17
This article was downloaded by: [University Of Maryland] On: 15 October 2014, At: 05:13 Publisher: Routledge Informa Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House, 37-41 Mortimer Street, London W1T 3JH, UK Journal of Clinical and Experimental Neuropsychology Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/ncen20 Nonlateralized Attentional Deficits: An Important Component Behind Persisting Visuospatial Neglect? Hans Samuelsson , Elisabeth Hjelmquist , Christer Jensen , Sven Ekholm & Christian Blomstrand Published online: 09 Aug 2010. To cite this article: Hans Samuelsson , Elisabeth Hjelmquist , Christer Jensen , Sven Ekholm & Christian Blomstrand (1998) Nonlateralized Attentional Deficits: An Important Component Behind Persisting Visuospatial Neglect?, Journal of Clinical and Experimental Neuropsychology, 20:1, 73-88 To link to this article: http://dx.doi.org/10.1076/jcen.20.1.73.1481 PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content. This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http:// www.tandfonline.com/page/terms-and-conditions

Nonlateralized Attentional Deficits: An Important Component Behind Persisting Visuospatial Neglect?

  • Upload
    hans

  • View
    212

  • Download
    0

Embed Size (px)

Citation preview

This article was downloaded by: [University Of Maryland]On: 15 October 2014, At: 05:13Publisher: RoutledgeInforma Ltd Registered in England and Wales Registered Number: 1072954 Registered office: MortimerHouse, 37-41 Mortimer Street, London W1T 3JH, UK

Journal of Clinical and ExperimentalNeuropsychologyPublication details, including instructions for authors and subscription information:http://www.tandfonline.com/loi/ncen20

Nonlateralized Attentional Deficits: An ImportantComponent Behind Persisting Visuospatial Neglect?Hans Samuelsson , Elisabeth Hjelmquist , Christer Jensen , Sven Ekholm & ChristianBlomstrandPublished online: 09 Aug 2010.

To cite this article: Hans Samuelsson , Elisabeth Hjelmquist , Christer Jensen , Sven Ekholm & Christian Blomstrand (1998)Nonlateralized Attentional Deficits: An Important Component Behind Persisting Visuospatial Neglect?, Journal of Clinicaland Experimental Neuropsychology, 20:1, 73-88

To link to this article: http://dx.doi.org/10.1076/jcen.20.1.73.1481

PLEASE SCROLL DOWN FOR ARTICLE

Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) containedin the publications on our platform. However, Taylor & Francis, our agents, and our licensors make norepresentations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose ofthe Content. Any opinions and views expressed in this publication are the opinions and views of the authors,and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be reliedupon and should be independently verified with primary sources of information. Taylor and Francis shallnot be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and otherliabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to orarising out of the use of the Content.

This article may be used for research, teaching, and private study purposes. Any substantial or systematicreproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in anyform to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http://www.tandfonline.com/page/terms-and-conditions

* This research was in part supported by grants from the Delegation for Social Research (No. 90-0176), The 1987year’s Foundation of Stroke Research, Greta and Einar Asker Foundation, Per-Olof Ahl Foundation, John andBrit Wennerström Foundation, Rune and Ulla Amlöv Foundation, and Hjalmar Svensson Foundation. The authorsthank Hans Naver for his neurological evaluation of the subjects, and Knut Larsson and Ulf Norrsell for com-ments on parts of this manuscript.Address correspondence to: Hans Samuelsson, Department of Psychology, University of Göteborg, Haraldsgatan1, 413 14 Göteborg, Sweden.Accepted for publication: September 17, 1997.

Journal of Clinical and Experimental Neuropsychology 1380-3395/98/2001-073$12.001998, Vol. 20, No. 1, pp. 73-88 © Swets & Zeitlinger

Nonlateralized Attentional Deficits:An Important Component Behind Persisting Visuospatial

Neglect?*

Hans Samuelsson1, E.K. Elisabeth Hjelmquist2, Christer Jensen3, Sven Ekholm3,and Christian Blomstrand2

1University of Göteborg, Sweden, and Departments of2Neurology, and3Radiology, Sahlgrenska UniversityHospital, Göteborg

ABSTRACT

Simple reaction time was examined in a consecutive series of 60 right hemisphere stroke patients at thepostacute stage and at 6 to 7 months poststroke. Reaction times to auditory stimuli were measured withinthe ipsilesional side of space. Patients showing contralateral neglect in conventional tests of neglectshowed significantly increased reaction times at the postacute stage and at the follow-up compared to thosenot showing neglect and to those in a group of normal controls. The results suggest that a lowered generalattentional capacity may constitute a central component behind persistent neglect. An additional analysisof the CT scans of the patients showed that a large lesion including the paraventricular white matter in thetemporal lobe was the most important anatomical correlate of persisting slow reactions.

Patients showing visuospatial neglect fail to re-spond to stimuli located at the side opposite tothe brain lesion. Spatial neglect is operationallydefined by the omissions made in tests such ascopying and freehand drawing, target cancella-tion, and reading (Heilman, 1979; Mesulam,1985). Clinical and experimental evidence indi-cates several direction-specific attentional defi-cits that are central components in the neglectphenomena, such as: (1) a pathologically en-hanced ipsilesional bias in the attentional orien-tation (Kinsbourne, 1970), (2) impaired abilityto disengage the focus of attention when atten-tion is to be shifted in a contralesional direction(Posner, Walker, Friedrich, & Rafal, 1984), and(3) impaired arousal and orienting responses to

contralesional stimulation (Heilman & Valen-stein, 1979).

In addition to direction-specific deficits, re-sults from recent studies on patients with righthemisphere brain damage indicate that a low-ered attentional capacity that is independent ofthe spatial location of the stimulus may repre-sent an important component behind the neglectphenomena. In support of this hypothesis, Kar-nath (1988) and Robertson (1989) demonstratedthat patients with visuospatial neglect showedslow reactions in target detection tasks with afixed exposure time. Further, Feinberg, Haber,and Stacy (1990) found that patients with visuo-spatial neglect differed from controls by show-ing a higher number of omissions in Double Si-

Dow

nloa

ded

by [

Uni

vers

ity O

f M

aryl

and]

at 0

5:13

15

Oct

ober

201

4

74 HANS SAMUELSSON ET AL.

multaneous Stimulation tests conducted exclu-sively on the ipsilesional (‘‘not neglected’’) sideof the body. In patients with neglect, significantassociations were observed in a test situationbetween increased symptoms of spatial neglectand increased demand upon selective attentionor divided attention (Kaplan et al., 1991; Rapc-sak, Verfaellie, Fleet, & Heilman, 1989; Robert-son & Frasca, 1992). Finally, Robertson (1990)presented results indicating a relationship be-tween the severity of neglect and difficultiesshown in a task with increased demand on serialinformation processing.

