Impact of post-stroke unilateral spatial neglect on goal-directed arm movements: systematic literature review.

Impact of post-stroke unilateral spatial neglect on goal-directed arm movements: systematic literature review Tatiana Ogourtsova, Philippe Archambault, Anouk Lamontagne McGill University, Montreal, QC, Canada Background: Unilateral spatial neglect (USN), a highly prevalent post-stroke impairment, refers to one’s inability to orient or respond to stimuli located in the contralesional visual hemispace. Unilateral spatial neglect has been shown to strongly affect motor performance in functional activities, including non-affected upper extremity (UE) movements. To date, our understanding of the effects of USN on goal-directed UE movements is limited and comparing performance of individuals post-stroke with and without USN is required. Objective: To determine, in individuals with stroke, how does the presence of USN, in comparison to the absence of USN, impacts different types of goal-directed movements of the non-affected UE. Methods: The present review approach consisted of a comprehensive literature search, an assessment of the quality of the selected studies and qualitative data analysis. Results: A total of 20 studies of moderate to high quality were selected. The USN-specific impairments were found in tasks that required a perceptual, memory-guided or delayed actions, and fewer impairments were found in tasks that required an immediate action to a predefined target. Conclusion: The results indicate that USN contributes to deficits observed in action execution with the non-effected UE that requires greater perceptual demands. Keywords: Hemineglect, Cerebrovascular accident, Arm, Goal-directed movement, Reaching, Pointing, Kinematics

Introduction One of the most serious visual perceptual post-stroke deficits is unilateral spatial neglect (USN), which is experienced by 23–46% of stroke survivors. Unilateral spatial neglect is characterized by the inability to orient, respond, or report to the stimuli appearing on the contralesional side.1 Unilateral spatial neglect is most common following a right hemisphere stroke (RHS) rather than a left hemisphere stroke, with the reported incidence of USN among patients with RHS ranging from 13 to 81%.2 Although 20–45% of USN resolves spontaneously within the acute post-stroke period, for the remainder, it can become long-standing and introduce major disability, activity restrictions,3 and reduced quality of life.4 Individuals with poststroke USN have longer rehabilitation stays, are at lower levels of independence post-discharge, have greater difficulty performing activities of daily living, are at higher risk of functional deterioration at 1 year,3 and are more prone to frequent falls1 than individuals without post-stroke USN. In addition to its

Correspondence to: Tatiana Ogourtsova, McGill University, Montreal, QC, Canada. Email: [email protected] ß W. S. Maney & Son Ltd 2015

DOI 10.1179/1074935714Z.0000000046

obvious burden on the patient, USN is also known to place a major burden on the family/caregivers.3,5 While several rehabilitation strategies for USN are available, the efficacy and effectiveness of those are still questionable. As suggested by recently completed meta-analyses, there is a limited number of high-quality studies suggesting that USN interventions are highly effective in improving functional outcomes and reducing disability.6–8 This may be explained by the high heterogeneity of USN’s neurological basis. For instance, damage to the angular gyrus, right inferior parietal lobe, parahippocampal region,9 and the right superior temporal cortex10 have all been identified as critical brain areas responsible for USN. In addition, USN can vary in its clinical presentation (e.g. in near personal but not for far-extrapersonal spaces11). In fact, a recent study found that the majority of individuals with USN present with neglect symptoms within the near-reaching space rather than far-reaching space.12 Based on this observation, it can be hypothesized that USN has a significant effect on one’s functional performance within the near-reaching space. Also, given that individuals with USN often present with concurrent contralesional Topics in Stroke Rehabilitation

2015

VOL .

22

NO .

6

3971

Ogourtsova et al.

Impact of post-stroke unilateral spatial neglect on goal-directed arm movements

hemiparesis or hemiplegia of the upper extremity (UE), it results in a predominant use of the ipsilesional UE to accomplish functional tasks within the near - reaching space. While it is clear that USN can affect one’s functional performance in even the simplest everyday tasks that require UE use (e.g. brushing only the right side of the head or eating from the right side of the plate, etc.), questions remain as to how this complex and multi-factorial disorder impacts the specific UE movement impairments underlying these activity limitations. Since the 80s, a significant body of literature has addressed this issue to enhance our knowledge and understanding of USN’s underlying mechanisms and refine or develop effective treatment strategies and evaluation methods. The body of research on goal-directed UE movements in individuals with post-stroke USN has been reviewed in the past and later contested for its conclusions. More precisely, while the review by Coulthard et al.13 argued that individuals with post-stroke USN do present with deficits in goaldirected ipsilesional UE movements, others contended that those deficits are not necessarily ‘‘USN-specific’’ and may be attributed to the effect of the actual brain damage,14 given that the reviewed studies by Coulthard et al.,13 included comparisons with healthy control individuals only and not with stroke survivors without USN. Another issue that remains unclear is whether the distinct types of goal-directed movements are differentially altered by post-stroke USN. Current literature has addressed a variety of goal-directed arm movements that could be categorized into two main categories: (1) movements that involve memory-guided/delayed components or otherwise called off-line actions and (2) movements that involve immediate type of component or otherwise called online actions (see Appendix 1 for details). The off-line actions are suggested to differ from online actions in that they implicate the use of relational metrics, scene-based coordinates, and working memory, whereas the online or immediate actions involve a simple response directed toward a predefined target. It is further hypothesized that different visuomotor streams are involved in the processing of off-line versus online type of actions. Research in healthy individuals suggests that the ventral stream is employed in off-line tasks, whereas the dorsal stream sub-serves online movements (reviewed in Ref. 15). A few recent studies also investigated whether the performance on off-line versus online tasks differs in individuals with post-stroke USN (e.g. Refs. 15–17), suggesting a higher impact of USN on off-line, rather than on online tasks, that tap into ventral processing stream. 398 2

Topics in Stroke Rehabilitation

2015

VOL .

22

NO .

6

Therefore, in addition to understand the impact of USN on goal-directed UE movement, it is also relevant to examine its effects on the two different movement types. The following question presents the goal of this review in PICO format (population, intervention/ exposure, comparison, and outcome). In individuals with RHS (P), how does the presence of left USN (I), in comparison to the absence of USN (C), impacts offline versus online goal-directed movement of the nonparetic UE (O)?

Methods The present systematic review approach consisted of a comprehensive literature search, a transparent study selection and data extraction, an assessment of the quality of the selected studies, and a categorization of studies according to movement type (off-line or online; see Appendix 1).

Search strategy Description of electronic databases Nine (n59) scientific databases available through McGill University library were systematically searched using their online search engines. The databases included (1) MEDLINE (Medical Literature Analysis and Retrieval System Online: from 1946 to 31 December 2013), (2) CINAHL (Cumulative Index to Nursing and Allied Health Literature: from 1989 to 31 December 2013), (3) EMBASE (Excerpta Medica Database: from 1947 to 31 December 2013), (4) Cochrane CENTRAL (Central Register of Controlled Trials: 31 December 2013), (5) Cochrane Database of Systematic Reviews (31 December 2013), (6) REHABDATA (Disability and Rehabilitation Literature Database: 31 December 2013), (7) PEDro (Physiotherapy Evidence Database: 31 December 2013), (8) AMED (Allied and Complementary Medicine Database: from 1985 to December 2013), and (9) PsychINFO (Psychological Information Database: from 1967 to Week 4 of December 2013). No start date limit was set on the search criteria of the databases, unless the database had an already existing start date. The end date was set to 31 December 2013. Approach to database search Search terms were developed by reviewing the literature found in previous reviews of USN and visuomotor control.13,18 The following keywords were used in the searches, and the corresponding Medical Subject Headings (MeSH) terms (Appendix 2) were selected and ‘‘exploded’’ during the search. The search strategy was the following (* for truncation):

Ogourtsova et al.

N N N N

Search 1: Cerebrovascular Accident, Cerebral Vascular Accident, CVA, Stroke* (combined by OR operator); Search 2: USN, Hemispatial Neglect, Neglect, Visual Neglect, Hemineglect, Hemi-inattention, Perceptual Disorders* (combined by OR operator); Search 3: UE Movement, Arm*, Movement*, UE*; Reaching, Grasping, Pointing, Movement Time, Reaction Time, Visuomotor, Psychomotor Performance, Kinematics (combined by OR operator); and Final search: (Search 1) AND (Search 2) AND (Search 3).

Following the electronic database search, a manual search of the reference lists of all relevant studies and existing reviews was conducted to ensure the completeness of the search. Moreover, the main recognized journals publishing on stroke and USN (Neuropsychologia, Neurology, Stroke, Behavioral Neurology, Brain Cognition, Topics in Stroke Rehabilitation, and Cerebral Cortex) were searched for the keywords. Lastly, to minimize the possibility of publication bias, the gray literature (unpublished or unindexed reports, conference proceedings, non-index journals, internal reports, and student dissertation/theses) was scanned for possible suitable reports in the following search engines: Google, Yahoo, and Bing.

Study selection criteria All the found citations from the databases were saved into EndNote X7 1988–2013 reference manager, where duplicates were removed. The study selection process consisted of four phases: (1) review of all identified studies by the electronic databases on the basis of their titles and abstracts; (2) review of the full texts of all selected studies in phase (1); (3) review of all relevant titles from the reference lists of the selected articles in phase (2), main publishing journals, and gray literature; and (4) selection of articles from phase (3) based on their full texts. Studies were included in the present review if the following conditions were met: Type of publication: The review was limited to English-written reports on human subjects. Type of studies: Observational/analytical studies (e.g. cross-sectional studies) investigating the effects of USN on goal-directed UE movement were included. Published literature reviews, clinical trials of treatment, case reports, case series, and letters to editors were excluded. Population: Only studies of adults (aged i18 years with no upper age limit) were included. Exposure: Studies with the main exposure variable as the presence versus absence of RHS and left USN were included. Studies including healthy control individuals as the only comparison group were excluded from the review.

N N N N

N


Outcome: Studies were included if non-affected UE goal-directed movement outcomes were compared between the groups with (USNz) and without (USN{) post-stroke.

Methodological quality assessment Quality assessment scale The modified Quality Index was chosen for the quality assessment of the studies in this review. It is a modified-scale checklist for assessing cross-sectional studies from the originally developed Quality Index checklist19 and the quality assessment scale by Crombie.20,21 The Quality Index was rigorously studied for its psychometric properties in the quality assessment of randomized and non-randomized (case–control and cohort) studies.19 Later, validity results and high intra-rater reliability (kappa values w0.70) values were reported for the modified Quality Index in assessing cross-sectional studies.21 The scale was selected for the present review given its previous applications in quality assessment of observational research, careful development, and strong psychometric properties. When the modified Quality Index is used to assess the quality of cross-sectional studies, the maximum obtainable score is 20 points, where criteria are scored as 1 for ‘‘yes,’’ 0 for ‘‘no’’ or ‘‘unable to determine,’’ where unclear or insufficient information was provided on a specific criterion. Overall level of evidence The approach of using only a numerical summary of a quality assessment tool such as the modified Quality Index to determine the overall level of evidence has been critiqued before due to high discrepancies in the determination and weighting of its individual components.22 Therefore, the system from the Scottish Intercollegiate Guidelines Network Methodology (SIGN)23 was used to summarize the level of evidence for each selected study as follows: (A) ‘‘zz’’ when all, or most of the quality criteria are fulfilled (i80%); (B) ‘‘z’’ when some of the criteria are fulfilled (50–79%); and (C) ‘‘{’’ when few or none of the criteria are fulfilled (v50%). Group (A) corresponded to highquality studies, group (B) to moderate-quality studies;, and group (C) to low-quality studies. It is acknowledged that the SIGN methodology can be subjective; thus, we also set a percentage criterion, as described above, to assist the rating.

Data extraction The studies fulfilling the inclusion criteria were used to extract data into data collection forms. Data extraction was performed by one investigator only (TO). The following data were extracted: Topics in Stroke Rehabilitation

2015

VOL .

22

NO .

6

3993

Ogourtsova et al.

N N N N


Study: design, year of study, quality, type of movement (online vs off-line as per Appendix 1) aim of study/testing paradigm; Population: sample size in each group studied, participant’s characteristics including mean age, sex, stroke location, time since stroke onset; Exposure and outcome variables description, assessment and results; (mean and standard deviations of the outcome measures, statistically significant differences in outcome measures between the USNz and the USN{ groups); Statistical analysis and findings/conclusions.

