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The complexity of the relationship betweenneuropsychological deficits and impairment in everydaytasks after stroke kiewicz1, Marie-Luise Brandi1,2, Charmayne Hughes1, Anna Voitl1 &Marta M. N. Bien rfer1Joachim Hermsdo t Mu nchen, Mu nchen, GermanyDepartment of Sport and Health Sciences, Institute of Human Movement Science, Technische Universita nchen, Planegg-Martinsried, GermanyGraduate School of Systemic Neurosciences, Ludwig-Maximilians-Universit at Mu12KeywordsAction disorganization syndrome, activities ofdaily living, apraxia, neuropsychologicaldeficits, strokeCorrespondence kiewicz, Lehrstuhl fu rMarta M. N. BienBewegungswissenschaft, Technische nchen, Georg-Brauchle-RingUniversit at Mu nchen, Germany. Tel: 49 89 28960-62, Mu24551; Fax: 49 89 289 24553; E-mail:mbienia@gmail.comFunding InformationThis work was funded by the EU STREPProject CogWatch (FP7-ICT-288912).Received: 11 May 2015; Revised: 17 June2015; Accepted: 19 July 2015Brain and Behavior, 2015; 0(0), e00371,doi: 10.1002/brb3.371AbstractBackground and purpose: A large body of research reports that stroke patientsare debilitated in terms of daily independence after dismissal from the hospitalunit. Patients struggle with the use of daily objects or performing complexactions. Differences between individual deficits of patients are often associatedwith the site of the brain damage. However, clinical studies suggest that patientsexhibit varied constellations of action-associated difficulties and neuropsychological deficits. There is a lack of conclusive evidence indicating how differentneuropsychological symptoms link to the impaired ability to perform activitiesof daily living (ADL). Materials and methods: To further address this matter,in this study we compared the behavior of patients with left brain damage(LBD) and right brain damage (RBD) following stroke in two naturalistic taskscenarios (tea making and document filing), and compared the committedaction errors to the neuropsychological screening results. Results: We observedmild to severe impairments in both the LBD and RBD groups amounting to37–55% of failure rate in attainment of action goal. Interestingly, the performance on both tasks was not correlated to each other, suggesting that the tasksinvolved a different set of higher cognitive functions. Despite similar behavioralmanifestations, in the LBD group poor task performance was related to deficitsin praxis performance and unilateral tactile and visual extinction. The presenceof aphasia did not correlate with task performance, except for a link betweenlow scores in Aachen aphasia test scales and misestimation error in the teamaking task. In the RBD group, difficulties with performance were primarilylinked to deficit in praxis and unilateral visual extinction. Conclusions: Despitesimilar behavior, the underlying mechanisms of the deficits after stroke mightbe different (in patients with LBD and RBD) and reveal complex interlinks ofcognitive networks involved in the ability to carry on everyday tasks.IntroductionApraxia and action disorganization syndrome (AADS)affects a significant amount of patients in the postacutephase of stroke. According to the widely accepted definition, apraxia (Rothi and Heilman 1997) is treated asimpairment in tool use, gesturing, and imitation that isindependent from sensory and motor impairments ofstroke. Usually apraxic behavior is associated with leftbrain damage (LBD) following a stroke and varies inclinical manifestations. Action disorganization syndromeis by some researchers differentiated from apraxia as aresultant of right brain damage (RBD) or frontal lobedamage (Humphreys and Forde 1998), and in the simplest description means impairment of the ability to organize multistep actions in a chain of subtasks. For thepurpose of this article, we will not disambiguate thosetwo syndromes, but assume that AADS is an umbrellaterm for behavioral manifestations of the inability toperform tool-oriented, meaningless, and communicativegestures. Patients can suffer from difficulties with actualobject use as well as the use of nonverbal communicationª 2015 The Authors. Brain and Behavior published by Wiley Periodicals, Inc.Brain and Behavior, doi: 10.1002/brb3.371 (1 of 14)This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium,provided the original work is properly cited.