Karnath (1988) proposed that a general defectof attentional capacity or information processingcapacity is one of three components specificallyresponsible for the clinical manifestation of ne-glect. Robertson and Frasca (1992) and Robert-son (1993) suggested that the presence of a gen-eral attentional deficit (i.e., deficient alertnessand arousal) in patients with visuospatial neglectmay be responsible for the persistence of neglectafter the acute stage has ended. The concept ofarousal refers to a number of physiological pro-cesses that have an energizing influence on per-formance, such as enhancement of stimulus pro-cessing and facilitation of response output (for areview, see Mesulam, 1985; Robbins, 1997).Arousal or arousal-like processes are involved inthe regulation of the level of wakefulness andalertness. The level of alertness is considered tobe an important component of attention, becauseit refers to the individual’s general receptivity toinput information (Posner, 1975). The level ofalertness may change slowly during the day(tonic alertness), or it may change fast (phasicalertness), for example, following a warningsignal in a reaction time task (Posner, 1975).

A growing number of findings indicates thatneural systems within the right hemisphere maybe dominant for the generation of certain aspectsof arousal or alertness (Coslett, Bowers, & Heil-man, 1987; Heilman, Schwartz, & Watson,1978; Heilman & Van Den Abell, 1979, 1980;Howes & Boller, 1975; Ladavas, Pesce, &Provinciali, 1989; Watson, Andriola, & Heil-man, 1977). Accordingly, Heilman et al. (1978)and Robertson and Frasca (1992) suggested thatdefective neural systems for the generation of

arousal or alertness within the right hemispheremay represent a possible anatomical componentbehind lowered attentional capacity in patientsexhibiting spatial neglect. According to Robert-son and Frasca, a deficient generation of an alertand vigilant state in patients showing neglectmay result in a lowered capacity to compensatefor the asymmetric defect in the orientation ofattention. This may then result in persistence ofthe neglect symptoms.

The hypothesis that persistent neglect is re-lated to impaired nonlateralised attention wasrecently supported by results from two studiesof patients showing persistent (chronic) spatialneglect after r ight hemisphere damage.Hjaltason, Tegner, Tham, Levander, and Ericson(1996) reported that the presence of chronic ne-glect 1 to 5 years post stroke was significantlyassociated with aberrant performance in a test ofsustained attention. Robertson, Tegner, Tham,Lo, and Nimmo-Smith (1995) showed thatsymptoms of chronic neglect in right hemi-sphere stroke patients improved after the admin-istration of a verbal self-alerting training proce-dure.

The present study was aimed at testingwhether persistent neglect is associated with ageneral attentional deficit (i.e., deficient alert-ness), and whether such a deficit is related to thelocation and extent of the lesion within the righthemisphere. The presence of a general atten-tional deficit was defined as the lengthening ofthe reaction time to auditory stimuli presentedipsilesionally. Simple reaction time was chosenbecause the use of reaction time tasks is wellestablished in clinical and experimental researchon attentive behavior (Posner, 1986; Sturm,1996; Van Zomeren & Brouwer, 1994). Thismeasure has the advantage of being brief andeasily administered, and perhaps more impor-tant, simple reaction time emphasizes mentalspeed, but minimizes the demand for cognitiveanalysis. Thus, the number of confounding vari-ables is minimized. Ratings of emotional stateand of perseverative responses were also in-cluded, because emotional state and deficientcontrol of impulsive responses may affect thereaction times assessed in this study.

Dow

nloa

ded

by [

Uni

vers

ity O

f M

aryl

and]

at 0

5:13

15

Oct

ober

201

4

ATTENTIONAL DEFICITS IN SPATIAL NEGLECT 75

METHODS

SubjectsOf 181 patients with a right hemisphere strokeconsecutively admitted to the stroke unit at theneurological department of Sahlgrens UniversityHospital, Göteborg, 60 patients were selected forthis study (Samuelsson, Hjelmquist, Naver, &Blomstrand, 1996). Patients were excluded if theymet any of the following criteria: a prior clinicallymanifested cerebrovascular accident or other cere-bral disorder; a return to normal or virtually nor-mal neurological function within 24 hr; a history ofmental retardation, serious drug abuse, orhospitalisation for psychiatric treatment; not right-handed; severely ill and not able to co-operate; notSwedish-speaking; older than 77 years of age; orhaving severely defective vision in both eyes. Acontrol group of 34 age- and gender-matched right-handed subjects without a history of neurologicaldeficits, serious drug abuse, or hospitalization forpsychiatric treatment was selected from the popu-lation of Göteborg.

A standard neurological examination was con-ducted on all patients at the initial postacute stage.Patients showing no neurological symptoms, oronly mild nondisabling symptoms 3 weeks poststroke were defined as minor stroke patients (n =19), and those showing symptoms persisting morethan 3 weeks after the stroke event were defined asmajor stroke patients (n = 41). A neuropsychologi-cal assessment was conducted at 1 to 4 weeks poststroke except for 4 patients who were examinedduring the second month post stroke. A follow-upexamination was made 6 to 7 months post stroke.The occurrence of visuospatial neglect was estab-lished by the following seven subtests: Line cross-ing, Letter cancellation, Star cancellation, Figurecopying, Representational drawing, Article read-ing, and Sentence copying. The tests were slightlymodified versions of the subtests in the Beha-vioural Inattention Test (BIT). BIT is a valid andstandardized measure of unilateral visual neglect(Wilson, Cockburn, & Halligan, 1987). The cutofflevel for an aberrant number of omissions in eachsubtest was represented by the first score below thenormal range obtained from the control group. Foreach test scoring at or below the individual cutofflevel, a laterality score was computed by measur-ing the asymmetry in the number of detected tar-gets; the number of detections made at the left sideof the test sheet or at the left side of the figureswas divided by the total number of detections andexpressed in percent (Friedman, 1992). Thus, thelaterality score ‘‘50%’’ means that an equal num-ber of targets were detected at both sides of the

test, whereas a lower percentage indicates a bias inthe performance with less detections on the leftside. In order to avoid confusion of centrally andlaterally located omissions, the midpart of eachtest was excluded from the computation of the lat-erality score (Gainotti, Giustolisi, & Nocentini,1990). In the control group, 23 subjects showedomissions in some of the tests. The average lateral-ity score for these tests was 50% (SD= 2%), witha range of 44%–56% (for details, see Samuelssonet al., 1996).

The following criteria for visuospatial neglectwere applied: a score below or at the cutoff levelfor omissions in at least one of the subtestsandacontralesional asymmetry for the number of targetsomitted (that is, a laterality score below 44% in atleast one of the tests, and no test with scores above56%).

On the basis of the above criteria, the patientswere divided into three groups: (1)the neglectgroup, consisting of 18 patients with a majorstroke showing visuospatial neglect; (2)the majorgroup, consisting of 23 patients with a majorstroke but without symptoms of visuospatial ne-glect; and (3)the minor group,consisting of 19patients with a minor stroke. None of the patientswith a minor stroke showed visuospatial neglect.