Systematic Search Result (n = 1,022) • • • • • • • • •

*duplicates automatically removed by OVID engine

Categorization of studies and data analysis All UE movement outcomes in each selected study were included in our analysis. For instance, outcomes included movement kinematic parameters related to velocity/speed (e.g. movement time, peak velocity, etc.), acceleration (e.g. peak acceleration, deceleration, etc.), movement stability measures (e.g. grip aperture), and end-point/trajectory accuracy measures (e.g. absolute angular error, directional error, and constant error/ accuracy in responses, hand path curvature, and curvature index). Outcomes were considered significantly different between groups with and without USN if: (1) the reported P-value was v0.05; (2) the author reported that an association was statistically significant; or (3) the 95% confidence intervals around a rate ratio or similar statistic did not include 1. For the groups with and without USN only, the means and standard deviations of the outcome variables were extracted from each study. In the event of missing information, study authors were contacted by email. Two effect sizes were calculated using the extracted means and standard deviations (Cohen’s d statistic): (1) for each outcome within a study; and (2) for the overall mean effect size for a study, combining the multiple outcomes.24 Meta-analyses were not performed given the high number of outcomes and the high heterogeneity in the experimental paradigms of each study (e.g. pointing vs grasping, middle vs lateral targets). Each study was assessed for its type of movement: off-line or online (see Appendix 1 for details).

Results Study selection Figure 1 describes the selection process of the observational studies included in this review. Twenty (n520) studies were included in the final review: two cross-sectional studies on pressing movements, seven cross-sectional studies on pointing movements, four cross-sectional studies on the perceptual judgment of pointing/bisecting movements, two cross-sectional studies on reaching movements, four cross-sectional studies on grasping, and one cross400 4


2015

VOL .

22

NO .

6

MEDLINE* (n = 392) CINAHL (n = 125) EMBASE* (n = 245) Cochrane databases (n = 66) REHABDATA (n = 15) PEDro (n = 59) AMED* (n = 14) PsychINFO* (n = 86) Hand screening of journals/grey literature search (n = 20)

41 retained after duplicates removal by EndNoteX7 and title and abstract screening

21 articles excluded following full texts review: • • • • • •

Only healthy control group as comparison (n = 4) No outcome of interest (n = 4) Case-report or case series (n = 5) Patient selection criteria (n = 4) No between group comparisons performed, no data available (n = 2) Review articles (n = 3)

20 retained for the systematic review: • • • • • •

2 cross-sectional studies on pressing 2 cross-sectional studies on reaching 7 cross-sectional studies on pointing 4 cross-sectional studies on grasping 1 cross-sectional study on moving object in a horizontal plane 4 cross-sectional studies on perceptual judgement action

Figure 1 Flow diagram of the selection process of studies.

sectional study on moving an object in a horizontal plane. All included studies are published peerreviewed articles. Table 1 lists the excluded studies and reasons for exclusion.

Study characteristics Table 2 describes each selected study in terms of its year, design, sample size for each group, demographics of study participants, the assessment method of the exposure variable (presence of USN) and the outcome variable (goal-directed UE movement). All the selected studies were identified as being cross-sectional, analytical/observational studies in which two groups or more

Ogourtsova et al.


Table 1 Excluded studies and reasons for exclusion Study

Reason for exclusion

From reference list Behrmann & Meegan50 Fisk & Goodale51

Healthy controls comparison only Patient selection: patients were not selected on the basis of USN presence or absence and therefore between-group differences in USNz and USN– participants were not calculated Patient selection: individuals with RHS that recovered from USN Goodale et al.52 No between-group analysis performed on the outcome of interest Harvey et al.53 54 Healthy controls comparison only Konczak et al. Healthy controls comparison only Mattingley et al.55 Meador et al.56 Patient selection: patients were selected and analyzed on the basis of a right hemisphere brain damage and not presence vs absence of USN, and compared with health control individuals only Case report Milner et al.57 Case report Pritchard et al.58 Case series Robertson et al.59 60 Brain function analysis of participants in Rossit et al.17 Rossit et al. From selected articles by abstract and title Review Harvey & Rossit18 Patient selection – patients with left-sided stroke only Bartolomeo et al.61 Case series Coslett62 Coulthard et al.13 Review Case report Edwards & Humphreys63 Gall et al.64 Absence of outcome of interest – eye movement recordings only A comment to Coulthard et al.13 Himmelbach et al.14 65 Maeshima et al. Absence of outcome of interest – assessment of lesion extent and presence of USN components 66 Healthy controls comparison only McIntosh et al. No between-group analysis performed on the outcome of interest, no data is provided for Tegner & Levander67 USN{ group (unable to reach author for missing information). USN: Unilateral spatial neglect; RHS: right hemisphere stroke.

of individuals were tested at one point in time for the exposure and the outcome variables; and results were compared between groups. The sample size in the studies ranged from 4 to 18 individuals with USN and from 3 to 20 individuals without USN. All but one study (Wu et al.)25 included a healthy control group comparison. The age of study participants with USN ranged from 52.5+ 17.1 (mean+ 1SD) to 69.7+ 9.3 years and from 46.6+ 17.9 to 68.8+ 7.7 years for participants without USN. The time since stroke ranged from an acute period (4.1+ 2.4 and 3.8+ 1.5 days post-stroke for the group with and without USN, respectively) to a chronic period (30.0+ 24.6 and 18.7+ 13.1 months post-stroke for the group with and without USN, respectively). Unilateral spatial neglect was measured using standardized assessment tools, such as the Line Bisection Test and the Behavioral Inattention Test. The outcome measures were determined via distance/time calculations, and/or tracking devices/motion analysis systems with markers on different body landmarks of the UE.

Methodological quality assessment The results of the methodological quality assessment using the modified Quality Index are summarized in Table 3. Fifteen studies were rated as high-quality studies and five as moderate-quality studies.

The modified Quality Index ranged from 14 to 17. All the selected studies described (1) the hypothesis/ objective/aim, (2) study setting and design, (3) source of subjects, (4) stated the sample size, (5) participation/follow-up rates, (6) non-participants/subjects lost to follow-up, (7) the study findings, (8) stated conclusions, (9) included subjects who were representational of the entire population, (10) demonstrated w80% participation rate, and (11) accurately measured the outcomes. On the other hand, none of the studies justified the sample size, provided confidence intervals, and described efforts to increase follow-up rates/participation. Only 15% of studies provided actual probability values (e.g. 0.035 rather than v0.05) for the main outcomes. The outcomes were described in the section Introduction or Methods of all but one study.26

Qualitative analysis Table 4 displays the results of each selected study for distinct UE movements (pressing, pointing, reaching, grasping, and moving an object). This table includes the description of the testing paradigm, UE movement category, outcomes being measured, outcome results for the USNz and USN{ groups, findings and their P-values, the effect size for each outcome and for the overall study (where possible). Topics in Stroke Rehabilitation

2015

VOL .

22

NO .

6

5 401

402 6


2015

VOL .

22

NO .

18 (11/7)

14 (11/3)

USNz

6

8 (2/6)

5 (4/1)

Harvey et al.27

Heilman et al.28

Pointing Chokron & 6 (6/0) Bartolomeo35

Mattingley et al.34

Pressing Bartolomeo et al.33

Study (year)

12 (6/6) RHS; 12 (6/6) LHS 5 (5/0) LHS

6 (6/0)

6 (5/1)

20 (16/4)

USN{

9 (N/A)

12 (4/8)

10 (N/A)

23 (14/9)

15 (3/12)

Healthy Controls

N (Sex (M/F))

Table 2 Description of studies

64+ 10.21

USN{

UTD

65.8+ 6.2; 58.4+ 12.3 58.6+ 6.26

UTD

67.5+ 8.6 48+ 10.29

USNz

USN{

Months/{weeks} ‘‘days’’, poststroke mean+ SD or (range)

N/A

66.2+ 3.8

UTD

N/A

5.4+ 3.4

UTD

{13.11 + 15.71}

N/A

9.5+ 5.3; 12.1+ 6.4

UTD

{11.83 + 10.94}

58.33+ 19.03 168.07 + 213.73 98.65 + 124.79

Healthy Controls

64.11+ 13.39 53.83 + 12.68 57.8+ 12.69

60.4+ 14.57

USNz

Age (years), mean+ SD (range)

USN{

2 T-P, 1 F-P, 1 Ps, 1 P-Ic

2 P, 2 F-P, 1 NA. 1 T-P, 1 F

UTD

2 Ps, 1 F, 1 T-P, 1 P-SubC

N/A

UTD

8 F-P, 2TP, 2 IcBG, 2 P, 1 Ic-Th, 1 P-I, 1 T-O, 1 F-T-BG, 1 F-T-PBG 2 P, 2 T-P, 2 O- 1 P-IcLentiN-Th, P, 1 LentiNCorona Radiata, 1 F-T-IcLentiN, 1 1 PerivN, 1 T-P, 1 FLentiN, 1 FP, 1 IcIntC,-LenitN, 1 LentiNF-P, 1 Corona Radiata-LentN- CaudN, 1 P CaudN, 1 T-PO, 1 F, 1 O-P, 1 F-P-Ic-Corona Radiata, 1 IcCaudN-LentiN, 1 F-P-T-Corona Radiata 3 T-P, 3 F-P, 2 T-O, 1 Th, 1 P, 1 Ic-Th, 1 F-T-P, 1 Ic-BG, 1 O-Th

USNz

Lesion location

Distance from midpoint calculations and digital logic system incorporated into the apparatus.

Digital logic system incorporated into the apparatus

Response time measurement incorporated into the computer

Outcome assessment

Bisection data calculation/deviation measurement Distance from Line bisection midpoint test or the cancellation test calculations

Battery of visuospatial tests which included line cancellation, identification or overlapping figures, and line bisection. Behavioral inattention yest

Line cancellation, circle cancellation task, star cancellation task from the behavioral inattention test

Line cancellation, identification of overlapping figures and line bisection

USN assessment

Ogourtsova et al.


5 (2/3)

Konczak & Karnath37

8 (3/5)

5 (2/3)

Karnath et al.42

Mattingley et al.30

6 (3/3)

USNz

Himmelbach & Karnath36

Study (year)

Table 2 Continued

8 (3/5)

5 (2/3)

5 (2/3)

7 (5/2)

USN{

8 (N/A)

6 (N/A)

6 (N/A)

9 (N/A)

Healthy Controls

N (Sex (M/F))

56+ 10.4

52.8+ 27.22

52.8+ 27.2

62+ 14.45

62+ 14.5

69.75+ 9.36

63 (53–80)

62.23+ 18.56 59+ 13.79

63.62+ 12.65 69.1+ N/A

56+ 10.4

Healthy Controls

USN{

USNz


USN{

4.13+ 2.41

16.4+ 11.58

16.4+ 11.58

3.87+ 1.55

81.2+ 155.91

81.2+ 155.91

105.33 + 170.07 8.43+ 4.68

USNz


1 BG, 2 BG-T, 1 2 MCA, 3 P-O, 1 F, 1 BG- P, 1 O-T, 1 T, 1 TIc, 1 F-T, 1 P BG

Albert’s line cancellation test, star cancellation from the behavioral inattention test, and line bisection test

2 T-P, 1 F-T-P, 1 1 T-P, 1 T, Letter F-P, 1 Thalamus 1 BG, 2 F cancellation, line bisection, copying and clock face tests

2 P, 1 T-I, 2 BG, 1 F, 1 F-T-IBG

USN{

USN assessment

Letter cancellation, Bell’s test, baking tray task and copying test 2 T-P, 1 F-T-P, 1 1 T-P, 1 T, Letter F-P, 1 Thalamus 1 BG, 2 F cancellation, line bisection, copying and clock face tests 1 F-T-P, 1 T-P-I, 1 F-P, 1 F-T-PBG-I, 1 TH, 1 BG

USNz

Lesion location

Opto-electric 3D camera system with markers on the shoulder, elbow, wrist, and base of the index finger Opto-electric 3D camera system with markers on the shoulder, elbow, wrist, and base of the index finger Digital logic system incorporated into the apparatus

Ultrasonic 3D tracking device with a marker at the tip of the index finger

Outcome assessment

Ogourtsova et al.



