical variables (Table 1).
Comprehensive Neuropsychological Assessment
Statistical analyses of the comparisons between the patients and controls in neuropsychological test scores are shown in Table 3. RH patients were significantly slower than the controls in the Trail Making Test A. Both RH and LH patients performed significantly worse than controls in design fluency. Also, LH patients performed significantly worse than controls in phonetics and RH patients in semantic fluency. Finally, LH patients performed significantly worse than controls in the Bourdon–Wiersma dot cancellation single task and in the dot cancellation and number count dual-tasks. LH and RH patients did not differ significantly on any of the neuropsychological variables.
Comprehensive neuropsychological assessment of the patients and controls
Note. LH = left hemisphere stroke; RH = right hemisphere stroke.
a Mean (SD), Kruskal–Wallis Test (X2), mean ranks and post hoc comparisons presented for significant group differences.
Large-Screen Tasks
Hit rates
Hit rates for the large-screen tasks and statistical comparisons between the participant groups and the two hemifields are shown in Table 4. One right hemisphere stroke patient failed to perform Crash, and therefore, the related analyses are missing one patient (marked with • in Tables 4 and 5).
Hit rates for the large-screen tasks in the LH and RH patients and controls
Note. Data for 1 patient missing. LH = left hemisphere stroke; RH = right hemisphere stroke.
a Kruskall–Wallis Test (X2), mean ranks and post hoc comparisons presented for significant group differences.
b Wilcoxon Signed-Rank Test (Z).
Reaction times for the large-screen tasks in the LH and RH patients and controls
Note. Data for 1 patient missing. LH = left hemisphere stroke; RH = right hemisphere stroke.
a Repeated-measures-ANOVA.
Detection task
The RH patients missed significantly more targets than the controls in the left hemifield but not in the right hemifield (see Figure 3). The LH patients did not differ significantly from the controls, and no significant differences in hit rates occurred between the patient groups. In the comparison of the two hemifields, the RH patients missed significantly more left hemifield than right hemifield targets (see Figure 3). No significant differences occurred between the two hemifields of the LH patients or the controls.
Average hit rates of the controls and the RH patients in Crash and Detection tasks. In both tasks, RH patients missed significantly more left hemifield targets than controls. Also, RH patients missed significantly more left than right hemifield targets in Detection, and controls missed significantly more right than left hemifield targets in Crash.
Crash task
The RH patients missed significantly more left hemifield targets than the controls, but no significant differences occurred in right hemifield targets (see Figure 3). The LH patients and the controls, or the patient groups, did not differ significantly in either hemifield. In the comparison of the two hemifields, the controls missed significantly more right than left hemifield targets (see Figure 3). No significant hemifield differences occurred in either patient group.
Reaction times
Average reaction times and statistical analyses of the between- and within-participants’ effects are shown in Table 5.
There were no significant differences in reaction times for the Detection or Crash targets between RH or LH patients and controls, nor between the patient groups. However, in all groups, within-participants comparisons showed significant task and hemifield × task effects, with the reaction times for Crash being slower than those for Detection, and for Crash, they were slower over the left than the right hemifield (see Figure 4).
Average reaction times of the participant groups in Crash and Detection tasks (error bars represent ±1 SD). In all groups, the reaction times for Crash were significantly slower than those for Detection, and for Crash, they were slower over the left than the right hemifield.
DISCUSSION
We examined whether varying the complexity of tasks would improve the sensitivity of the assessment and enable the identification of subclinical neglect. We developed and compared two computerized tasks. In both tasks, we used a dual-task paradigm which is reportedly sensitive in detecting neglect (Bonato, Reference Bonato2012; Robertson & Frasca, Reference Robertson and Frasca1992; van Kessel et al., Reference van Kessel, van Nes, Geurts, Brouwer and Fasotti2013). We presented the tasks on a large screen in order to enhance ecological validity (Nakatani et al., Reference Nakatani, Notoya, Sunahara, Takahashi and Inoue2013; Ulm et al., Reference Ulm, Wohlrapp, Meinzer, Steinicke, Schatz, Denzler and Winter2013). Of particular interest was finding whether the demands of the simpler dual-task (Detection) were sufficient to differentiate the findings obtained through the traditional Bells Test, or whether additional demands introduced in the more complex dual-task (Crash) would be required.