Subject CharacteristicsDuring the administration of the neuropsychologi-cal test battery, none of the patients showed signsof gross deficits in visual acuity or hearing; that is,all patients could read words in 12-point Geneva-type print viewed from a distance of approximately45-50 cm, and all subjects took part in a normaldiscussion without showing any hearing problems.In connection with the reaction time measurementand the clinical examination conducted by a staffneurologist, the subjects were asked about hearingand sight deficits before the stroke event. Also,these sensory functions were screened in the pa-tient groups at the neurological examination. Asshown in Table 1, no statistically significant dif-ferences were found between the groups regardingthe incidence of impaired hearing and sight.

A screening of general intellectual ability andbasic attention span efficiency was conducted us-ing a short form of the Similarities subtest consist-ing of six word pairs; the forward part of the DigitSpan subtest from the Swedish version (the CVB-scale) of the Wechsler Bellevue Scale (Wechsler,1944); and the Mini-Mental State Examination(Folstein, Folstein, & McHugh, 1975). The cutofflevel for defective performance was set at 23 forthe Mini-Mental State Examination (Dick et al.,1984) and four digits for the Digit Span subtest

Dow

nloa

ded

by [

Uni

vers

ity O

f M

aryl

and]

at 0

5:13

15

Oct

ober

201

4

76

HA

NS

SA

MU

EL

SS

ON

ET

AL

.

Table 1. Subject Characteristics.

Neglect group(n = 18)

Major stroke(n = 23)

Minor stroke(n = 19)

Controls(n = 34) pa

Age (years)M (SD)Range

GenderM/F

Education (years)M (SD)

Similaritiesb

M (SD)Digit Span Forward 4 digits

n (%)MMSE 23

n (%)Defective hearing

n (%)Defective sight

n (%)Visual field deficit

n (%)

62.1145-75

8/10

9.61

7.61

1

2

5

2

9

(19.49)

(14.07)

(13.09)

(16)

(11)

(28)

(11)

(50)

59.6521-77

16/7

11.39

9.18

2

1

7

2

6

(15.23)

(14.46)

(12.10)

(19)

(14)

(30)

(18)

(26)

59.2130-74

11/8

10.84

9.05

2

1

2

3

(12.04)

(15.09)

(12.01)

(10)

(15)

(10)

(16)

61.2129-75

17/17

10.88

9.26

1

0

6

1

(12.50)

(14.92)

(11.78)

(13)

(10)

(18)

(13)

NS

NS

NS

NS

NS

NS

Note.MMSE = Mini-Mental State Examination.a Tested with the one-factor ANOVA or the chi-square test.b A short form consisting of six word pairs.

Dow

nloa

ded

by [

Uni

vers

ity O

f M

aryl

and]

at 0

5:13

15

Oct

ober

201

4

ATTENTIONAL DEFICITS IN SPATIAL NEGLECT 77

(Lezak, 1983). No differences were found betweenthe groups regarding age, gender, years in school,and basic intellectual abilities (Table 1).

Reaction Time AssessmentGeneral attention was measured usingwarned sim-ple reaction timeto auditory stimuli presented onthe side opposite to the neglected left side. Thepatient was sitting in front of a table on which akey response box was placed. The subject’s righthand rested on the table in front of the box and theindex finger was resting on the response key. Anauditory stimulus was presented from a separatebox with a small loudspeaker. The box was placedon top of the response box about 10 cm above thekey. The response key and the stimulus box wereplaced at the right side of the subject, approxi-mately 23 cm from the subject’s body midline.Thus, the locations of the stimuli and the manualresponses were ipsilesional and accordingly con-tralateral to the part of space neglected by the pa-tients in the neglect group. The stimulus box wasviewed from a distance of approximately 45 cm.

The stimulus consisted of a loud and short puretone. The patient was instructed to press the key asrapidly as possible on the appearance of the stimu-lus. A practice series of 3 trials followed by a con-secutive series of 11 presentations were given. Re-action times longer than 999 ms or shorter than100 ms were omitted from the analysis and re-placed by a new trial until 11 adequate responseswere obtained. The omitted trials were registeredaserrors of omissions (> 999)anderrors of com-missions (< 100)respectively. All patients wereable to perform 11 adequate responses. All sub-jects were asked if they experienced difficulties inhearing the tone. No substantial difficulties werereported.

The experimenter started each trial by giving averbal warning and initiating the presentation ofthe target stimulus by pushing a button at the backof the response box. Each stimulus then appearedat random intervals of 2 to 7 s. The verbal warningconsisted of the expression ‘‘are you ready’’ givenat the demonstration trials and at three additionaltrials. The remaining eight trials were initiated bygiving the expression ‘‘and again.’’ The reactiontime was the time lapse between the presentationof the target stimulus and the depressing of thekey. The time was measured in milliseconds by aninternal integrated electronic counter. Individualperformance was defined by the median values ofthe 11 reaction trials.

Other Variables

Variability of reaction timesThe intraindividual variability of the reaction timeswas defined by the interquartile range (IQR) of the11 reaction time trials (Individual IQR of RT).

Rating of the emotional stateEach subject was told to estimate his or her emo-tional state by putting a mark on a visual analoguescale. The scale was modified from Aitken (1969)and consisted of a 100-mm long vertical line withthe lower end representing ‘‘worst mood’’ and theupper end representing ‘‘best mood.’’ At the initialassessment, a sheet with two lines was used to ratethe present perception of the emotional state andthe state before the accident. A third line presentedon a single sheet was used to assess perception ofthe emotional state at the time of the follow-upassessment.

Perseverative responsesPerseverative responses were assessed using theAlternating Sequences task. This task was modi-fied from Christensen (1975) and Luria (1966) andis considered sensitive for defective executive con-trol functions. The subjects were asked to draw asequence of two circles, one cross, and three trian-gles in the first 6 squares in a vertical row of 50consecutive squares. The subjects were then told tocontinue to draw exactly the same sequence of fig-ures repeatedly until all of the squares in the rowwere filled. Perseverative (erroneous repeated)drawing of figures within each sequence was re-corded. This measurement was only executed atthe initial assessment.

Location and size of brain damageRoutinely, all patients had an acute CT scan of thebrain. A second CT scan examination was con-ducted 4 weeks or later after onset. Exceptions in-cluded one patient who was examined during thesecond day post stroke only, and another patientwho was re-examined with MR scanning. Withguidance from the atlas of Kretschmann and Wein-rich (1986), two trained neuroradiologists – with-out knowledge of the neuropsychological data –judged the presence or absence of lesions within38 individual brain areas. In addition, the extent ofthe lesion was described by the measure of the sag-ittal and transversal size of the lesion (rounded offto the nearest 0.5 cm) on the scan where the lesionhad its greatest extent. Details of these assessmentswere reported elsewhere (Samuelsson, Jensen,Ekholm, Naver, & Blomstrand, 1997).