2015

VOL .

22

NO .

6

4037

404 8


2015

VOL .

22

NO .

6

11 (3/8)

11 (4/7)

Rossit et al.15

9 (3/6)

8 (5/3)

Rossit et al.32

Rossit et al. (2009a)17

Richard et al.29

USNz

Continued

Study (year)

Table 2

10 (7/3)

9 (6/3)

10 (7/3)

8 (3/5)

USN{

10 (N/A)

10 (N/A)

10 (N/A)

8 (N/A)

Healthy Controls

N (Sex (M/F))

USN{

Healthy Controls

67.2+ 7.8

66.5+ 7.7

66.5+ 8.0

68.8+ 7.7

66.8+ 7.7

66.3+ 6.2

72.3+ 4.4

71.0+ 4.8

72.1+ 4.2

61.12 + 12.44 52.12 + 13.61 54+ N/A

USNz


8.9+ 8.0

7.72+ 7.66

9.33+ 8.33

59.62+ 45.08

USNz

5.4+ 2.2

5.77+ 3.56

5.6+ 2.36

89.37 + 74.75

USN{


USN{

Outcome assessment

Behavioral inattention test, balloons test, line bisection test

Distance from Bell’s midpoint cancellation calculations test, line bisection test, and scene copy test

USN assessment

Electromagnetic motion analysis system and a marker on the tip of the right index finger Electromagnetic Behavioral motion analysis inattention test system and a or significant marker on the tip of rightward the right index bisection error or impairment in finger a lateralized manner in the subtest B of the balloons test Electromagnetic 2 BG; 2 F- Behavioral 2 F-T-P; 1 T-O, motion analysis inattention test 1 F-T-P-Ins; 1 F- T; 1 system and a T-O, 1 T-P, 1 F- LentiN; 1 or significant marker on the tip of rightward F-PostT; 1 F-P, 1 Tthe right index Ins-PeriV White temporal- bisection error Matter; 1 F-T-P- P; 1 P-O; or impairment in finger 1 CaudN; a lateralized O; 1 F-T-Ins; 1 LentiN, manner in the subtest B of the 1 F; balloons test

2 Ic-S; 1 F-P-R; 1 CO-Ic-S; 1 F-R-CO; 1 F-P-T-R; 1 F-P-T-RCO-Ic-S; 1 P-T-RIc-S-Th 2 BG, 1 F, 2 T-P, 1 T-Ic2 F-T, 2 PeriV White Matter, 1 F-T-P- LentiNuc, 1 P-O, 1 Ins, 1 F-T, 1 FCaudN, 1 T-Ins, 1 F-T-O, 1 F-T-P-O, 1 TO F-T-P 2 BG, 2 F2 F-T-P, 1 T-O, 1 F-T-P-Ins, 1 F- T, 1 T-P, 1 T-P, 1 F- LentiN, 1 DF-PT-P, T, 1 F-P, 1 TInsC-Periv white 1 CaudN, 1 LentiN, matter, 1 F-T1F Ins, 1 DF-OCorona Radiata 2 F-P-T-R-OCO-Ic-S; 1 F-PT-R-O-CO; 1 TIc-S-Th; 1 P-TO-CO; 1 F-P-TR-CO; 1 Ic

USNz

Lesion location

Ogourtsova et al.


7 (N/A)

Wu et al.25


6 (6/0)

3 (2/1)

3 (N/A)

Farne et al.31 4 (N/A)

Marotta et al.26

3 (5/2 USNz and USN{)

8 (N/A) RHS; 12 (N/A) LHS

8 (5/3)

USN{

6 (3/3)

6 Elderly and 6 Young (N/A)

5 (N/A)

0

8 (N/A)

Healthy Controls

N (Sex (M/F))

4 (5/2 USNz and USN{)

Grasping Harvey et al.39,53

7 (2/5)

Reaching Rossit et al.38

USNz

Continued

Study (year)

Table 2

46.66+

59.33+ 3.05

52.5+ 17.13

67.33 + 6.28

68+ 9.7

63+ N/A

63+ N/A

68+ 9.7

62.5+ 10.3

USN{

68.1+ 9.5

USNz

64+ N/A

55 (Elderly) and 23 (Young)

68+ 5.7

N/A

72.9+ 4.3

Healthy Controls


(0.1–9.4)

8+ 5.97

USN{

N/A

2 F-T-P-O, 1 P, 1 F-T-O, 1 F-T, 1 F-AnT-Ins, 1 T-INsC-Periv white matter

USNz

N/A

3.5+ 2.3

N/A

26.66+ 41.86

1 P, 1 F-T Th BG, 1 F-T

1 Ic, Th, 1 F-TP, 1 F-T-P , BG

Behavioral inattention test

Subtest of the behavioral inattention test, or significant rightward bisection error or subtest B of the balloons test Line bisection test

USN assessment

1 Ic, Th, 1 Line, letter and bell’s F-T-P, 1 F-T-P, BG cancellation test, line bisection and drawing form a model test. 1 P, 1 F-T Behavioral Th BG, 1 inattention test F-T

1 T-P, 1 F-P, 1 S-P

N/A

2 BG, 2 FT-P, 1 BG-T, 1 P-O, 1 FT-P, 1 FIns-T-P, 1 T-P

USN{

Lesion location

740.75+ 482.53 341.66 + 252.30 1 T-P, 1 F-P, 1 S-P

(0.1–9.4)

8.42+ 8.54

USNz


Grasp stability: grasp line measurement

Infrared motion analysis system with markers placed on the distal portion of the index, thumb and wrist of the right hand Optotrak 3020 system with markers on the index and the thumb

6-camera motion analysis system with markers on the fifth metacarpal of the hand and the target

Electromagnetic motion analysis system and a marker on the tip of the right index finger

Outcome assessment

Ogourtsova et al.


2015

VOL .

22

NO .

6

4059

406 10


2015

VOL .

22

NO .

6

7 (0/7)

7 (4/3)

USN{ 65.9+ 10.5

USN{

53.16+ 12.59 52+ 21.77

68.6+ 5

USNz

N/A

68.5+ 5.0

Healthy Controls


N/A

30+ 24.67

USNz

N/A

18. 71+ 13.14

USN{


USN assessment

Line bisection and line cancellation

1 BG, 2 F- Line crossing, star P, 1 P, 1 cancellation, T-P, 2 F figure copying, representational drawing and line bisection

USN{

2P, 1 F-P, 1 F-T- 3 F-P, 1 T-P, 1 F, P, 1 P-BGCorona Radiata, 2 N/A 1F

1 BG, 2 F-P, 1 P, 1 T-P, 2 F

USNz

Lesion location

Digital logic system incorporated into the apparatus

Opto-electronic movement analysis system or a portable electromagnetic movement analysis system with infrared or magnetic markers attached to the distal phalanxes of the right index finger and thumb

Outcome assessment

N/A: not available; USNz: presence of unilateral spatial neglect; USN{: absence of unilateral spatial neglect; SD: standard deviation; T: temporal; P: parietal; F: frontal; O: occipital; Ic: internal capsule; BG: basal ganglia; I: inferior; Subc: subcortical; PS: perisylvian lesion; LentiN: lentiform nucleus; PerivN: periventricular nucleus; CaudN: caudate nucleus; MCA: middle cerebral artery region; CO: centrum ovale; S: striatum; Ins: insular; Periv: periventricular; An: anterior; DF: dorsal frontal; InsC: insular cortex; RHS: right hemisphere stroke; LHS: left hemisphere stroke; UTD: unable to determine.

12 (N/A)

10 (N/A)

Healthy Controls

N (Sex (M/F))

Moving object in horizontal plane Heilman 6 (N/A) 7 (LHS, et al.41 sex distribut ion N/A)

McIntosh et al.40

USNz

Continued

Study (year)

Table 2

Ogourtsova et al.


Topics in Stroke Rehabilitation Yes Yes

No 16 High

No 16 High

Yes

Yes

Yes

Yes

Yes

Yes

UTD

UTD

Yes

Yes

Yes

Yes

No

Yes Yes

Yes Yes

No

Yes

Yes

No Yes Yes

Yes

Yes

No

Yes

Yes

No Yes Yes

Yes

Yes

Yes

No 16 High

Yes

Yes

Yes

No Yes Yes

Yes

UTD

Yes

Yes Yes

Yes

Yes

Yes

Yes

Yes

Yes

Yes

Yes

Yes

Harvey & Milner27

Yes

Mattingley et al.34

Items related to reporting quality: 1, 2, 3, 4, 5, 6, 7, 9, 10, 11, 13, 14, 15; Items related to external validity: 16, 17; Items related to internal validity – bias: 19; Items related to confounding – selection bias: 8; Items related to power: 20, 18. UTD: unable to determine.

1. Hypothesis/aim/objective statement 2. Description of main outcomes in the Introduction or Methods section 3. Description of study design 4. Description of study setting 5. Source of subjects statement 6. Study population described by age and gender 7. Sample size statement 8. Participation/follow-up rates statement 9. Non-participants/subjects lost to follow-up description 10. Efforts to increase the participation/follow-up rate description 11. Clear description of main study findings 12. Description of statistical methods 13. Actual probability values report for the main outcomes 14. Confidence intervals report 15. Conclusion statement 16. Subjects’ asked to participate in the study representation of the entire population from which they were recruited 17. Subjects’ prepared to participate representation of the entire population from which they were recruited 18. Participation/follow-up rate w80% 19. Accurate measurement of the main outcomes measured 20. Sample size justification TOTAL (out of 20) STUDY QUALITY

Bartolomeo et al.33

Table 3 Individual study quality assessment

No 15 Moderate

Yes

Yes

Yes

No Yes Yes

No

No

Yes

UTD

Yes

Yes Yes

Yes

Yes

Yes

Yes

Yes

Yes

Heilman et al.28

No 17 High

Yes

Yes

Yes

No Yes Yes

Yes

Yes

Yes

UTD

Yes

Yes Yes

Yes

Yes

Yes

Yes

Yes

Yes

Richard et al.29

No 154 Moderate

Yes

Yes

Yes

No Yes Yes

No

Yes

Yes

UTD

Yes

Yes Yes

UTD

Yes

Yes

Yes

Yes

Yes

Chokron & Bartolomeo35

No 16 High

Yes

Yes

Yes

No Yes Yes

No

Yes

Yes

UTD

Yes

Yes Yes

Yes

Yes

Yes

Yes

Yes

Yes

Himmelbach & Karnath36

No 16 High

Yes

Yes

Yes

No Yes Yes

No

Yes

Yes

UTD

Yes

Yes Yes

Yes

Yes

Yes

Yes

Yes

Yes

Karnath et al.42

No 17 High

Yes

Yes

Yes

No Yes Yes

Yes

Yes

Yes

UTD

Yes

Yes Yes

Yes

Yes

Yes

Yes

Yes

Yes

Konczak & Karnath37

No 16 High

Yes

Yes

Yes

No Yes Yes

No

Yes

Yes

UTD

Yes

Yes Yes

Yes

Yes

Yes

Yes

Yes

Yes

Rossit et al.15,32

No 16 High

Yes

Yes

Yes

No Yes Yes

No

Yes

Yes

UTD

Yes

Yes Yes

Yes

Yes

Yes

Yes

Yes

Yes

Mattingley et al.30

No 16 High

Yes

Yes

Yes

No Yes Yes

No

Yes

Yes

UTD

Yes

Yes Yes

Yes

Yes

Yes

Yes

Yes

Yes

Rossit et al.17

No 16 High

Yes

Yes

Yes

No Yes Yes

No

Yes

Yes

UTD

Yes

Yes Yes

Yes

Yes

Yes

Yes

Yes

Yes

Rossit et al.38

No 16 High

Yes

Yes

Yes

No Yes Yes

No

Yes

Yes

UTD

Yes

Yes Yes

Yes

Yes

Yes

Yes

Yes

Yes

Wu et al.25

No 16 High

Yes

Yes

Yes

No Yes Yes

No

Yes

Yes

UTD

Yes

Yes Yes

Yes

Yes

Yes

Yes

Yes

Yes

Harvey et al.39,53

No 16 High

Yes

Yes

Yes

No Yes Yes

No

Yes

Yes

UTD

Yes

Yes Yes

Yes

Yes

Yes

Yes

Yes

Yes

Farne et al.31

No 14 Moderate

Yes

Yes

Yes

No Yes Yes

No

No

Yes

UTD

Yes

Yes Yes

Yes

Yes

Yes

Yes

No

Yes

Marotta et al.26

No 16 High

Yes

Yes

Yes

No Yes Yes

Yes

Yes

Yes

UTD

Yes

Yes Yes

Yes

Yes

Yes

Yes

Yes

Yes

McIntosh et al.40

No 15 Moderate

Yes

Yes

Yes

No Yes Yes

No

Yes

Yes

UTD

Yes

Yes Yes

No

Yes

Yes

Yes

Yes

Yes

Heilman et al.41

Ogourtsova et al.