kiewicz et al.M. M. N. BienNeuropsychological Correlates of Apraxiaand pantomime (Goldenberg 2013). Pantomime performance (i.e., demonstrating tool use without holding theobject) is regarded as one of the core features of apraxicdifficulties (among impaired tool use and imitation ofmeaningless gestures). Although pantomime does notinclude every feature of the movement sequence thatwould occur during the actual manipulation of the object,it is believed to reflect the core features of “simulated”use (Buxbaum et al. 2014). According to cognitive conceptualizations of apraxia, if the access to, or the conceptof use, is impaired then patients will not be able todemonstrate how they would use an object. Hermsd orferet al. (2012) used a “scooping” motion task, and demonstrated that pantomime performance may translate intothe actual tool use. However, the relationship between theactual tool use, performance in naturalistic scenarios, andpantomime can vary between patients following stroke(Buxbaum et al. 2000; Bickerton et al. 2012). As proposedby Bienkiewicz et al. (2014), we grouped difficulties withmotor performance in naturalistic task scenarios intothree categories of deficits—sequencing, concepts of useincluding gesture knowledge, and spatiotemporal features.This taxonomy partially overlaps with the categorizationof apraxic pantomime and imitation errors proposed byHoeren et al. (2014), namely content and movementerrors. In comparison, Hartmann et al. (2005) did notuse an error classification in their study, but a percentagescoring for the naturalistic task performance. In the paperof Buxbaum (1998) overall error scoring was used withratio of error types. Many authors distinguish more errorcategories that provide more detailed description of theAADS difficulties (for review see Goldenberg 2013,Chapter 9).Despite the plethora of research describing the differentdifficulties that patients have when performing activities ofdaily living (ADL)-like tasks (Buxbaum 1998; Humphreysand Forde 1998; Schwartz et al. 1999; Sunderland et al.2006; Bickerton et al. 2007, 2012), there is no clarityregarding the link between the deficits that patients exhibitand other neuropsychological syndromes that can occur asa consequence of stroke. According to Katz et al. (1999),around 30% of ischemic stroke survivors suffer fromcomorbid to motor impairment signs of stroke. Depending on the hemisphere and the location within the damaged hemisphere, the patient can suffer from motordisability, impairment of language production and comprehension (aphasia), cognitive decline, spatial attentiondifficulties (neglect), and visual deficits (hemianopia).There is conflicting evidence about the links between thosesyndromes and the ability to perform ADL-oriented tasks.For example, in patients with RBD it was demonstratedthat visuospatial deficits are related to the outcome ofrehabilitation in the posthospitalization phase (DenesBrain and Behavior, doi: 10.1002/brb3.371 (2 of 14)et al. 1982; Jehkonen et al. 2006; Walker et al. 2012).Wade and Hewer (1987) added that hemianopia is a secondary important predictor for the functional outcome.Jehkonen et al. (2000) argued that other symptoms suchas hemiparesis and language deficits were reported to lackpredictive power. In the study of Hartmann et al. (2005),performance of aphasic LBD patients in multistep actionscorrelated with the severity of aphasia for preparing coffee,but not for fixing and starting a tape recorder. In the sametasks, patients with RBD demonstrated difficulty withkeeping track of the multistep action performance andtheir performance correlated with the severity of hemineglect. Likewise, Schwartz et al. (1999) reported that RBDpatients had a variety of action errors correlated with theseverity of their hemineglect, which was not limited to theleft side of the work space. Consistent with the presentedevidence, Katz et al. (1999) argued that rehabilitationstrategies for stroke patients should be oriented on theindividual neuropsychological symptoms in order toincrease independence of daily living. However, the extentto which the neuropsychological syndromes comorbid toAADS play a role in limiting daily functioning remains asubject of debate.In this study, we investigated the relationship betweenaphasia, spatial attention (neglect and extinction), andother neuropsychological symptoms occurring as a consequence of stroke in the context of ADL performance. Onthe basis of previous reports, we expected to find similarextent of ADL deficits in both groups of patients. Wehypothesized AADS impairment can be linked to theseverity of other perceptual and cognitive deficitsobserved in both LBD and RBD stroke survivors. Precisely, we expected that difficulties with ADL-like taskscorrelate with not only gestural praxis but also with aphasia in LBD sample, and with spatial attention in RBDpatients.MethodsParticipantsIn all, 38 LBD patients were included in the analysis alongwith 17 RBD patients. The mean age for the LBD patientgroup was 58 years (SD 12 years) and for the RBDpatient group was 61 years (SD 12 years). The LBDgroup comprised 20 males and 18 females and the RBDgroup comprised nine males and eight females. All participants suffered from a first stroke and were tested withinthe range of 2 weeks poststroke up to 4 months. Allparticipants were patients of the ward of the Departmentof Neuropsychology at the Hospital Bogenhausen Munichor attended the outpatients’ clinic. Recruited patients suffered from typical neuropsychological syndromes follow-ª 2015 The Authors. Brain and Behavior published by Wiley Periodicals, Inc.