Dow

nloa

ded

by [

Uni

vers

ity O

f M

aryl

and]

at 0

5:13

15

Oct

ober

201

4

78 HANS SAMUELSSON ET AL.

Statistical AnalysesComparisons between the patient groups and thecontrol group of median reaction times, intra-individual IQR of reaction times, perceived emo-tion, perseverative responses, errors of omission,and errors of commission were made using theKruskal-Wallis one-way analysis of variance andpost hoc two sample tests adjusted for multiplecomparisons (Siegel & Castellan, 1988). Compari-sons of the reaction times exhibited at the first andsecond assessment were made by using theWilcoxon signed ranks test. These analyses werecorrected for multiple comparisons by theBonferroni method.

The relationships between increased reactiontimes and the neuroradiological variables were an-alyzed using stepwise logistic regression (Hosmer& Lemeshow, 1989). An interactive forward pro-cedure was applied using the presence or absenceof increased reaction time as a dependent variable.All neuroradiological variables showingp < .05 attwo-sample comparisons (Fisher exact test orMann-Whitney test without correction for multiplecomparisons) were included in this analysis. Oddsratios and 95% confidence intervals of the ratioswere given for the variables selected by thestepwise procedure. Odds ratios were consideredstatistically significant when they did not include‘‘1’’ in the confidence interval.

Nonparametric methods were used because: (1)the variability of the reaction time values was nothomogenous across the groups, (2) the valuesshowed a poor fit to the normal distribution, and(3) the neglect group at the follow-up assessmentwas small (n = 6).

RESULTS

Figure 1 shows the box-plot of the median val-ues of reaction times in the control group and inthe three groups of patients. Compared with thenonneglect patient groups and the control group,the neglect group showed longer reaction times(H = 32.64,df = 3, p < .001). The median reac-tion times exhibited by the control, minor, ma-jor, and neglect groups were 217, 240, 251, and343 ms, respectively. Errors of commission dur-ing the reaction time test were found in all fourgroups and no statistically significant differ-ences were obtained between the groups (H =0.19,df = 3, p = .98). Errors of omission wereuncommon; only three patients in the neglectgroup showed this phenomenon.

Other Neuropsychological VariablesIn addition to a lengthening of the reaction time,the patients in the neglect group showed greatervariability of the reaction times, a lower ratingof the perceived emotional state, and a higherincidence of perseverative responses relative tothe control group (Table 2).

In order to examine if any of these variablescould explain the lengthening of the reactiontimes obtained for the neglect group, a split wasmade of the neglect group into two subgroupsfor each variable (Table 3). For individual IQRof reaction times, the cutoff value for the splitwas the 95th centile of the IQR values obtainedin the control group (IQR cutoff = 92ms); forperseverative responses the cutoff was the pres-ence of a perseverative response; and for per-ceived emotion, the split was the median valueof perceived emotion in the neglect group (cut-off = 61mm). The aim was to compare the reac-tion times between the control group and theneglect group, eliminating the influence of othervariables. Table 3 shows that the patients in theneglect group exhibited significantly slower re-actions as compared to the control group irre-spective of the presence or absence of aberrantindividual IQR, of perseverative responses, or ofperceived emotions below the median.

Neuroradiological VariablesIn order to examine the relationship between theneuroradiological variables and the reactiontimes, the patients were divided into two groups:one consisting of patients with normal medianreaction time values, and the other consisting ofpatients with aberrant median reaction time val-ues. The cutoff for aberrant values was the 95thcentile of the median reaction time obtained inthe control group (cutoff = 315 ms). The minorgroup was not included in this part of the studybecause these patients differed from the othersby not showing slow reactions at the follow-upand by showing only a few abnormal values atthe initial assessment. Furthermore, the patientsin the minor group differed from the other pa-tients by showing small lesions; the size of thelesion was < 1.5 cm in the sagittal and thetransversal plane in a majority of these patients.Also, one patient in the major group was ex-

Dow

nloa

ded

by [

Uni

vers

ity O

f M

aryl

and]

at 0

5:13

15

Oct

ober

201

4

ATTENTIONAL DEFICITS IN SPATIAL NEGLECT 79

Fig. 1. Simple reaction time at the first assessment. The box plots display the 10th, 25th, 50th, 75th and 90thcentiles for each group. The values above the 90th centile and below the 10th centile are plotted sepa-rately.* p < .05, after adjustments for multiple comparisons.

cluded from this part of the study because noclearly defined lesion was found on the CT scan.Thus, 40 patients with a major stroke were in-cluded and divided into a group with slow per-formers (n = 16) and a group with normal per-formers (n = 24).

Univariate two-sample analysis with theFisher exact test or the Mann-Whitney test re-vealed a significant association between inci-dence of increased reaction times and a lesionincluding the lateral part of the semioval centrewithin the frontal lobe (p = .005); a lesion in-volving the paraventricular white matter in the

temporo-parietal border area (p = .014); and alarge size of the lesion in the sagittal plane (p =.015).

Table 4 shows the results from the applicationof the stepwise selection of the above variablesusing logistic regression. The table shows thevariables selected as the most important corre-lates of slow reactions. Unadjusted and adjustedodds ratio and 95% confidence interval aregiven. The adjustment of the odds ratio wasmade by including the maximal transversal andsagittal size of the lesion into the logistic model.The table shows that after adjusting for the size

Dow

nloa

ded

by [

Uni

vers

ity O

f M

aryl

and]

at 0

5:13

15

Oct

ober

201

4

80

HA

NS

SA

MU

EL

SS

ON

ET

AL

.

Table 2. First Assessment Results.

Group

Significanttwo sample

comparisonsb

Control Minor Major Neglect

Mdn (IQR) Mdn (IQR) Mdn (IQR) Mdn (IQR) pa

Individual IQR on RT trialsPerseverative responsesPerceived emotional state

471079

(43)(10)(26)

631066

(30)(10)(47.2)

521078

(47)(10)(42.8)

921161

(54)(15)(25)

< .01< .01< .05

1 vs. 41 vs. 41 vs. 4

2 vs. 4

Note. IQR = Interquartile range; RT = Reaction time; Mdn = median.a Kruskal-Wallis test.b Two sample comparisons showing at leastp = .05 after correction for multiple comparisons.

Dow

nloa

ded

by [

Uni

vers

ity O

f M

aryl

and]

at 0

5:13

15

Oct

ober

201

4

ATTENTIONAL DEFICITS IN SPATIAL NEGLECT 81

Table 4. Neuroradiological Variables Selected by Stepwise Logistic Regression.

Neglect

OR 95% CI ORadjusteda 95% CI

First assessmentLateral semioval centerwithin the frontal lobe

Follow-upb

Temporal paraventricularwhite matter

9.0

29.3

1.9

4.1

42.9

209.0

5.8

25.1

1.0

2.4

33.4

260.2

Note. OR = Odds ratios for increased reaction times; CI = confidence intervals.a Odds values adjusted for the size of the lesion.b Follow-up missing in 5 patients.