2015

VOL .

22

NO .

6

11 407

408 12

Testing paradigm


2015

VOL .

22

NO .

6

Mattingley et al.34 HIGH (15.29) B

Response time (milliseconds): 1. LTCM left (0.8) 2. LTCM right (0.6) 3. CTLM left (1.4) 4. CTLM right (1.4)

Outcome variables (effect size)

Percentage of accuracy/correct responses (%): 1. LTCM left (N/A, no SD available) 2. LTCM right (N/A, no SD available) 3. CTLM left (N/A, no SD available) 4. CTLM right (N/A, no SD available) Pressing a button (located Kinematic parameters: at the 1. Reaction time annulus at the base of left/rightward each visual movement (milliseconds) cue) with right index finger (15.8/9.19) in 2. Movement time response to appearing left/rightward visual cues; movement (milliseconds) thus, producing left or (24.4/11.8) rightward movements across the body’s midline.

A. Results from Studies – Pressing. 1. Lateral targets/central Bartolomeo et al.33 movement: HIGH (1.05) pressing (LTCM) the B computer spacebar (central response) with the right index finger as quickly as possible to the response of a right- or a left-sided target (black circles) appearance. 2. Center targets/lateral movement (CTLM): moving the right hand from a central position of the keyboard to the right or to the left upon the appearance of a midline target.

Type (A vs. B)

Quality (mean effect size)

Study (year)

Table 4 Results from studies – pressing

1. *96 2. *98 3. *90 4. *91

1. *109+ 5/104+ 5 2. 410+ 5/448+ 5

1. *188+ 5/139+ 5 2. *532+ 5/507+ 5

1. *1200+ 500 2. *900+ 500 3. *1700+ 500 4. *1600+ 500

USN{

1. *86 2. *98 3. *77 4. *82

1. *1600+ 500 2. *1200+ 500 3. *2400+ 500 4. *2300+ 500

USNz

1. (N/A) – USNz group is slower to initiate movements than controls; and this for leftward more than for rightward targets; 2. (N/A) – USNz group is slower to execute movements than controls; Note: All comparisons made with the healthy control group only that failed to show any significant differences with the USN{ group.

1. ({) 2. (z) – USNz group showed more correct responses to the right-sided targets; 3. ({) 4. (z) – USNz group shower more correct responses to the right-sided targets;

1. (z) – USN group were slower for left-sided targets; 2. ({) 3. ({) 4. ({)

(z) Significant ({) Not significant

Findings (between USNz and USN{ groups only):

Ogourtsova et al.


Testing paradigm

B. Results from Studies – Pointing 1. Pointing straight-ahead Chokron & Bartolomeo35 with index MODERATE (N/A) finger while blindfolded B (16 trials, 4 with each starting position: 30uu and 15uu to the left and to the right of the objective center of the table); 2. Upon the appearance of the upper, lower or middle target among the three vertically arranged gray circles (as a traffic light), subjects were asked to move their right hand from a center position to the key situated in the right (for upper), left (for lower) or middle (for middle target) area (12 practice trials, and 10 blocks of 4 upper, 4 middle and 4 lower target trials). 1. Line bisection task: Harvey et al.27 bisecting 12 lines with HIGH (4.97) cues (letters) on the left, A right, bilateral ends, or no cues; and presented in the left, right, and central location with respect to the body’s midline; using the ipsilesional hand.

Type (A vs. B)


Study (year)

Table 4 Continued

Bisection errors (mm) (4.97; z17.9 – rightward calculated with t-statistic bisection error (7)56.58)

{1.70 – leftward bisection error

2. 149 milliseconds 3. 0.34

2. reaction time differences 2. 223 milliseconds between latencies to 3. 0.35 produce left or right directed response (milliseconds) (N/A, no SD available) 3. Correlation between subjective straight-ahead and reaction times (N/A)

USN{

1. N/A

USNz

1. Subjective straight-ahead 1. {1.2 (leftward bias) (uu) (N/A, no SD available), difference from objective midline


(z) rightward shift in USNz; with unilateral left cues decreasing the extent of rightward bisection error;

2. UTD (no between USNz and USN{ group analyses are performed) 3. UTD (no between USNz and USN{ group analyses are performed)

1. UTD (no between USNz and USN{ group analyses are performed)

Findings (between USNz and USN{ groups only): (z) Significant ({) Not significant

Ogourtsova et al.



2015

VOL .

22

NO .

6

13 409

410 14


2015

VOL .

22

NO .

6

Richard et al.29 HIGH (0.96) A

Heilman et al.28 MODERATE (N/A) A

Type (A vs. B)


Study (year)

Table 4 Continued

(2) Landmark task: pointing to the end of the line that appeared closed to the landmark in 22 lines: 12 were transected in the center and cued as in (1); 10 were asymmetrically transected and uncued; and presented in the left, right, and central locations with respect to the body’s midline using the ipsilesional hand. Pointing to an imaginary point in space perpendicular to the midline of the chest with the right hand (USNz and healthy controls) and the left hand (USN-patients with LHS). (1) Body-centered line bisection task of 24 black lines (2.5 cm, 5 cm, 10 cm, and 20 cm lines) using a pencil and the right hand.

Testing paradigm

1. {0.005+ 0.23

End-point accuracy: 1. 1.16+ 1.54 1. Body-centered line bisection constant error averaged for 2.5/5/10/20 cm lines (cm) (1.05)

23–85

USN{

1. 1.2 to the left

Only one in 8 individuals (premotor pattern); other responded to the left end of the lines (perceptual pattern);

USNz

End-point accuracy (cm): 1. 8.77 to the right 1. Directional deviation error (N/A, no SD or degree of freedom for t-statistic provided)

Number of rightward responses (N/A)


1. (z) – rightward shift in USNz

1. (z) – USNz showed more directional error to the right.

(z) – most USNz patients demonstrated a perceptual bias by pointing leftward.



Ogourtsova et al.


Himmelbach & Karnath36 HIGH ({0.03) B

Type (A vs. B)


Study (year)

Table 4 Continued

(2) Manual pointing with the right index finger: imagining a line starting from their navel and going straight-ahead through a pointing board, putting their index finger on this line, in the dark; Pointing task using the right hand: making an accurate pointing movement from a fixed starting position to one of the eight targets (green LEDs) located on the left and right sides under lights (closed loop) and in the darkness (open loop) with 24 trials per condition.

Testing paradigm

USNz

End-point accuracy: 1. Terminal accuracy of pointing (uu) averaged over two lighting conditions for (a) horizontal, (b) vertical, axes and left/right targets ((a) {0.44/{0.18; (b) 0.02/{0.42) 2. Hand path curvature index (mm) for (a) closed loop left/center/right; (b) open loop left/right (N/A) **(Authors emailed twice to obtain data – no response received). 3. Straightness index averaged over the two lighting conditions for left/right targets (0.65/0.18)

1. *(a) 0.01+ 2.47/{1.75+ 3.55 * (b) {0.90+ 2.97/{1.85+ 1.68 2. UTD 3. *1.14+ 0.05/1.1+ 0.05

2. Subjective straight-ahead 2. 9.4+ 3.2 (to the right) (uu) (0.87)


2. (z) – rightward shift in USNz

1. ({) 2. ({) 3. ({)

1. *(a) {0.94+ 1.58/{1.15+ 2.88 *(b) {0.95+ 1.44/{0.85+ 2.83 2. UTD 3. *1.10+ 0.07/1.09+ 0.06


2. 1.6+ 1.6

USN{


Ogourtsova et al.



2015

VOL .

22

NO .

6

15 411

16 412


Unrestrained threedimensional pointing movements with the right hand to three LEDs targets with a ‘‘comfortable’’ movement speed, under normal room lighting (closed loop) (n57 to each target) or in complete darkness (open loop) (n57 to each target) for a total of 42 arm movements.

Unrestrained threedimensional pointing movements with the right hand to three LEDs targets with a ‘‘comfortable’’ movement speed, under normal room lighting (closed loop) (n57 to each target) or in complete darkness (open loop) (n57 to each target) for a total of 42 arm movements.

Konczak & Karnath37 HIGH (1.82) B

Testing paradigm

Karnath et al.42 HIGH ({0.37) B

Type (A vs. B)


Study (year)

Table 4 Continued

End-point accuracy: 1. Terminal accuracy of pointing (uu) averaged over the two lighting conditions for (a) horizontal, (b) vertical, and (c) anterior–posterior axes and left, center and right targets (mm) (a. {0.016, b.{1.26, c. 0.16) 2. Straightness of the hand path **(Authors emailed to obtain– unable to retrieve results as per authors given that they were saved into external disks that can no longer be read by current technology). Kinematic parameters: 1. Peak tangential velocity averaged for left/center/right targets (mm/s) (1.51) 2. Time to peak hand velocity for left/center/right targets (mm/s) (0.04) 3. Total movement time averaged for light/dark conditions (milliseconds) (3.91) 4. Deceleration time (milliseconds) (N/A)

Outcome variables (effect size) USN{

2015

VOL .

22

NO .

6

2. UTD

1. 1107+ 142.27 2. *410+ 100/410+ 100/405+ 100 3. 1393+ 287.59 4. UTD

2. UTD

1. 1470+ 307.64 2. *520+ 300/420+ 200/415+ 100 3. 2916+ 468.40 4. UTD

1. (a) 2.03+ 12.82; 1. (a) 2.4+ 29.35; (b) 5.43+ 17.41; (c) {9.47+ 15.38 (b) {11.06+ 6.07; (c) {7.26+ 13.03

USNz

1. ({) 2. ({) 3. ({) 4. (z) – larger deceleration phase in the USNz group

2. ({)

1. ({)



Ogourtsova et al.


Rossit et al.32 HIGH (0.73) A (task 2), B (task 1)

Type (A vs. B)


Study (year)

Table 4 Continued

(1) Pointing condition: pointing to 3 targets/white circles (left, central and right) as quickly and accurately as possible (n536 trials, 12 per condition) using the right hand, under normal room lighting (closed loop) or in complete darkness (open loop); (2) Gap bisection condition: pointing midway between two presented white circles (appearing in the left, right or central positions) as quickly and accurately as possible (n536 trials, 12 per condition) using the right hand, under normal room lighting (closed –loop) or in complete darkness (open loop)

Testing paradigm

End-point accuracy for (a) Closed loop left/center/right; (b) open loop left/center/right: 1. Absolute angular error (uu) (a. N/A, b. {0.28) 2. Hand path curvature index (mm) (a. 3.09, b. 0.03). Kinematic parameters (a) Closed loop left/center/right; (b) open loop left/center right: 1. Total movement time (milliseconds) (a. 0.97, b. {0.78)

Kinematic parameters averaged for (a) closed loop left/center/right; (b) open loop left/center right 1. Total movement time (milliseconds) (a. 2.13, b. {0.29) 2. Reaction time (milliseconds) (a. 1.81, b. {0.81)


1. (a) 623.78+ 22.33; (b) 768.5+ 38.81 2. (a) 300.03+ 20.88; (b) 407.96+ 33.88

USN{


2015

1. (a) 688.63+ 37.09; (b) 765.2+ 51.29

1. (a) 657.4+ 26.17; (b) 801.67+ 40.93

1. (a) 0.4+ 0.0; (b) 3.1+ 0.64 2. (a) 14.33+ 2.03; (b) 8.5+ 4.1 2. (a) 7.93+ 2.11; (b) 1.76+ 2.67

1. (a) 0.4+ 0.0; (b) 2.9+ 0.76

1. (a) 680.37+ 30.11; (b) 755.9+ 46.22 2. (a) 409.53+ 82.64; (b) 384.17+ 23.85

USNz

1. ({)

2. ({)

1. ({)

1. ({) 2. ({)



Ogourtsova et al.