The main findings of our study are that both the simpler and more complex large-screen dual-tasks were sensitive in identifying RH patients’ subclinical neglect. The RH group missed significantly more left Detection and Crash targets than the control group. The RH group also missed significantly more Detection targets in their left than in their right hemifields. RH patients’ neglect did not become evident in the traditional Bells Test. LH patients’ performance did not differ from the controls in either of the large-screen tasks or the Bells Test. Task complexity had a general rather than a specifically neglect-revealing effect on reaction times. All groups showed significantly slower reactions for Crash than Detection targets, and they showed prolonged Crash reactions in the left compared to the right hemifields. Both patient groups differed from the controls in several cognitive domains in the comprehensive neuropsychological assessment but did not differ from each other.
The finding that RH patients missed significantly more left targets than the controls in the large-screen tasks but not in the Bells Test was in line with various previous studies comparing new computerized visuospatial and traditional tests (Deouell et al., Reference Deouell, Sacher and Soroker2005; Kim et al., Reference Kim, Ku, Chang, Park, Lim, Han and Kim2010; Tanaka et al., Reference Tanaka, Sugihara, Nara, Ino and Ifukube2005; Ulm et al., Reference Ulm, Wohlrapp, Meinzer, Steinicke, Schatz, Denzler and Winter2013; van Kessel et al., Reference van Kessel, van Nes, Brouwer, Geurts and Fasotti2010). Hence, an absence of symptoms in simpler test environments is not necessarily consistent with observations in more complex ones (Blini et al., Reference Blini, Romeo, Spironelli, Pitteri, Meneghello, Bonato and Zorzi2016; Bonato, Reference Bonato2015; Bonato et al., Reference Bonato, Priftis, Marenzi, Umiltá and Zorzi2010, Reference Bonato2012; Hasegawa et al., Reference Hasegawa, Hirono and Yamadori2011). It is possible that the rehabilitation received by the patients may have affected our findings at least to a degree, as early-stage neuropsychological rehabilitation typically utilizes traditional pen-and-paper cancellation tasks. Therefore, the Bells Test may have fallen under a test type familiar to the patients, thereby facilitating the use of compensatory strategies for neglect. It should also be noted that large-screen tasks assess neglect in the extrapersonal space while the Bells Test does so in the peripersonal space. Some studies (e.g. Cowey, Small, & Ellis, Reference Cowey, Small and Ellis1994; Halligan & Marshall, Reference Halligan and Marshall1991) have indicated that these forms of neglect can occur separately from each other. It is, therefore, possible that RH patients in this study suffered from extrapersonal but not peripersonal neglect. However, most previous studies (e.g. Andres et al., Reference Andres, Geers, Marnette, Coyette, Bonato, Priftis and Masson2019; Blini et al., Reference Blini, Romeo, Spironelli, Pitteri, Meneghello, Bonato and Zorzi2016; Bonato, Reference Bonato2015; Bonato et al., Reference Bonato, Priftis, Marenzi, Umiltá and Zorzi2010, Reference Bonato2012), which have compared more complex computer-based tasks to pen-and-paper methods in the peripersonal space, have found that the computer-based tasks are more sensitive in identifying mild neglect.
Which factors contributed to both large-screen tasks being sensitive in identifying RH patients’ subclinical neglect? Traditional tests have been criticized for their poor ecological validity since the stimuli are presented in a narrow visual space (Nakatani et al., Reference Nakatani, Notoya, Sunahara, Takahashi and Inoue2013; Ulm et al., Reference Ulm, Wohlrapp, Meinzer, Steinicke, Schatz, Denzler and Winter2013). Hence, a large test field may be one of the components that increase sensitivity. Further, a dual-task assignment presumably eliminates the typical top-down coping mechanism and brings out symptoms that would otherwise be compensated for (Andres et al., Reference Andres, Geers, Marnette, Coyette, Bonato, Priftis and Masson2019; Bonato, Reference Bonato2015; Robertson & Frasca, Reference Robertson and Frasca1992; Robertson & Manley, Reference Robertson, Manly, Karnath, Milner and Vallar2004; van Kessel et al., Reference van Kessel, van Nes, Geurts, Brouwer and Fasotti2013). Increases in task demands need not be either visuospatial or attentional in order to improve assessment (Mennemeier, Morris, & Heilman, Reference Mennemeier, Morris and Heilman2004; Ricci et al., Reference Ricci, Salatino, Garbarini, Ronga, Genero, Berti and Neppi-Mòdona2016). For example, arithmetic processing, which was needed in our large-screen central tasks, also enhances task demands to better bring out neglect (Mennemeier et al., Reference Mennemeier, Morris and Heilman2004; Robertson & Frasca, Reference Robertson and Frasca1992). Presumably, simultaneous arithmetic and visuospatial processing introduces deficits in both general and lateralized attention (Ricci et al., Reference Ricci, Salatino, Garbarini, Ronga, Genero, Berti and Neppi-Mòdona2016). These components interact in neglect, whereby the presence of a general deficit exacerbates the severity of a lateralized one (van Kessel et al., Reference van Kessel, van Nes, Brouwer, Geurts and Fasotti2010). Successful performance in the large-screen tasks also requires effective executive functions, processing speed, and working memory. These cognitive domains are the ones typically affected after stroke (Farnè et al., Reference Farnè, Buxbaum, Ferraro, Frassinetti, Whyte, Veramonti and