Table 3. Reaction Time in the Neglect Group.a

Reaction Time

n Median (IQR)

Control groupNeglect group splits

High auditory IQRNormal auditory IQRPerseverative responsesNo perseverative responsesPerceived emotion medianPerceived emotion > median

34

9911799

217

372321341345372305

(162)* b

(161)*b

(137)*b

(159)*b

(159)*b

(134)*b

(160)*b

Note. IQR = Interquartile range.a Neglect group divided into patients with defective and normal performance in three neuropsychological vari-ables.b p < .05 compared with the control group (post hoc two-sample comparisons adjusted for multiple comparisons).* p > .05 compared with the other subgroup in the split of the neglect group.

of the lesion, the odds ratio was lowered for le-sions including the lateral part of the semiovalcentre within the frontal lobe. The adjusted oddsratio only reached the cutoff point for a statisti-cally significant value.

Reaction Time at the Follow-upFor the analyses of the follow-up data, the ne-glect group was split into one group of patientswho had recovered from the initial symptoms ofvisuospatial neglect (the recovered group;n = 9)and another group that still showed symptoms ofvisuospatial neglect (the unrecovered group;n =6). The recovered patients performed within therange of the controls in all neglect tests, whereas

the unrecovered patients fulfilled the criterionfor neglect in at least one of the tests. Three pa-tients in the neglect group were missing at thefollow-up; two had suffered a second stroke andone had moved to another part of the country. Ofthe patients in the other two groups, two haddied, one had suffered a second stroke, one hadmoved to another part of the country, one couldnot be located, and one refused to participate.Thus, at the follow-up, the minor group con-sisted of 15 patients and the major group con-sisted of 21 patients.

The box-plots of the median reaction timevalues in Figure 2 show that patients with re-maining symptoms of neglect also showed a per-

Dow

nloa

ded

by [

Uni

vers

ity O

f M

aryl

and]

at 0

5:13

15

Oct

ober

201

4

82 HANS SAMUELSSON ET AL.

Fig. 2. Simple reaction time at the follow-up. The box plots display the 10th, 25th, 50th, 75th and 90th centilesfor each group. The values above the 90th centile and below the 10th centile are plotted separately.* p < .05, after adjustments for multiple comparisons.

sistent lengthening of the reaction times as com-pared to the control group and the minor group(H = 19.6,df = 4, p < .001). In contrast to thepatients with persistent neglect, the patients whohad recovered from neglect showed significantlyimproved reaction times (Wilcoxon signed-ranktest:z = 2.67,p < .05). In the patients showingtransient neglect symptoms, the median reactiontime at the first and the second assessment was341 and 232 ms, respectively, and the same me-dian values in the patients showing persistentsymptoms of neglect were 400 and 393 ms. Er-rors of omission were not observed in any of thegroups with the exception of one patient in themajor group. Errors of commission were ob-served for some subjects in each group, but nosignificant group differences were found (H =4.9,df = 4, p = .30).

Table 5 shows that a low rating of the per-ceived emotional state was obtained for the re-covered group as well as for the unrecoveredgroup as compared to the controls. The rating ofthe perceived emotional state as well as the indi-vidual IQR of the reaction times did not differbetween the group that recovered and the onethat did not (Table 5).

Neuroradiological Variables at the Follow-upThe analysis of the relationship between inci-dence of impaired reaction times at the follow-up and the location and size of the lesion waslimited to the patients with a major stroke. Of 35patients with a major stroke, 10 showed abnor-mally slow reactions. A statistically significantassociation was found between a lengthening ofthe reaction times and lesions involving the fol-

Dow

nloa

ded

by [

Uni

vers

ity O

f M

aryl

and]

at 0

5:13

15

Oct

ober

201

4

ATTENTIONAL DEFICITS IN SPATIAL NEGLECT 83

Table 5. Intraindividual IQR of Reaction Time and Perceived Emotional State at the Follow-up.

Neglect groupTwo samplecomparisonsNot recovered Recovered Controls

Mdn (IQR) Mdn (IQR) Mdn (IQR) pa 1vs.2 1vs.3 2vs.3

Individual IQR on RT trialsPerceived emotional state

77.544

(82)(14)

4750

(28.5)(28.2)

4779

(43)(26)

< .121< .001

–NS

–< .05

–< .05

Note. IQR = Interquartile range; RT = Reaction time; Mdn = median.a Kruskal-Wallis test.

lowing structures: the paraventricular white mat-ter in the temporal lobe (Fishers exact test:p =.0003), the paraventricular white matter in thetemporo-parietal border area (p = .002), thetransverse temporal gyri (p = .007), the middletemporal gyrus (p = .003), and the superior tem-poral gyrus (p = .002). An association with ab-normally slow reactions was also indicated forlesions involving the genu of the internal cap-sule (p = .043) and for a large-sized lesion in thesagittal plane (p = .015). The application ofstepwise selection of these variables using logis-tic regression analysis resulted in a selection oflesions involving the paraventricular white mat-ter in the temporal lobe as the most importantcorrelate of slow reactions. None of the othervariables was selected by the stepwise proce-dure.

As shown in Table 4, the odds ratio for in-creased reaction times following a lesion involv-ing the paraventricular white matter in the tem-poral lobe was high, and independent of the sizeof the lesion, this finding was statistically true.Of 10 patients with abnormally increased reac-tion times, 8 (80%) showed a lesion that in-volved this area of the brain, whereas only 3 of25 patients (12%) with normal reaction timesshowed such a location of the lesion.

DISCUSSION

The present results clearly indicate that patientssuffering from contralesional visuospatial ne-glect also suffer from attentional defects withinthe ipsilesional side of space; that is, patients

with visuospatial neglect showed a disturbedability to respond to auditory stimuli presentedwithin the ipsilesional side of the extrapersonalspace. Furthermore, the patients with symptomsof neglect remaining 6 to 7 months after thestroke still showed significantly increased reac-tion times, whereas patients who showed signifi-cant improvements in their reaction times alsorecovered from the neglect symptoms. The re-sults seem to support the notion that patientswith visuospatial neglect suffer from a generalattentional deficit, and that remaining symptomsof neglect are associated with a persistent defectof general attentional capacity. Furthermore, theresults emphasize the relationship between thepersistence of a general attentional deficit and alarge lesion including the deep white matter inthe temporal lobe. The finding that patients withsignificant improvements of their reaction timesalso recovered from the neglect symptoms,shows that the presence of increased reactiontimes at the early postacute stage are not suitableas a predictor of persistence of the neglectsymptoms. Increased reaction times at the fol-low-up are, on the other hand, indicative of per-sistent neglect.