VOL .

22

NO .

6

17 413

18 414



Quality (mean effect size) Type (A vs. B)

Study (year)

Table 4 Continued


2. Reaction time (milliseconds) (a. 0.83, b. {1.67) End-point accuracy (a) closed loop left/center/right; (b) open loop left/center/right: 1. Absolute angular error (uu) (a. 1.7, b. 1.24) 2. Hand path curvature index (mm) (a. 2.43, b. 0.56) 1. Directional error 1. Propointing task: (% of errors) (N/A) pointing directly toward targets presented on their 2. Absolute angular error (uu) averaged left ({12;{6uu) or right (z6;z12uu) in a. propointing to left/right 2. Anti-pointing task: targets; b. pointing toward a mirror anti-pointing to left/right position of the appearing targets (a. 2.98, target (i.e. position in the b. 3.81) opposite hemispace) on 3. Reaction time the left ({12;{6uu) or right (milliseconds) a. (z6;z12uu) propointing to left/right targets; b. anti-pointing to left/right targets (a. 0.15, b. 2.18) 4. Movement time (milliseconds) a. propointing to left/right targets; b. anti-pointing to left/right targets (a. {1.18, b. 1.49)

Testing paradigm

2015

VOL .

22

NO .

6

1. 13.8 2. a. 0.6+ 0.08; b. 11.83+ 2.88; 3. a. 339.03+ 41.41; b. 511.23+ 77.29 4. a. 590.55+ 29.49; b. 751.78+ 31.68;

1. 0.6 2. a. 0.43+ 0.1; b. 3.88+ 0.62 3. a. 333.23+ 30.29; b. 382.15+ 32.43; 4. a 623.35+ 25.56; b. 686.05+ 53.76;

1. (z) – more errors in USNz group 2. (z) – increased absolute angular error in anti-pointing task only; 3. ({) * Within group comparison revealed that anti-pointing reaction times were correlated significantly with the severity of neglect; 4. ({)

2. (a) 4.7+ 2.22; (b) 4.57+ 3.08 2. ({)

2. (a) 10.1+ 2.22; (b) 7.13+ 5.74

2. ({)

1. (a) 0.63+ 0.1; (b) 2.77+ 0.47 1. ({)

2. (a) 325.6+ 36.17; (b) 424.43+ 30.11

2. (a) 360.23+ 46.40; (b) 375.93+ 27.90


1. (a) 0.8+ 0.1; (b) 3.33+ 0.43

USN{

USNz


Ogourtsova et al.


Testing paradigm


Kinematic parameters 1. Movement time (milliseconds) for predictable/unpredictable sequence (2.76/3.8) 2. Movement time (milliseconds) for absence/presence of a distractor* (N/A)


1. 432+ 30/619+ 5 2. 566/793 (leftward movement); 553/563 (rightward movement)

USNz

Kinematic parameters 1. *250+ 100/700+ 100 1. Reprogramming direction 2. *120+ 10/300+ 10 3. (5/49) and (7/64) (milliseconds) for rightward/leftward targets (1/3) 2. Reprogramming of extent (milliseconds) for rightward/leftward targets ({1.3/0) 3. Movement execution errors for reprogramming direction (right/left targets) and reprogramming extent (right/left targets) (N/A) (1) Immediate pointing Kinematic parameters for condition (n584 trials, 12 (a) immediate pointing to for each target) to 7 visual the left/center/right targets; white circles as targets (3 and (b) delayed pointing to in the left hemispace, 3 in the left/center/right targets: the right hemispace, and 1 at a central position); pointing to the target as quickly and as accurately as possible using the right hand;

Experiment (1): perform a Mattingley et al.30 HIGH (1.54) sequence of movement A (task 1 [predictable], task 2), with the ipsilesional right B (task 1 [unpredictable]) hand to LED targets (predictable or unpredictable, target-only or with a distractor) in the right and left hemispaces of the responding limb (32 trials) Experiment (2): interrupt a predictable, reciprocating sequence of leftward or rightward movements to move to an occasional, unpredictable target located either (A) in the same direction but of twice the extent or (B) opposite to that expected (2 blocks of 8 trials of 15 movements each).

Type (A vs. B)


Study (year)

Table 4 Continued

1. * 150+ 10/400+ 10 2. *250+ 10/300+ 10 3. (2/20) and (4/25)

1. 294+ 30/429+ 5 2. UTD

USN{

1. ({) 2. ({) 3. ({)

1. (z) – slower movement time in USNz for predictable sequences 2. (z) – slower leftward movement with a distractor than in the absence of it (not significant in USN{ group).



Ogourtsova et al.



2015

VOL .

22

NO .

6

19 415

416 20


2015

VOL .

22

NO .

(2) Delayed pointing condition (n584 trials, 12 for each target) to same targets: refraining from pointing for 5000 milliseconds and point to the remembered location as quickly and accurately as possible only following an auditory signal.

Testing paradigm

C. Results from Studies – Reaching (1) Reach toward a central Rossit et al.38 HIGH ({0.33) target (white circle) that B could jump unexpectedly, at movement onset, to the right or left hemispace;

Type (A vs. B)


Study (year)

Table 4 Continued

6

Kinematic parameters (a) location go left jump/no jump/right jump; (b) location stop left/jump/no jump/right jump:

2. time to peak hand velocity (milliseconds) (a. 0.42, b.{0.41) 3. total movement time (milliseconds) (a. 0.60, b. 1.29) 4. reaction time (milliseconds) (a. {0.14, b. N/A) End-point accuracy: 1. Absolute angular error (uu) in (a) immediate pointing to the left/center/right targets; and (b) delayed pointing to the left/center/right targets (a. 1.10, b. 0.80). 2. directional angular error (uu)

1. Peak velocity (mm/s) (a. {0.06 b. {0.01)


4. (a352+ 84.54; (b) N/A

1. (a) 0.4+ 0.08; (b) 1.06+ 0.41 1. (z) – USNz less accurate for leftward targets in delayed condition only.

2. UTD

4. (a) 366.33+ 105.48; (b) N/A

1. (a) 0.5+ 0.1; (b) 1.73+ 1.10

2. UTD

2. ({)

4. ({)

3. ({)

3. (a) 633.7+ 71.23; (b) 832.8+ 103.64

3. (a) 680.56+ 82.79; (b) 846.27+ 80.28

2. ({)

1. ({)

2. (a) 217.13+ 48.28; (b) 321.63+ 62.36

1. (a) 1230+ 141.63; (b) 1054.43+ 147.44

USN{

2. (a) 236.9+ 44.73; (b) 295.03+ 61.70

1. (a) 1219+ 185.03; (b) 1052.53+ 177.44

USNz


Ogourtsova et al.


Type (A vs. B)


Study (year)

Table 4 Continued


4. Movement time (milliseconds) (a. 1.87, b. N/A). 5. Peak velocity (mm/s) (a. {1.36, b. N/A) 6. Number of peaks (a. {3.39, b. N/A) 7. Percentage of successful stops (%) left/right jump ({3.61) 8. Stop time (milliseconds) left/right jump (2.39) End-point accuracy: 1. directional end-point error (uu)for location go left jump/no jump/right jump (0)

(2) Either follow the target 1. Reaction time (i.e. location go) or stop (milliseconds) their movement (i.e. (a. {0.93, b. {1.95) location stop) with the right index finger. 2. terminal correction status (%) (a. {1.28, b. 1.47) 3. Correction time (milliseconds) left/right jump (1.57/1.17)

Testing paradigm


3. *350+ 50/290+ 30

4. (a) 598.4+ 21.02; (b) N/A 5. (a) 1366.4+ 82.86; (b) N/A 6. (a) 1.7+ 0.1; (b) NA 7. 79.9+ 5.65 8. 459.6+ 23.54

3. *410+ 20/320+ 20

4. (a) 655.46+ 37.63; (b) N/A 5. (a) 1262.4+ 68.54; (b) N/A

7. 47.65+ 11.30 8. 594.6+ 76.26

1. {0.06+ 0.4

1. {0.06+ 0.1

2. (a) 97.95+ 1.40; (b) 63.25+ 12.37

2. (a) 88.5+ 10.29; (b) 80.45+ 10.83

6. (a) 1.36+ 0.1; (b) NA

1. (a) 1318.06+ 27.54; (b) 1405.93+ 37.18

USN{

1. (a) 1293.13+ 25.83; (b) 1333.5+ 36.18

USNz

1. ({)

8. ({)

7. (z) – USNz less accurate.

6. ({)

5. ({)

3. (z) – USNz slower when adjusting their reaches to a left target jump. 4. ({)

1. ({) 2. ({)



Ogourtsova et al.


2015

VOL .

22

NO .

6

21 417

418 22


2015

VOL .

22

NO .

6

Randomly assigned sequences of 4 experimental conditions: (1) Reaching to take a drink of most-preferred beverage; (2) Reaching to take a drink of least-preferred beverage; (3) Reaching for and brining to the mouth, but not drinking the mostpreferred beverage; (4) Reaching for and brining to the mouth, but not drinking the leastpreferred beverage.

Testing paradigm

USNz

2. Movement time (sec) ({0.95) 3. Total displacement (N/A) 4. Amplitude of peak velocity (N/A) 5. Percentage of movement where peak velocity occurs (%) (N/A) 6. Number of movement units (N/A)

2. *1.36+ 0.2 3. Not provided 4. Not provided 5. Not provided

6. Not provided

3. Not provided 4. Not provided 5. Not provided

6. Not provided

1. *0.73+ 0.2

USN{

2. * 1.55+ 0.2

Kinematic parameters for conditions 1/2/3/4 1. Reaction time (sec) (0.45) 1. *0.64+ 0.2


D. Results from Studies – Grasping (1) Grasping one of five Kinematic parameters for Farne et al.31 HIGH (0.01) possible objects the 5 target positions (uu): B (translucent plastic {20/-10/0/z1{/z20 cylinders), equally sized and distributed over a 40uu wide workspace, using their right thumb and index finger, as accurately and rapidly as possible (i.e. fixed condition) (50 trials, 10/object)

Wu et al.25 HIGH ({0.25) B

Type (A vs. B)


Study (year)

Table 4 Continued

6. ({)

5. ({)

3. ({) 4. ({)

2. ({)

1. (z) – individuals in the USNz group showed least reaction times for condition (1); and greatest reaction time in condition (2) as opposed by USN{ ad LHS groups who demonstrated opposite results: greatest reaction time for condition (1) and least reaction time for condition (2).


Ogourtsova et al.


Type (A vs. B)


Study (year)

Table 4 Continued

(2) Correcting the movement ‘‘in-flight’’ in response to a sudden change of object position (perturbed condition) (180 trials).

Testing paradigm

1. Reaction time (milliseconds) (0.61) 2. Movement time (milliseconds) (1.14) 3. Time to peak acceleration (milliseconds) (1.03) 4. Peak acceleration* (milliseconds/s2) ({2.18) 5. Time to peak velocity (milliseconds) (0.88) 6. Peak velocity (mm/s) ({1.46) 7. Time to peak velocity (2) (milliseconds) (1.10)

1. Reaction time (milliseconds) (1.34) 2. Movement time (milliseconds) (1.32) 3. Time to peak acceleration (milliseconds) ({0.66) 4. Peak acceleration* (milliseconds /s2) ({0.58) 5. Time to peak velocity (milliseconds) (0.03) 6. Peak velocity (mm/s) ({1.13) 7. Time to maximum grip aperture (milliseconds) (0.82) 8. Maximum grip aperture (mm) ({0.82) Kinematic parameters for the 5 target positions (uu): {20/{10/0/z1{/z20



2015

VOL .