Làdavas2004; Jaillard, Naegele, Trabucco-Miguel, LeBas, & Hommel, Reference Jaillard, Naegele, Trabucco-Miguel, LeBas and Hommel2009; Jokinen et al., Reference Jokinen, Melkas, Ylikoski, Pohjasvaara, Kaste, Erkinjuntti and Hietanen2015; Middleton et al., Reference Middleton, Lam, Fahmi, Black, McIlroy, Stuss and Turner2014; Nys et al., Reference Nys, van Zandvoort, de Kort, van der Worp, Jansen, Algra and Kappelle2005). Based on the comprehensive neuropsychological assessment, this was also the case with our patients. It may be that these other cognitive deficits exhausted RH patients’ attentional resources while performing the large-screen tasks and weakened their ability to compensate for neglect (Smit, Eling, & Coenen, Reference Smit, Eling and Coenen2004a; van Kessel et al., Reference van Kessel, van Nes, Brouwer, Geurts and Fasotti2010). Apparently, sufficient load (i.e. increased task difficulty together with limited processing time) is needed to improve assessment (Priftis et al., Reference Priftis, Di Salvo and Zara2019).
Although the large-screen tasks differentiated the RH patients from the controls in terms of left hemifield omissions, there were no group differences in reaction times. This finding seems logical considering the fact that the tasks required constant reactions on short interstimulus intervals, and responses were only registered during a short window. Therefore, it may be that longer response times would register more readily as omitted. Supporting the above, some previous studies (Deouell et al., Reference Deouell, Sacher and Soroker2005; Rengachary, d’Avossa, Sapir, Shulman, & Corbetta, Reference Rengachary, d’Avossa, Sapir, Shulman and Corbetta2009) that successfully demonstrate right hemisphere patients’ neglect in reaction times have either deliberately chosen a long response window or substituted missed trials with the longest-permitted reaction time. This was done to maximize hits and, hence, improve the signal-to-noise ratio of reaction times. Another essential factor behind the finding might be the fact that controls displayed prolonged Crash reactions for the left as well. This possibly hindered the group difference from becoming noticeable.
In the Crash task, the reactions to the left-side targets were significantly slower than those to the right-side targets. Subject groups did not differ in this respect. As the simpler dual-task, Detection, failed to identify this difference, the increased task complexity possibly influenced the results. This interpretation is supported by the observation of considerably shorter reaction times in Detection than Crash. More demanding tasks could be expected to require more time to process (Bartolomeo, Reference Bartolomeo2000). Crash was not only more demanding from a cognitive perspective, but its duration was also twice that of Detection, and all participants performed Detection first. It may be that the increases in both difficulty and duration, as well as the presentation order, affected the results, possibly through alertness. In fact, several studies have suggested that a decrease in alertness—be it from sleep deprivation, a long test protocol, or high task demands—is associated with a rightward orientation shift. In addition to patients with right hemisphere strokes (Peers et al., Reference Peers, Ludwig, Cusack and Duncan2006; Robertson et al., Reference Robertson, Manly, Beschin, Daini, Haeske-Dewick, Hömberg and Weber1997), similar behaviors have been found with left hemisphere patients (Peers et al., Reference Peers, Ludwig, Cusack and Duncan2006) as well as healthy subjects (Bellgrove, Dockree, Aimola, & Robertson, Reference Bellgrove, Dockree, Aimola and Robertson2004; Dobler et al., Reference Dobler, Anker, Gilmore, Robertson, Atkinson and Manly2005; Dodds et al., Reference Dodds, van Belle, Peers, Dove, Cusack, Duncan and Manly2008; Fimm, Willmes, & Spijkers, Reference Fimm, Willmes and Spijkers2006; Pérez et al., Reference Pérez, Peers, Valdés-Sosa, Galán, García and Martínez-Montes2009; Takio, Koivisto, Laukka, & Hämäläinen, Reference Takio, Koivisto, Laukka and Hämäläinen2011; Takio, Koivisto, Tuominen, Laukka, & Hämäläinen, Reference Takio, Koivisto, Tuominen, Laukka and Hämäläinen2013). This phenomenon has been explained by the domination of right hemispheres in both spatial and sustained attention, as well as their close interconnection (Cavézian et al., Reference Cavézian, Perez, Peyrin, Gaudry, Obadia, Gout and Chokron2015; Corbetta, Kincade, Lewis, Snyder, & Sapir, Reference Corbetta, Kincade, Lewis, Snyder and Sapir2005; He et al., Reference He, Snyder, Vincent, Epstein, Shulman and Corbetta2007; Posner & Petersen, Reference Posner and Petersen1990; Robertson, Reference Robertson1989, Reference Robertson, Robertson and Marshall1993, Reference Robertson2001). It may be that, as proposed by Bellgrove and coworkers (2004), the reduction in sustained attention is associated with decreased activity within the frontoparietal attentional networks underlying both sustained and spatial attention. This decreased activity, then, weakens the right hemisphere spatial attentional systems and drives attention toward the right (Bellgrove et al., Reference Bellgrove, Dockree, Aimola and Robertson2004). Thus, in the present study, the general rightward bias in Crash reactions might be related to a possible alertness decrement effect as a result of depleted resources in high-complexity tasks (Peers et al., Reference Peers, Ludwig, Cusack and Duncan2006; Smit et al., Reference Smit, Eling and Coenen2004a; Smit, Eling, & Coenen, Reference Smit, Eling and Coenen2004b; Takio, Koivisto, & Hämäläinen, Reference Takio, Koivisto and Hämäläinen2014).