The concept of attention is not a homogenousconstruct; it may be subdivided into an intensitycomponent, a selectivity component, and a com-ponent related to supervisory attentional control(Van Zomeren & Brouwer, 1994). Alertness andsustained attention represent the intensity aspectof attention. Alertness has been described as ahypothetical concept referring to physiologicalchanges in the organism, which alter the recep-tivity to stimulation (Posner, 1975). For exam-

Dow

nloa

ded

by [

Uni

vers

ity O

f M

aryl

and]

at 0

5:13

15

Oct

ober

201

4

84 HANS SAMUELSSON ET AL.

ple, a warning signal or instruction telling thesubject that a target stimulus is at hand, willprobably lead to a heightened level of alertness.The alert state is believed to result in a greaterreceptivity and faster response to the target stim-ulus. This altered level of alertness is defined asphasic changes of alertness (Posner, 1986).

Slow changes in alertness, for example overthe course of a day, are termed tonic changes(Posner, 1986). Altered levels of tonic alertnessare probably closely related to the ability to sus-tain attention during the entire performance of atest. Tests requiring performance over longerperiods of time and tests with a low rate of tar-get stimulus are suggested to be sensitive to adeficient sustained attention. According to VanZomeren and Brouwer (1994), the clinical signsof defective sustained attention include:

(1) differences between the performance atthe initial trials and the trials at the end of thetest (the time-on-task effect), (2) the occurrenceof short lapses of attention during the perfor-mance of the test, and (3) intraindividual vari-ability of the results obtained in the test.

The reaction time task as measured in thisstudy, probably reveals the intensity aspects ofattention, because this task requires fast reac-tions to a single stimulus following an auditorywarning. The cerebral mechanism for mediationof phasic alertness is probably crucial for theperformance in this task. Defective tonic alert-ness may also influence the performance in thistask, although the tonic component may be lessimportant as compared to the phasic component,because the reaction time series was relativelyshort (11 trials) and each reaction trial was pre-ceded by a warning. Furthermore, although theinfluence of the intraindividual variation of thereaction times was controlled, there were stillstatistically significant group differences in thereaction times.

Selectivity of attention refers to the ability toselect one source of information or one targetstimulus among other distractors (focused atten-tion) and the ability to attend and respond simul-taneously to multiple sources of task-relevantinformation (divided attention) (Van Zomeren &Brouwer, 1994). The present reaction time taskdoes not represent a measure of the selectivity

component of attention, because only one stimu-lus was presented at each trial and no distractorswere included. Consequently, the results do notallow inferences about these components of at-tention.

Supervisory attentional control refers to one’sability to use mental control strategies in orderto adjust the attentional resources in accordancewith the requirements of a task. Supervisoryattentional control may be an important factor incomplex non-routine tasks requiring a flexiblealternation ofattention betweendifferent aspectsof the stimulus material (Van Zomeren &Brouwer, 1992). The present reaction time taskis not a measure of complex attentional control,as the task is rather simple and the requirementsof altered focus of attention are low. However,some components of ‘‘executive’’ control arerequired, namely, the inhibition of an impulsiveresponse to press the button on the auditorywarning or before the appearance of the targetstimuli. Although an impulsive response wasregistered in several subjects, patients in the ne-glect group did not differ from the other subjectson this variable.

Other nonattentional components that mayhave influenced the reaction time were motiva-tional components and primary motor and sen-sory functions. These variables were screened ina relatively rough way, but there were no indica-tions that the results obtained were due to defec-tive motor or sensory functions, or to alteredmotivation due to perception of a low emotionalstate.

Another methodological problem is that ne-glect of sensory information per se can result inslow reactions. We tried to control for the contra-lesional inattention in the neglect phenomenonby placing the stimulus box at the side ipsilateralto the location of the brain damage. Furthermore,in an attempt to control for a hemispatial or di-rectional akinesia, the response box was placedon the ipsilesional side and all patients used theirunaffected right hand during the testing. Also,the arrangement with a stationary stimulus andresponse box and with the subject resting the in-dex finger on the response key during the entireexamination, was aimed to control for deficientability to move attention in external space.

Dow

nloa

ded

by [

Uni

vers

ity O

f M

aryl

and]

at 0

5:13

15

Oct

ober

201

4

ATTENTIONAL DEFICITS IN SPATIAL NEGLECT 85

In summary, the patients in the neglect groupseem to differ from the other patients by suffer-ing from a general defect in the intensity aspectsof attention, that is, from deficient generationand/or maintenance of alertness. It is also likelythat the patients with persistent symptoms ofneglect suffered from a prolonged defect inalertness, whereas the patients showing recoveryfrom neglect may have gained better attentionalcapacity from the recovery of alertness.

Abnormally slow reactions at the first assess-ment as well as at the follow-up were associatedwith large lesions mainly involving cortical andsubcortical structures within the territory of arte-ria cerebri media. Within this area of the brain,damage to the lateral part of the semioval centerwithin the frontal lobe was the most importantcorrelate of increased reaction times at the firstassessment, whereas damage to the paraventri-cular white matter in the temporal lobe was themost important correlate of the lengthening ofthe reaction times at the follow-up.

The importance of the frontal white matter ingeneration of fast reaction times at the postacutestage, indicated by present results, is in line withthe hypothesis postulated by Posner and Peter-sen (1990) that ascending pathways from struc-tures in the midbrain (i.e., noradrenergic input tocortex from the locus coeruleus) are involved inthe maintenance of an alert state. According toPosner and Petersen, these pathways modulatethe activity in areas within the frontal and pari-etal lobes which are involved in the generationof selective visuospatial attention. These path-ways may run through the frontal lobe, and,therefore, lesions located in the white matterwithin the frontal part of the centrum semiovalemay result in a lowered ability to maintain analert state. Also, the results obtained at the firstassessment suggested that the size of the lesionwas related to the occurrence of defective alert-ness. The early importance of the size of the le-sion may relate to a widespread and diffusemass effect on the attentional systems in thebrain following a significant brain damage. Atthe early stage post stroke, several dysfunctions,such as deranged circulation within the‘‘ischaemic penumbra,’’ intracellular and extra-cellular edema, and ionic and transmitter imbal-

ance, may temporarily interfere with neuronalfunctioning in nearby areas of the lesion(Speach & Dombovy, 1995). For example, brainswelling in a large supratentorial infarct mayinterfere secondarily with neuronal functioningin the upper brainstem, causing impairment ofwakefulness with subsequently lowered mentalefficiency and increased fatigue.

Another potential explanation for a wide-spread effect of brain damage at the early stagepost stroke is a temporary deactivation (diaschi-sis) of neural activity in undamaged areas,which are functionally connected to the dam-aged area (Meyer, Obara, & Muramatsu, 1993,for review). A local brain lesion may damageone part of a network of functionally connectedbrain regions (Mesulam, 1990). Due to themechanisms of diaschisis, undamaged structureswithin such a network may suffer from a tempo-rary deactivation. It is likely that a large lesionwill involve multiple networks and thus willproduce deactivation of a larger extent of theundamaged brain tissue at the acute andpostacute stage. The secondary mass effects onthe brain and behaviour caused by the lesionmay lead to a more marked correlation betweenincreased reaction times and the extent of thelesion, and a less distinct correlation with a localdamage.