7. 1059.4+ 478.9

7. 681.8+ 69.16

6. 650.6+ 96.23

5. 294+ 82.88

5. 358.8+ 62.55 6. 478.4+ 135.88

4. 4749.8+ 727.60

8. 52.24+ 13.76

8. 43.14+ 7.49

4. 2938+ 922.55

7. 601.6+ 122.161

7. 697.2+ 110.55

3. 186.4+ 57.16

6. 707.2+ 91.11

6. 580+ 130.18

3. 194.4+ 51.98

5. 344.4+ 43.22

5. 346.2+ 68.65

2. 1218+ 117.49

4. 4771+ 665.81

4. 4156+ 1337.98

2. 1882+ 818.01

3. 215.2+ 40.00

3. 183.8+ 52.95

1. 577+ 79

2. 895.8+ 208.30

2. 1154+ 180.19

1. 1144.6+ 619.92

1. 480.2+ 82.69

USN{

1. 771.8+ 294.45

USNz

7. ({)

6. ({)

4. (z) – lower in USNz group 5. ({)

3. ({)

2. ({)

1. ({)

8. ({)

7. ({)

6. ({)

5. ({)

4. ({)

3. ({)

2. ({)

1. ({)



Ogourtsova et al.


22

NO .

6

23 419

420 24


2015

VOL .

22

NO .

6

Marotta et al.26 MODERATE (2.2) A

Harvey et al.39,53 HIGH ({0.19) B

Type (A vs. B)


Study (year)

Table 4 Continued


8. Peak velocity (2) (mm/s) ({1.92) 9. Time to maximum grip aperture (milliseconds) (2.29) 10. Maximum grip aperture (MGA)(mm) ({1.36) 11. Time to MGA (2) (milliseconds) (1.34) 12. MGA (2)(mm) ({1.60) Grasping task to four red Kinematic parameters wooden dowels (near and 1. peak grip aperture (PGA) far right-sided; and near (mm) (0) and far left-sided) with the 2. Percentage of time taken right hand, in both, open- to reach and closed-loop PGA (%) (0.06) conditions (48 trials, 3. Movement duration 24/condition, 12/target (milliseconds) type). ({0.71) 4. Peak velocity (mm/s) (0.02) 5. Percentage of time spend decelerating (N/A) End-point accuracy: 1. Hand path curvature (N/A) 2. Hand path curvature index ({0.33) (1) Discrimination task: Perceptual errors (% of visually determine if the correct two white shapes were responses) (N/A –no SD same or different provided) Grasp performance: 1. Number of grasp lines (N/A, no SD provided).

Testing paradigm

9. 477.4+ 37.04 10.43.86+ 6.69 11. 891.8+ 57.87 12. 50.52+ 4.91 1. 93+ 10.6 2. 75+ 12.4 3. 1205+ 226 4. 478+ 89 5. UTD (USNz and USN – grouped for results comparing to controls)

9. 714+ 141.36 10.34.34+ 7.32 11. 1433.6+ 564.72 12. 42.06+ 5.58

92

1. 58.6

1. 27.8

2. 0.08+ 0.03

2. 0.07+ 0.03

69.8

1. UTD

1. UTD

1. 93+ 10.8 2. 76+ 20.3 3. 1057+ 186 4. 480+ 89 5. UTD (USNz and USN – grouped for results comparing to controls)

8. 543.2+ 57.89

USN{

8. 373+ 110.64

USNz

1. (z) – USNz showed fewer grasp lines;

(z) – less accurate in USNzgroup;

2. ({)

1. ({)

12. ({) 1. ({) 2. ({) 3. ({) 4. ({) 5. N/A

11. ({)

10. ({)

9. (z) –longer in USNz group

8. ({)



Ogourtsova et al.


McIntosh et al.40 HIGH (1.27) B

Type (A vs. B)


Study (year)

Table 4 Continued

Grasping a translucent cylinder (40 trials, 4 types of target cylinders with different diameters and appearing in different locations) with the right hand.

(2) Grasping task: picking up the target shape with the thumb and index finger of their right hand as accurately and quickly as possible (96 trials).

Testing paradigm

2. *550+ 50

USNz

1. Maximum grip aperture (mm): for (a) left-side objects, (b) right-side objects of 20/30/40/50 mm diameters (a. 3.80, b. 0.32) 2. Manual estimation performance (mm) for (a) left-side objects, (b) right-side objects of 20/30/40/50 mm diameters (a. 0.67, b. 0.72)

2* (a) 41.25+ 3; (b) 41.5+ 3

2* (a) 44+ 5; (b) 44.5+ 5


2. ({)

1. ({)

4. (z) – USNz produced greater distance when the grasp were to the right of the center;

4. *4+ 5/3.7+ 2

1* (a) 53.25+ 2; (b) 68.25+ 2

3. (z) – USNz produced more grasp lines to the right of the center;

2. (z) – USNz produced grasp lines over twice the distance from the center of the mass;


3. *18+ 3/17+ 3

2. *250+ 30

USN{

1.* (a) 67.75+ 5; (b) 69.5+ 5

3. Number of grasp lines in 3. *35+ 5/5+ 5 right/left of the center of the object (3.75/{3.80) 4. Magnitude of grasp lines 4. *7.3+ 5/3.6+ 2 in right/left of the center of the object (distance (mm)) (3.3/{0.1) Kinematic parameters

2. Grasp stability: distance between grasp lines and center of mass (mm) (7.87)



Ogourtsova et al.


2015

VOL .

22

NO .

6

25 421

26 422

Testing paradigm



2015

VOL .

22

NO .

6

N/A: not available; USNz: presence of USN; USN{: absence of USN.

3. Movement time (milliseconds) for left/right objects (4.46/3.39) 4. Peak velocity (mm/s) for left/right objects ({1/{3.8) 5. Time to peak velocity for left/right objects (milliseconds) ({0.4/{1.25) 6. Time after peak velocity for left/right objects (milliseconds) (6.25/2.42) 7. Percentage time to maximum grip aperture (%) for 20/3/40/50 mm object’s diameters (0.95) E. Results from Study – Moving an Object in a Horizontal Plane Manually move a wooden Kinematic parameters Heilman et al.41 handle as quickly as MODERATE (1.33) Reaction time B possible using the (milliseconds): ipsilesional (stroke 1. Mean reaction times subjects) or dominant (1.81) (controls) hand along a 2. Left to right (1.52) fixed linear pathway in the 3. Right to left (1.75) horizontal plane (60 trials Movement time divided in two blocks of (milliseconds): 30 trials each), where 1. Mean movement times block (1): apparatus (1.02) located in the right body 2. Left hemispace (1.05) hemispace; and block (2): 3. Right hemispace (0.80) apparatus located in the left body hemispace.

Type (A vs. B)


Study (year)

Table 4 Continued

5* 460+ 50/350+ 50

5* 480+ 50/400+ 50

1. 578.6+ 135.7 2. 586.0+ 139.4 3. 611.1+ 178.5

2. 950.0+ 466.6 3. 916.0+ 506.4

3. 399.7+ 88.4

1. 933.3+ 470.3

3. 870.0+ 367.8

2. 723.8+ 312.4

1. 386.9+ 82.3

1. 798.2+ 309.4

2. 374.2+ 88.3

7* 78.75+ 5

7* 83.5+ 5

6* 600+ 50/640+ 50

4* 610+ 50/800+ 50

4* 560+ 50/610+ 50

6* 850+ 50/750+ 50

3* 1100+ 40/990+ 30

USN{

3* 1290+ 45/1130+ 50

USNz

2. ({) 3. ({)

1. (z) – longer in USNz


2. ({)


7. ({)

6. (z) – USNz showed longer time

5. (z) – USNz showed longer time

4. ({)

3. ({)



Ogourtsova et al.


Ogourtsova et al.

Off-line movements The following, UE movements were categorized as off-line: subjective straight-ahead (SSA) pointing, line/gap bisection, pointing to a mirror image of the target (i.e. anti-pointing), delayed pointing to a remembered target location, grasping different shapes with thumb and index finger only. This type of UE movement was analyzed in only 6 out of 20 selected studies.15,26–32 Overall, across the six studies that investigated off-line UE movement, 26 outcomes were studied, and 11 of these (i.e. 42.31%) were found to be significantly different between USNz and USN{ groups: Bisection and directional deviation errors and subjective straight-ahead (SSA) for straight-ahead pointing task (rightward shift in USNz group)27–29; Slower movement times for predictable (vs unpredictable) sequencing pointing30; Increase in absolute angular errors and increase in direction angular errors in anti-pointing tasks31; Fewer grasp lines, lower grasping stability, and magnitude of grasping lines in a ‘‘perceptual grasping’’ task26; Decrease in absolute angular error for left-sided targets in a delayed/memory-guided pointing task17; Increase in absolute angular error in anti-pointing task (i.e. pointing to a mirror image of a target).15 The following outcomes of interest (61.53%) were not found to be significantly different in USNz when compared with USN{ group: Reprogramming direction and extent and movement execution errors for reprogramming direction in a pointing task where the sequence of pointing was interrupted and subjects were asked to reprogram their movement in the same direction or opposite direction of the presented new target30; Kinematic parameters (movement/reaction time, endpoint accuracy, hand path curvature) of a gap bisection task32; Kinematic parameters (peak velocity, time to peak hand velocity, total movement time, reaction time, directional angular error) in a delayed pointing task to a remembered target location17; Direction error, reaction and movement time in antipointing task (i.e. pointing to a mirror location of the target).15

N N N N N N N N N N

Online movements The following UE movements were categorized as immediate or online: immediate button pressing, pointing, reaching or grasping actual targets and moving objects horizontally. This type of UE movement was studied in 16 out of the 20 selected studies.15,17,25,30–41 Overall, across the 16 studies that investigated immediate type of UE movement, 87 outcomes were studied, and only 15 of these (i.e. 17.2%) were found to be significantly different between USNz and USN{ groups:

N N N N N N N N


Slower reaction time and percentage of correct response to left-sided targets in a pressing task33; Larger deceleration phase in pointing37; More directional errors in pointing15; Slower correction/adjustment time and lower accuracy in a reaching task38; Slower reaction time in reaching to least-preferred midline beverage, and faster reaction time for most-preferred midline beverage25; Slower reaction (mean, and right to left) and movement times in moving an object horizontally task41; Longer times to and after peak velocity in a grasping task40; Lower peak acceleration, and longer time to maximum grip aperture in a correcting movement to grasp an object that changed position.31

The following outcomes of interest (82.8%) were not found to be significantly different in USNz as compared to USN{ group: Reaction time to right and central targets, and percentage of accuracy in response to left targets, and movement time in a pressing task33,34; Subjective straight-ahead, reaction time, and correlation between SSA and reaction time in a pointing task35; End-point accuracy measures in a pointing task36,42; Peak tangential velocity, time to peak hand velocity, and movement time in a pointing task37; Movement time, reaction time, and end-point accuracy measures in a pointing task15,32; Reprogramming of direction and extent, and movement execution errors in a pointing task30; Peak velocity, time to peak hand velocity, movement and reaction time, and directional angular error in an immediate pointing task17; Reaction time, terminal correction status, movement time, peak velocity, number of peaks, stop time, and directional end-point error in a reaching and following/stopping the target task38; Movement time, total displacement, amplitude of peak velocity, percentage of movement where peak velocity occurs, number of movement units in a reaching task for preferable versus non-preferable objects25; Kinematic parameters (reaction and movement time, time to peak acceleration, peak acceleration, time to peak velocity, peak velocity, time to maximum grip aperture, and maximal grip aperture) in a grasping task; and kinematic parameters (reaction and movement time, time to peak acceleration, time to peak velocity, peak velocity, time to maximum grip aperture, and maximal grip aperture) in correcting the grasping movement in response to a sudden change of object position31; Kinematic (peak grip aperture, percentage of time taken to reach peak grip aperture, movement time, peak velocity, and percentage of time spend decelerating); and end-point accuracy measures (hand path curvature, and hand path curvature index) in a grasping task39;

N N N N N N N N N N

N


2015

VOL .

22

NO .

6

27 423

Ogourtsova et al.

N N


Maximum grip aperture, manual estimation performance, movement time, peak velocity, and percentage time to maximum grip aperture in a grasping task40; Reaction time (left to right); and movement time in left and right hemispace in moving the object in an horizontal plane task.41

Discussion The present review identified studies of moderate to high quality and found USN-specific impairments for particular movement types. Overall, impairments specific to individuals with USN as compared to those without USN emerged predominantly in behaviors that required a process of perceptual, memory-guided or delayed actions, and less or not at all in behaviors that required a direct or immediate response to visual targets.