Generalizations from the present interpretations should be made with some caution. The sample size of the study sets certain limitations. Our findings were also inconsistent with some previous studies. There are observations of high task complexity emphasizing right-sided neglect in left hemisphere patients (Blini et al., Reference Blini, Romeo, Spironelli, Pitteri, Meneghello, Bonato and Zorzi2016; Bonato et al., Reference Bonato, Priftis, Marenzi, Umiltá and Zorzi2010). In our study, conversely, high complexity caused a rightward shift. A possible explanation for this contradiction might be that the LH patients in the present study did not suffer from even subclinical neglect. Hence, the high task complexity would have caused a similar reaction time effect in LH patients as displayed by healthy controls. Another reason may be that the rightward bias in our study was observed in terms of reaction times, while the abovementioned studies analyzed hit rates. This might explain the contradiction which seems to be supported by healthy controls in our study displaying shorter but more inaccurate reactions toward the right. Supplementary studies are required to clarify this issue. Future studies may also uncover additional information on the effects of task duration on identifying neglect. A longer task would be a more ecologically valid way to assess whether neglect becomes more pronounced through the effects of load and fatigue. Such information would be crucial in a clinical setting, particularly with a view toward a patient’s ability to work or operate a vehicle. Future studies should assess the effect of individual factors (i.e. the large perceptual field or the dual-task paradigm) in increasing the overall sensitivity of the method. The present study attempted to increase sensitivity by combining several factors known to increase sensitivity, and because of this, the significance of the individual factors remains elusive. Several previous studies (e.g. Andres et al., Reference Andres, Geers, Marnette, Coyette, Bonato, Priftis and Masson2019; Blini et al., Reference Blini, Romeo, Spironelli, Pitteri, Meneghello, Bonato and Zorzi2016; Bonato, Reference Bonato2015; Bonato et al., Reference Bonato, Priftis, Marenzi, Umiltá and Zorzi2010, Reference Bonato2012; van Kessel et al. Reference van Kessel, van Nes, Geurts, Brouwer and Fasotti2013) have already noted that a dual-task paradigm is in itself more sensitive than a single task in bringing out mild neglect. Therefore, the effect of the large visual field would require particular attention in future studies.
To conclude, in this study, we presented a new method for the assessment of visual neglect. We demonstrated that, in a large extrapersonal space, dual-tasks sensitively reveal right hemisphere stroke patients’ subclinical neglect. It is important to identify and diagnose all forms of neglect in order to assess the efficacy of rehabilitation and to address specific concerns such as driving ability or working ability in tasks requiring high attention. More sensitive methods than traditional cancellation tests are needed to evaluate these issues. A large test field, together with dynamic stimuli, enhances ecological validity and sensitivity in neglect assessment.
Acknowledgments
This work was supported by a grant from the Oskar Öflunds Stiftelse sr. We thank Jari Lipsanen for statistical consultancy, Esko Ruuskanen for his assistance in building the tools for raw data analysis, Viljami Salmela for consultations on visual perception, and Kimmo Alho and Daniel Villarreal for their assistance in proofreading the manuscript. We also thank our colleagues who assisted in the recruitment of their patients to the study and the participants who generously gave their time to take part in this research.
Conflict of Interest
The authors have no conflicts of interest to disclose.
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