The observation that the patients with a per-sistent lengthening of the reaction times 6 to 7months post stroke showed large lesions extend-ing deep into the paraventricular white matter inthe temporal and temporo-parietal area of thebrain, is in accordance with the fact that subcor-tical structures such as the thalamic reticularnucleus, the thalamic intralaminar nuclei, andthe pathways connecting these structures withcenters in the posterior association cortex, havebeen regarded as critical in the generation ofalertness and arousal (for a comprehensive re-view see Butter, 1987 or Watson, Valenstein, &Heilman, 1981). These thalamo-cortical andcortico-thalamic connections will probably suf-fer from severe damage following a lesion in-volving a large extent of the paraventricularwhite matter in the temporal and temporo-pari-etal area, and thus may result in persistent low-ered alertness. Furthermore, several investiga-

Dow

nloa

ded

by [

Uni

vers

ity O

f M

aryl

and]

at 0

5:13

15

Oct

ober

201

4

86 HANS SAMUELSSON ET AL.

tors have suggested that the right hemisphere isspecialized for mediation of alertness and spatialattention (Heilman et al., 1978; Heilman & VanDen Abell, 1980; Weintraub & Mesulam, 1987).If so, the damage to the system for generation ofarousal described above may lead to persistentand more severe attentional defects when thelesion is located in the right hemisphere.

Patients with large lesions mainly involvingcortical and subcortical structures within theterritory of arteria cerebri media but with spar-ing of the deep white matter in the temporallobe, showed a favorable recovery from the slowreactions. The sparing of the white matter in thetemporal lobe may have facilitated a re-estab-lishment of some of the neural functions in theanatomical systems for generation of alertnessand arousal described by Butter (1987) and Wat-son et al. (1981).

To our knowledge, no group studies havebeen conducted on the anatomical correlates ofimpaired simple reaction times at the late‘‘chronic’’ state following a right hemispherestroke. On the other hand, several studies havebeen conducted on this relationship at the acuteand postacute stage following hemispheric braindamage. In these studies, some authors failed toestablish a relationship between the location ofthe lesion and the reaction time (Anzola &Vignolo, 1992), and others reported a significantassociation between slow reactions and damageto the right posterior parietal lobe and to thebasal ganglia (Howes & Boller, 1975), or to theright frontal lobe (Tartaglione, Oneto, Manzino,& Favale, 1987). A positive relationship be-tween the slow reactions and the size of the le-sion within the right hemisphere was reported byTartaglione et al. (1987), although other authorsfailed to demonstrate such a relationship (Anzo-la & Vignolo, 1992; Howes & Boller, 1975).

In conclusion, the present findings lendstrong support to the notion that generalattentional defects may constitute an importantcomponent behind the neglect phenomena(Karnath, 1988), and that in patients with ne-glect, persistent defects of alertness may hamperthe capacity to recover from neglect (Robertson,1993). Also, it lends support to the statements ofRobertson et al. (1995), and Diller and Riley

(1993), that the rehabilitation of patients suffer-ing from neglect should not only focus on theasymmetric defects in the orientation of atten-tion, but also emphasize the importance of gen-erating strategies to rehabilitate the generalattentional defects from which these patientssuffer.

REFERENCES

Aitken, R.C.B. (1969). Measurement of feelings usingvisual analogue scales.Proceedings of the RoyalSociety of Medicine, 62, 989-993.

Anzola, G.P., & Vignolo, L.A. (1992). Simple reac-tion time to lateralized visual stimuli is not relatedto the hemispheric side of lesion.Cortex, 28, 401-409.

Butter, C.M. (1987). Varieties of attention and distur-bances of attention: A neuropsychological analy-sis. In M. Jeannerod (Ed.),Neurophysiological andneuropsychological aspects of spatial neglect, ad-vances in psychology(pp. 1-23). Amsterdam:Elsevier Science.

Christensen, A.L. (1975).Luria’s neuropsychologicalinvestigation. Copenhagen, Denmark: Munks-gaard.

Coslett, H.B., Bowers, D., & Heilman, K.M. (1987).Reduction in cerebral activation after right hemi-sphere stroke.Neurology, 37,957-962.

Dick, J.P.R., Guiloff, R.J., Stewart, A., Bielawska, C.,Paul, E.A., & Marsden, C.D. (1984). Mini-mentalstate examination in neurological patients.Journalof Neurology, Neurosurgery, and Psychiatry, 47,496-499.

Diller, L., & Riley, E. (1993). The behavioural man-agement of neglect. In I.H. Robertson & J.C. Mar-shall (Eds.),Unilateral neglect: Clinical and ex-perimental studies. Brain damage, behaviour &cognition series(pp. 293-308). Hillsdale, NJ: Law-rence Erlbaum.

Feinberg, T.E., Haber, L.D., & Stacy, C.B. (1990).Ipsilateral extinction in the hemineglect syndrome.Archives of Neurology, 47, 802-804.

Folstein, M.F., Folstein, S.E., & McHugh, P.R.(1975). ‘‘Mini-Mental State’’. A practical methodfor grading the cognitive state of patients for theclinician. Journal of Psychiatric Research, 12,189-198.

Friedman, P.J. (1992). The Star Cancellation Test inacute stroke.Clinical Rehabilitation, 6, 23-30.

Gainotti, G., Giustolisi, L., & Nocentini, U. (1990).Contralateral and ipsilateral disorders of visualattention in patients with unilateral brain damage.Journal of Neurology, Neurosurgery, and Psychia-try, 53, 422-426.

Dow

nloa

ded

by [

Uni

vers

ity O

f M

aryl

and]

at 0

5:13

15

Oct

ober

201

4

ATTENTIONAL DEFICITS IN SPATIAL NEGLECT 87

Heilman, K.M. (1979). Neglect and related disorders.In K.M. Heilman & E. Valenstein (Eds.),Clinicalneuropsychology(pp. 268-307). New York: OxfordUniversity Press.

Heilman, K.M., Schwartz, H.D., & Watson, R.T.(1978). Hypoarousal in patients with the neglectsyndrome and emotional indifference.Neurology,28, 229-232.

Heilman, K.M., & Valenstein, E. (1979). Mechanismsunderlying hemispatial neglect.Annals of Neurol-ogy, 5, 166-170.

Heilman, K.M., & Van Den Abell, T. (1979). Righthemispheric dominance for mediating cerebral ac-tivation.Neuropsychologia, 17, 315-321.

Heilman, K.M., & Van Den Abell, T. (1980). Righthemisphere dominance for attention: The mecha-nism underlying hemispheric asymmetries of inat-tention (neglect).Neurology, 30, 327-330.