Dorsal and ventral visual streams Dorsal stream – processing of immediate or online actions Research suggests that there are different types of action control43 processed via distinct visual streams, ventral and dorsal, and that the presence of USN can affect those actions in different ways. In healthy individuals, parts of the dorsal stream were shown to be involved in visual search tasks performed in the near space (i.e. within one’s reaching distance), while parts of ventral stream were found to be implicated in far visual search tasks (i.e. beyond the reaching distance).44 In other words, it is speculated that individuals can immediately act upon targets that are presented within the near space, but need more perceptual abilities to act upon the objects that are located in the far space. Thus, the results of the present review are complimentary to the findings of Lane et al.,44 suggesting that the dorsal visual stream is involved in the role of processing immediate action response to visual targets. Likewise, in individuals with a right-side stroke, a recent voxel-based lesion-symptom mapping studies showed that the actual observed deficits in immediate action response to visual targets are associated with brain lesions in specific areas that include: basal ganglia, frontal regions, and parieto-occipital regions (i.e. parts of the dorsal stream).18 Those regions, however, are often spared in individuals with post-stoke USN, where the parieto-temporal junction,45 angular gyrus, right inferior parietal lobe, parahippocampal region,9 and the right superior temporal cortex10 are found to be predominantly affected. In line with this concept, the present review did find that 28 424


2015

VOL .

22

NO .

6

the majority of outcome measures in immediate actions response to visual targets are not different between USNz and USN{ groups with the exception of the observed directional slowing (i.e. response time25,33,41). These observations suggest that the deficits observed in immediate action response to visual targets are not a consequence of damaged USNspecific brain areas, but could arise from other lesions of the visuomotor network, similarly affecting USNz and USN{ individuals. Ventral stream – Processing of memory-guided, delayed or off-line actions The review identified that off-line tasks were more affected by USN (i.e. 42.31% of studied outcomes) than the immediate, online type of tasks (i.e. 17.23% of studied outcomes). Previous research suggests that off-line tasks are associated with ventral stream lesions (occipito-temporal and parahipoccampal cortex),15,18 which are also considered as core regions responsible for USN presentation. Indeed, the results of this systematic review are in concordance with the suggestion of Milner and Goodale46 that USN is predominantly a perceptual disorder, and is associated with the damage to the high-level representation ventral stream of visual processing. These findings have important clinical implications in the understanding of USN and furthering the research on more sensitive evaluation methods and effective treatment techniques. For instance, we propose that evaluation tools that require a memoryguided or delayed type of action are more likely to elicit the subtle signs of USN rather than tools that involve simple immediate action. Similarly, treatment activities that include non-affected UE movement can be aimed at employing tasks of perceptual/ memory-guided or delayed type of action rather than immediate action, to enhance ventral stream stimulation and ensuing recovery. For instance, if considering the results of Rossit et al.17 on immediate versus delayed reaching abilities, the treating clinician could introduce a delay between the presentation of the object to be reached (e.g. tooth paste placed in the left-sided visual hemispace) and the actual reaching response when performing the practice of activities of daily living performance with the patient (e.g. grooming). Similarly, according to results of Rossit et al.,15 pointing to a mirror location of the object or target instead of the actual target location can be attempted in treatment when pointing/visual scanning is used. In addition, as per Marotta et al.,26 therapists could practice grasping the object (e.g. toothpaste)

Ogourtsova et al.

as close to the midline as possible, to elicit the analysis of object contour/its structural representation to guide the movement. Moreover, dissociations also exist with respect to what exactly the individual is neglecting. Egocentric USN refers to a deficit in directing attention to the space on the left side of one’s body. On the other hand, allocentric USN refers to neglecting one side of each object, irrespective of whether they are present in the right or left visual hemispaces. It is suggested that these two types of USN can occur independently or co-occur in the same individual (reviewed in Bickerton et al.47). Nonetheless, none of the studies included in this review that involved object manipulation (e.g. grasping) contained a sensitive assessment of allocentric versus egocentric type of USN. This could possibly lead to the lack of significant between-group differences that we observed (for instance, if the majority of selected individuals for the study had egocentric and not allocentric USN). We propose that stroke survivors with allocentric USN would potentially have more accentuated difficulty manipulating (e.g. grasping or reaching for) objects given their distorted perception of the object’s structural representation. Therefore, we suggest that studies in this field of post-stroke rehabilitation and also clinicians managing poststroke USN could use a sensitive assessment of allocentric versus egocentric USN (e.g. the Apples Test47). Lastly, it is important to consider USN’s spacerelated distinctions. More specifically, a recent study found that certain post-stroke individuals can have USN in both the near and the far hemispaces.12 All of the studies included in the present review used USN screening/assessment tests that predominantly assess USN in the near-extrapersonal space. Thus, individuals with co-occurring far-extrapersonal space USN might have been included in the testing, justifying the evidence of motor effects of USN for some participants (e.g. Refs. 12,27,37). We suggest that future studies could aim at differentiating near versus. far space USN, and at determining the ability of reaching for, pointing to, grasping or moving objects/targets located in the near and far-extrapersonal space.

Limitations To statistically detect a difference, the magnitude of the effect to detect and the sample size of a study matter.48,49 The sample size in the identified studies ranged from 4 to 18 individuals per group only, possibly being insufficient. In fact, none of the studies in the present review estimated the required sample size.


Given the difference in movement, kinematic measures that is considered significant is of rather small magnitude, a large sample size is required. Owing to relatively small sample sizes in the included studies, their results are to be interpreted with caution and sample size calculations are needed in future research to ensure that there are adequate numbers of subjects to detect real differences and provide a less-biased conclusion. In addition, confounding factors (e.g. stage of stroke recovery, USN type and severity, misclassification of USNz versus USN{ individuals, etc.) that could have influenced the results were not controlled for and necessitate more detailed and accurate analysis in future studies. For instance, several studies included individuals with acute and chronic stroke in the same group35,37,42 or subacute and chronic stroke in the same group.31 Moreover, this review is limited by employing only one investigator to perform the search, selection, and quality rating of the selected studies. Lastly, meta-analyses could not be performed given high heterogeneity of examined movements in the studies.

Conclusion The evidence reviewed in this manuscript supports the view of USN’s high heterogeneity and complexity. The current review suggests that USN can have more effect on certain goal-directed UE movements (e.g. memory-guided/delayed or off-line actions) and less on others (e.g. immediate response or online actions). It has identified potential grounds for these effects including differences in the neural basis of USN and goal-directed actions (i.e. ventral vs dorsal visual stream hypothesis).

Disclaimer Statements Contributors TO performed the literature search, studies selection, data extraction, quality analysis, and composed the manuscript. PA and AL were involved in reviewing and revising the manuscript.

Funding Tatiana Ogourtsova was supported by the Edith and Richard Strauss Fellowship in Rehabilitation Sciences 2014, PB Baily Fellowship and the Graduate Excellence award 2014 (McGill University, School of Physical and Occupational Therapy).

Conflicts of interest The authors declare no conflict of interest.

Ethics approval No ethics approval were required to conduct this systematic review. Topics in Stroke Rehabilitation

2015

VOL .

22

NO .

6

29 425

Ogourtsova et al.


Appendix 1: Description of movement types

Definition

Hypothesized visuomotor stream that is used to process each type of action Examples of actions

Memory-guided/delayed or off-line

Immediate or online

Action that necessitates relational metrics, scenebased coordinates, and/or working memory.Actions that are not directed at the target itself but instead pantomimed to a spatially displaced location besides it, or actions toward a target previously seen that is no longer present. Visual information regarding target position cannot be used directly during action execution. Ventral

Immediate guidance of actions directed toward targets, uses spatial information coded in egocentric coordinates.

Dorsal

Bisecting lines, pointing to a mirror location of a target, delayed pointing to a remembered target location, grasping different shapes.

Grasping of an actual target, pressing a button, pointing to an actual target.

Adapted from Rossit et al.15

Appendix 2: Definitions of MeSH terms

References

N

1 Jutai JW, Bhogal SK, Foley NC, Bayley M, Teasell RW, Speechley MR. Treatment of visual perceptual disorders post stroke. Top Stroke Rehabil. 2003;10(2):77–106. 2 Pierce SR, Buxbaum LJ. Treatments of unilateral neglect: a review. Arch Phys Med Rehabil. 2002;83(2):256–268. 3 Paolucci S, Antonucci G, Grasso MG, Pizzamiglio L. The role of unilateral spatial neglect in rehabilitation of right braindamaged ischemic stroke patients: a matched comparison. Arch Phys Med Rehabil. 2001;82(6):743–749. 4 Gillen R, Tennen H, McKee T. Unilateral spatial neglect: relation to rehabilitation outcomes in patients with right hemisphere stroke. Arch Phys Med Rehabil. 2005;86(4):763–767. 5 Buxbaum LJ, Ferraro MK, Veramonti T, Farne A, Whyte J, Ladavas E, et al. Hemispatial neglect: subtypes, neuroanatomy, and disability. Neurology. 2004;62(5):749–756. 6 Pollock A, Hazelton C, Henderson CA, Angilley J, Dhillon B, Langhorne P, et al. Interventions for visual field defects in patients with stroke. Cochrane Database Syst Rev. 2011;10: CD008388. 7 Bowen A, Lincoln NB. Cognitive rehabilitation for spatial neglect following stroke. Cochrane Database Syst Rev. 2007;2: CD003586. 8 Luaute´ J, Halligan P, Rode G, Rossetti Y, Boisson D. Visuospatial neglect: a systematic review of current interventions and their effectiveness. Neurosci Biobehav Rev. 2006;30(7): 961–982. 9 Mort DJ, Malhotra P, Mannan SK, Rorden C, Pambakian A, Kennard C, et al. The anatomy of visual neglect. Brain. 2003; 126(Pt 9):1986–1997. 10 Karnath HO, Fruhmann Berger M, Ku¨ker W, Rorden C. The anatomy of spatial neglect based on voxelwise statistical analysis: a study of 140 patients. Cereb Cortex. 2004;14(10): 1164–1172. 11 Halligan PW, Marshall JC. Left neglect for near but not far space in man. Nature. 1991;350(6318):498–500. 12 Aimola L, Schindler I, Simone AM, Venneri A. Near and far space neglect: task sensitivity and anatomical substrates. Neuropsychologia. 2012;50(6):1115–1123. 13 Coulthard E, Parton A, Husain M. Action control in visual neglect. Neuropsychologia. 2006;44(13):2717–2733. 14 Himmelbach M, Karnath HO, Perenin MT. Action control is not affected by spatial neglect: a comment on Coulthard et al. Neuropsychologia. 2007;45(8):1982–1984], [discussion 1982–1984]. 15 Rossit S, Malhotra P, Muir K, Reeves I, Duncan G, Harvey M. The role of right temporal lobe structures in off-line action:

N

N N

N N

426 30

Stroke: a group of pathological conditions characterized by sudden, non-convulsive loss of neurological function due to brain ischemia or intracranial hemorrhages. Stroke is classified by the type of tissue necrosis, such as the anatomic location, vasculature involved, etiology, age of the affected individual, and hemorrhagic versus non-hemorrhagic nature (PubMed MEDLINE: mesh database, 2008). Perceptual disorders: cognitive disorders characterized by an impaired ability to perceive the nature of objects or concepts through use of the sense organs. These include spatial neglect syndromes, where an individual does not attend to visual, auditory, or sensory stimuli presented from one side of the body (PubMed MEDLINE: mesh database, 1969). Upper extremity (UE): the region of the upper limb in animals, extending from the deltoid region to the hand, and including the arm, axilla, and shoulder (PubMed MEDLINE: mesh database, 2003. Movement: the act, process, or result of passing from one place or position to another. It differs from locomotion in that locomotion is restricted to the passing of the whole body from one place to another, while movement encompasses not only locomotion but also a change in the position of the whole body or any of its parts. Movement may be used with reference to humans, vertebrate and invertebrate animals, and microorganisms. Differentiate also from motor activity, movement associated with behavior (PubMed MEDLINE: mesh database, 2000–2003). Psychomotor performance: the coordination of a sensory or ideational (cognitive) process and a motor activity (PubMed medline: mesh database, 1983). Reaction time: the time from the onset of a stimulus until a response is observed (PubMed MEDLINE: mesh database, 1970–1976).