Hjaltason, H., Tegner, R., Tham, K., Levander, M., &Ericson, K. (1996). Sustained attention and aware-ness of disability in chronic neglect.Neuropsycho-logia, 34, 1229-1233.

Hosmer, D.S., & Lemeshow, S. (1989).Applied logis-tic regression. New York: John Wiley.

Howes, D., & Boller, F. (1975). Simple reaction time:Evidence for focal impairment from lesions of theright hemisphere.Brain, 98, 317-332.

Kaplan, R.F., Verfaellie, M., Meadows, M.E., Caplan,L.R., Pessin, M.S., & DeWitt, L.D. (1991). Chang-ing attentional demands in left hemisphere neglect.Archives of Neurology, 48, 1263-1266.

Karnath, H.O. (1988). Deficits of attention in acuteand recovered visual hemi-neglect.Neuropsycho-logia, 26, 27-43.

Kinsbourne, M. (1970). A model for the mechanismof unilateral neglect of space.Transactions of theAmerican Neurological Association, 95, 143-145.

Kretschmann, H.-J., & Weinrich, W. (1986).Neuro-anatomy and cranial computed tomography.Stuttgart, Germany: Georg Thieme Verlag.

Ladavas, E., Pesce, M.D., & Provinciali, L. (1989).Unilateral attention deficits and hemispheric asym-metries in the control of visual attention.Neuro-psychologia, 27, 353-366.

Lezak, M.D. (1983).Neuropsychological assessment(2nd ed.). New York: Oxford University Press.

Luria, A.R. (1966).Higher cortical functions in man.New York: Basic Books.

Mesulam, M.-M. (1985). Attention, confusionalstates, and neglect. In M.-M. Mesulam (Ed.),Prin-ciples of behavioral neurology(pp. 125-168). Phil-adelphia: F.A. Davis.

Mesulam, M.-M. (1990). Large-scale neurocognitivenetworks and distributed processing for attention,language, and memory.Annals of Neurology, 28,597-613.

Meyer, J.S., Obara, K., & Muramatsu, K. (1993). Di-aschisis.Neurological Research, 15, 362-366.

Posner, M.I. (1975). The psychobiology of attention.In M.S. Gazzaniga & C. Blakemore (Eds.),Hand-book of psychobiology(pp. 441-480). New York:Academic Press.

Posner, M.I. (1986).Chronometric explorations ofmind. New York: Oxford University Press.

Posner, M.I., & Petersen, S.E. (1990). The attentionsystem of the human brain.Annual Reviews ofNeuroscience, 13, 25-42.

Posner, M.I., Walker, J.A., Friedrich, F.J., & Rafal,R.D. (1984). Effects of parietal injury on covertorienting of attention.The Journal of Neuroscien-ce, 4, 1863-1874.

Rapcsak, S.Z., Verfaellie, M., Fleet, W.S., & Heil-man, K.M. (1989). Selective attention in hemi-spatial neglect.Archives of Neurology, 46, 178-182.

Robbins, T.W. (1997). Arousal systems and atten-tional processes.Biological Psychology, 45, 57-71.

Robertson, I. (1989). Anomalies in the laterality ofomissions in unilateral left visual neglect: Implica-tions for an attentional theory of neglect.Neuro-psychologia, 27, 157-165.

Robertson, I.H. (1990). Digit span and visual neglect:A puzzling relationship.Neuropsychologia, 28,217-222.

Robertson, I.H. (1993). The relationship betweenlateralised and non-lateralised attentional deficitsin unilateral neglect. In I.H. Robertson & J.C. Mar-shall (Eds.),Unilateral neglect: Clinical and ex-perimental studies. Brain damage, behaviour &cognition series(pp. 257-275). Hillsdale, NJ: Law-rence Erlbaum.

Robertson, I., & Frasca, R. (1992). Attentional loadand visual neglect.International Journal of Neuro-science, 62, 45-56.

Robertson, I.H., Tegner, R., Tham, K., Lo, A., &Nimmo-Smith, I. (1995). Sustained attention train-ing for unilateral neglect: Theoretical and rehabili-tation implications.Journal of Clinical and Experi-mental Neuropsychology, 17, 416-430.

Samuelsson, H., Hjelmquist, E., Naver, H., &Blomstrand, C. (1996). Visuospatial neglect and anipsilesional bias during the start of performance inconventional tests of neglect.The Clinical Neuro-psychologist, 10, 15-24.

Samuelsson, H., Jensen, C., Ekholm, S., Naver, H., &Blomstrand, C. (1997). Anatomical and neurologi-cal correlates of acute and chronic visuospatial ne-glect following right hemisphere stroke.Cortex,33,271-285.

Siegel, S., & Castellan, N.J. (1988).Nonparametricstatistics for the behavioral sciences. New York:McGraw-Hill.

Speach, D.P., & Dombovy, M.L. (1995). Recoveryfrom stroke: Rehabilitation. In V. Hachinski (Ed.),Bailliere’s clinical neurology: Cerebrovasculardisease(pp. 317-338). London: Bailliere Tindall.

Dow

nloa

ded

by [

Uni

vers

ity O

f M

aryl

and]

at 0

5:13

15

Oct

ober

201

4

88 HANS SAMUELSSON ET AL.

Sturm, W. (1996). Evaluation in therapeutical con-texts: Attentional and neglect disorders.EuropeanReview of Applied Psychology, 46, 207-214.

Tartaglione, A., Oneto, A., Manzino, M., & Favale, E.(1987). Further evidence for focal effect of righthemisphere damage on simple reaction time.Cor-tex, 23, 285-292.

Van Zomeren, A.H., & Brouwer, W.H. (1992). As-sessment of attention. In J.R. Crawford, D.M.Parker, & W.W. McKinlay (Eds.),A handbook ofneuropsychological assessment(pp. 241-266).Hillsdale, NJ: Lawrence Erlbaum.

Van Zomeren, A.H., & Brouwer, W.H. (1994).Clini-cal neuropsychology of attention. New York: Ox-ford University Press.

Watson, R.T., Andriola, M., & Heilman, K.M. (1977).The EEG in neglect.Journal of Neurological Sci-ence, 34, 343-348.

Watson, R.T., Valenstein, E., & Heilman, K.M.(1981). Thalamic neglect. Possible role of the me-dial thalamus and nucleus reticularis in behavior.Archives of Neurology, 38, 501-506.

Wechsler, D. (1944).The measurement of adult intel-ligence. Baltimore, MD: Williams & Wilkins.

Weintraub, S., & Mesulam, M.-M. (1987). Right cere-bral dominance in spatial attention.Archives ofNeurology, 44, 621-625.

Wilson, B., Cockburn, J., & Halligan, P. (1987).Behavioural inattention test; Manual. Fareham,UK: Thames Valley Test Company.

Dow

nloa

ded

by [

Uni

vers

ity O

f M

aryl

and]

at 0

5:13

15

Oct

ober

201

4