2015

VOL .

22

NO .

6

Ogourtsova et al.

16

17 18 19

20 21 22

23 24 25 26 27 28 29 30

31

32 33 34

35 36 37 38

evidence from lesion-behavior mapping in stroke patients. Cerebral Cortex. 2011;21(12):2751–2761. Rossit S, Fraser JA, Teasell R, Malhotra PA, Goodale MA. Impaired delayed but preserved immediate grasping in a neglect patient with parieto-occipital lesions. Neuropsychologia. 2011; 49(9):2498–2504. Rossit S, Muir K, Reeves I, Duncan G, Birschel P, Harvey M. Immediate and delayed reaching in hemispatial neglect. Neuropsychologia. 2009;47(6):1563–1572. Harvey M, Rossit S. Visuospatial neglect in action. Neuropsychologia. 2012;50(6):1018–1028. Downs SH, Black N. The feasibility of creating a checklist for the assessment of the methodological quality both of randomised and non-randomised studies of health care interventions. J Epidemiol Community Health. 1998;52(6):377–384. Crombie IK. The Pocket Guide to Critical Appraisal: A Handbook for Health Care Professionals. xi. London: BMJ Pub Group; 1996. Macfarlane TV, Glenny AM, Worthington HV. Systematic review of population-based epidemiological studies of orofacial pain. J Dent. 2001;29(7):451–467. Sanderson S, Tatt ID, Higgins JP. Tools for assessing quality and susceptibility to bias in observational studies in epidemiology: a systematic review and annotated bibliography. Int J Epidemiol. 2007;36(3):666–676. Sign. Notes on the Use of Methodology Checklist 1: Systematic Reviews and Meta-Analyses. 2013.http://www.sign.ac.uk/ guidelines/fulltext/50/notes1.html Borenstein M. Introduction to Meta-Analysis. Chichester, U.K: John Wiley & Sons; 2009; p. p.xxviii, 421. Wu CY, Wong MK, Lin KC, Chen HC. Effects of task goal and personal preference on seated reaching kinematics after stroke. Stroke. 2001;32(1):70–76. Marotta JJ, McKeeff TJ, Behrmann M. Hemispatial neglect: its effects on visual perception and visually guided grasping. Neuropsychologia. 2003;41(9):1262–1271. Harvey M, Milner AD, Roberts RC. An investigation of hemispatial neglect using the landmark task. Brain Cogn. 1995;27(1): 59–78. Heilman KM, Bowers D, Watson RT. Performance on hemispatial pointing task by patients with neglect syndrome. Neurology. 1983;33(5):661–664. Richard C, Honore´ J, Bernati T, Rousseaux M. Straight-ahead pointing correlates with long-line bisection in neglect patients. Cortex. 2004;40(1):75–83. Mattingley JB, Corben LA, Bradshaw JL, Bradshaw JA, Phillips JG, Horne MK. The effects of competition and motor reprogramming on visuomotor selection in unilateral neglect. Exp Brain Res. 1998;120(2):243–256. Farne` A, Roy AC, Paulignan Y, Rode G, Rossetti Y, Boisson D, et al. Visuo-motor control of the ipsilateral hand: evidence from right brain-damaged patients. Neuropsychologia. 2003; 41(6):739–757. Rossit S, Malhotra P, Muir K, Reeves I, Duncan G, Livingstone K, et al. No neglect-specific deficits in reaching tasks. Cereb Cortex. 2009;19(11):2616–2624. Bartolomeo P, D’Erme P, Perri R, Gainotti G. Perception and action in hemispatial neglect. Neuropsychologia. 1998;36(3): 227–237. Mattingley JB, Bradshaw JL, Phillips JG. Impairments of movement initiation and execution in unilateral neglect. Directional hypokinesia and bradykinesia. Brain. 1992;115(Pt 6): 1849–1874. Chokron S, Bartolomeo P. Position of the egocentric reference and directional arm movements in right-brain-damaged patients. Brain Cogn. 1998;37(3):405–418. Himmelbach M, Karnath HO. Goal-directed hand movements are not affected by the biased space representation in spatial neglect. J Cogn Neurosci. 2003;15(7):972–980. Konczak J, Karnath HO. Kinematics of goal-directed arm movements in neglect: control of hand velocity. Brain Cogn. 1998;37(3):387–403. Rossit S, McIntosh RD, Malhotra P, Butler SH, Muir K, Harvey M. Attention in action: evidence from on-line corrections in left visual neglect. Neuropsychologia. 2012;50(6): 1124–1135.


39 Harvey M, Jackson SR, Newport R, Kra¨mer T, Morris DL, Dow L. Is grasping impaired in hemispatial neglect? Behav Neurol. 2001;13(1–2):17–28. 40 McIntosh RD, Pritchard CL, Dijkerman HC, Milner AD, Roberts RC. Prehension and perception of size in left visual neglect. Behav Neurol. 2001;13(1–2):3–15. 41 Heilman KM, Bowers D, Coslett HB, Whelan H, Watson RT. Directional hypokinesia: prolonged reaction times for leftward movements in patients with right hemisphere lesions and neglect. Neurology. 1985;35(6):855–859. 42 Karnath HO, Dick H, Konczak J. Kinematics of goal-directed arm movements in neglect: control of hand in space. Neuropsychologia. 1997;35(4):435–444. 43 Milner AD, Goodale MA. The Visual Brain in Action (Oxford psychology series). 1st ed. Oxford, NY: Oxford University Press; 1995; p. p.xvii, 248. 44 Lane AR, Ball K, Smith DT, Schenk T, Ellison A. Near and far space: understanding the neural mechanisms of spatial attention. Hum Brain Mapp. 2013;34(2):356–366. 45 Bartolomeo P. Visual neglect. Curr Opin Neurol. 2007;20(4): 381–386. 46 Milner AD, Goodale MA. The Visual Brain in Action (Oxford psychology series). 2nd ed. New York: Oxford University Press; 2006; p. p.xxii, 297. 47 Bickerton WL, Samson D, Williamson J, Humphreys GW. Separating forms of neglect using the apples test: validation and functional prediction in chronic and acute stroke. Neuropsychology. 2011;25(5):567–580. 48 Noordzij M, Tripepi G, Dekker FW, Zoccali C, Tanck MW, Jager KJ. Sample size calculations: basic principles and common pitfalls. Nephrol Dial Transplant. 2010;25(5): 1388–1393. 49 Moher D, Dulberg CS, Wells GA. Statistical power, sample size, and their reporting in randomized controlled trials. JAMA. 1994;272(2):122–124. 50 Behrmann M, Meegan DV. Visuomotor processing in unilateral neglect. Conscious Cogn. 1998;7(3):381–409. 51 Fisk JD, Goodale MA. The effects of unilateral brain damage on visually guided reaching: hemispheric differences in the nature of the deficit. Exp Brain Res. 1988; 72(2):425–435. 52 Goodale MA, Milner AD, Jakobson LS, Carey DP. Kinematic analysis of limb movements in neuropsychological research: subtle deficits and recovery of function. Can J Psychol. 1990; 44(2):180–195. 53 Harvey M, Kra¨mer-McCaffery T, Dow L, Murphy PJ, Gilchrist ID. Categorisation of ‘perceptual’ and ‘premotor’ neglect patients across different tasks: is there strong evidence for a dichotomy? Neuropsychologia. 2002; 40(8):1387–1395. 54 Konczak J, Himmelbach M, Perenin MT, Karnath HO. Do patients with neglect show abnormal hand velocity profiles during tactile exploration of peripersonal space? Exp Brain Res. 1999;128(1–2):219–223. 55 Mattingley JB, Phillips JG, Bradshaw JL. Impairments of movement execution in unilateral neglect: a kinematic analysis of directional bradykinesia. Neuropsychologia. 1994;32(9): 1111–1134. 56 Meador KJ, Loring DW, Baron MS, Rogers OL, Kimpel TG. Hemispatial-limb hypometria. Int J Neurosci. 1988;42(1–2): 71–75. 57 Milner AD, Harvey M, Roberts RC, Forster SV. Line bisection errors in visual neglect: misguided action or size distortion? Neuropsychologia. 1993;31(1):39–49. 58 Pritchard CL, Dijkerman HC, McIntosh RD, Milner AD. Visual and tactile size distortion in a patient with right neglect. Neurocase. 2001;7(5):391–396. 59 Robertson IH, North N. Spatio-motor cueing in unilateral left neglect: the role of hemispace, hand and motor activation. Neuropsychologia. 1992;30(6):553–563. 60 Rossit S, Malhotra P, Muir K, Reeves I, Duncan G, Birschel P, et al. The neural basis of visuomotor deficits in hemispatial neglect. Neuropsychologia. 2009;47(10):2149–2153. 61 Bartolomeo P, Chokron S, Gainotti G. Laterally directed arm movements and right unilateral neglect after left hemisphere damage. Neuropsychologia. 2001;39(10):1013–1021.


2015

VOL .

22

NO .

6

31 427

Ogourtsova et al.


62 Coslett HB, Bowers D, Fitzpatrick E, Haws B, Heilman KM. Directional hypokinesia and hemispatial inattention in neglect. Brain. 1990;113(Pt 2):475–486. 63 Edwards MG, Humphreys GW. Pointing and grasping in unilateral visual neglect: effect of on-line visual feedback in grasping. Neuropsychologia. 1999;37(8):959–973. 64 Gall C, Gu¨nther T, Fuhrmans F, Sabel BA. Contralesional cross-over in chronic neglect: visual search patterns reveal neglect of the ipsilesional hemispace. NeuroRehabilitation. 2012;31(2):171–184.

428 32


2015

VOL .

22

NO .

6

65 Maeshima S, Truman G, Smith DS, Dohi N, Nakai K, Itakura T, et al. Is unilateral spatial neglect a single phenomenon? A comparative study between exploratory-motor and visual-counting tests. J Neurol. 1997;244(7):412–417. 66 McIntosh RD, McClements KI, Dijkerman HC, Birchall D, Milner AD. Preserved obstacle avoidance during reaching in patients with left visual neglect. Neuropsychologia. 2004;42(8):1107–1117. 67 Tegner R, Levander M. Through a looking glass. A new technique to demonstrate directional hypokinesia in unilateral neglect. Brain. 1991;4(114(Pt 4)):1943–1951.

Leftward search in left unilateral spatial neglect.

Recovery from unilateral visuo-spatial neglect?

Unilateral spatial neglect: assessment and rehabilitation strategies.

Different patterns of dissociation in unilateral spatial neglect.

Through the Eyes of Neglect Patients: A Preliminary Eye-Tracking Study of Unilateral Spatial Neglect.

Lateral specialization in unilateral spatial neglect: a cognitive robotics model.

Combining language and space: sentence bisection in unilateral spatial neglect.

Hearing and music in unilateral spatial neglect neuro-rehabilitation.

(Un)awareness of unilateral spatial neglect: a quantitative evaluation of performance in visuo-spatial tasks.

Influence of the stimulus parameters of galvanic vestibular stimulation on unilateral spatial neglect.

Spatial neglect.

Determining the barriers and facilitators to adopting best practices in the management of poststroke unilateral spatial neglect: results of a qualitative study.

Influence of spatial accuracy constraints on reaction time and maximum speed of performance of unilateral movements.

Spatial and temporal dynamics of visual search tasks distinguish subtypes of unilateral spatial neglect: Comparison of two cases with viewer-centered and stimulus-centered neglect.

Impact of spatial neglect on stroke rehabilitation: evidence from the setting of an inpatient rehabilitation facility.

Spatial representation of words in the brain implied by studies of a unilateral neglect patient.

Language-specific dysgraphia in Korean patients with right brain stroke: influence of unilateral spatial neglect.

Unilateral spatial neglect as a presenting manifestation of nonconvulsive status epilepticus.

Perception of moving and stationary gratings in brain damaged patients with unilateral spatial neglect.

Effects of lateralized light flash and color on unilateral neglect.

Spatial attention systems in spatial neglect.

Perceptual and premotor factors of unilateral neglect.

Preferred directions of arm movements are independent of visual perception of spatial directions.

Children's development of reaching: temporal and spatial aspects of aimed whole-arm movements.