kiewicz et al.M. M. N. BienNeuropsychological Correlates of Apraxiaing stroke, such as aphasia, apraxia, neglect, other spatialdeficits, and deficits of attention. Patients with history ofprevious stroke, nonstroke-related neurological problems,psychiatric disorders, substance abuse history, or aninability to understand instructions were excluded fromrecruitment.We tested 12 age-matched control subjects in the teamaking (TM) task. All were neurologically healthy(M 58.1, SD 13.4 years). Six females and six maleswere recruited (10 right-handed, 2 left-handed, all performed the task bimanually). In the document filing (DF)task, we tested 12 age-matched control subjects(M 55.8, SD 15.1 years), including six females, allparticipants were right-handed and performed the taskbimanually. Table 1 shows demographic and clinical dataof the participants. No significant difference was found interms of age between the control and patient groups withone-way analysis of variance, F(3, 75) 0.45, P 0.05.Ethical considerationsThis report is based on the clinical screening for the CogWatch project conducted in the Hospital BogenhausenMunich. The study design was approved by the ethicalcommittee of the Medical Faculty of the TechnicalUniversity of Munich. Informed consent was obtainedfrom all subjects, and the study was conducted in accordance with the Declaration of Helsinki. Participation wasTable 1. Demographic and clinical data.Patient groupGender: female/maleAgeDays since strokeEducation: Vocational/Middle School/AcademicAetiology: Ischemia/Bleeding/BothLocus: MCA/ACA/PCA/ICB/MCA plus/CB/TH/BG/NAPatients with neglectPatients with hemianopiaHemiparesis/plegiaAphasia: No, Amnesic,Anomia, Broca, Global,Non-classificable,TMA, WernickeLBDn 38RBDn 1716/2258.9 (34–89)99.4 (18–269)8/16/148/961 (44–85)127.3 lues in brackets denote range of values.Cortical: MCA, middle cerebral artery; ACA, anterior cerebral artery;PCA, posterior cerebral artery; ICB, intra cerebral haemorrhage; MCAplus, MCA with subarachnoid bleeding or MCA with PCA. Subcortical: CB, cerebellar infarction; TH, thalamus infarction; BG, basal ganglia; NA, unknown; TMA, transcortical motor aphasia.ª 2015 The Authors. Brain and Behavior published by Wiley Periodicals, Inc.voluntary, and patients were informed that they couldwithdraw at any time without giving a specific reason andwithout their treatment at the hospital being affected.ProcedureThe testing procedure comprised scales of a BirminghamCognitive Screen (BCoS) (Humphreys et al. 2012): praxis,spatial, and controlled attention sections; and two naturalistic tasks: tea making and document filing. BCoS sections included were as follows: complex figure copymultistep object use (MOT), gesture production, gesturerecognition, gesture imitation (praxis subscales), appletest (used for the evaluation of spatial attention), andvisual and tactile extinction scales. The BCoS assessmentapproximately takes 30 min and allows for the testing ofaphasic individuals, as the patients are allowed to respondnonverbally. The complex figure copy task, similar to theRey–Osterrieth figure copy test (Meyers and Meyers1995), assesses participants’ ability to copy a complex, butmeaningless rectangular shape comprised many geometrical features. The recent study by Chechlacz et al. (2014)showed that performance on this task involves a numberof complex cognitive processes such as spatial coding,attention, motor execution and planning, and a discretenetwork of neural substrates.The MOT assesses patients’ ability to select adequatecomponents (among distractor items) and assemble (withthe batteries placed in the correct orientation) and switching on a torch. This scale aims to provide an overview ofperformance capacity in everyday like context, and performance in this task is reportedly independent from the performance on praxis scales (Bickerton et al. 2012;Humphreys et al. 2012). Praxis subscales cover cognitiveprocesses that support praxis such as action semantics,coding of body parts, input processing of visual stimuli,and gesture output processing. Gesture production assessesthe ability to produce pantomime to auditory commandfrom the examiner. In gesture recognition tests patientswere asked to recognize communicative gestures and pantomime demonstrated by the examiner (aphasic patientsare given forced choice options), and in gesture imitationpatients are ask to imitate a meaningless gestures. Thepraxis subtests comprised three to six items each. Theapple cancelation test is designed to measure allocentricand egocentric types of neglect (Chechlacz et al. 2012,Bickerton et al. 2011). Driver and Vuilleumier (2001) conceptualized neglect as a bias to favor stimulus on the ipsilateral side and dismiss the stimuli presented in thecontralesional peripersonal space after unilateral braindamage. Participants are presented with a printout in alandscape orientation with 50 whole apples spaced outgeometrically among other distractors (i.e., apples with anBrain and Behavior, doi: 10.1002/brb3.371 (3 of 14)
kiewicz et al.M. M. N. BienNeuropsychological Correlates of Apraxiaopening on either the left or right side). Egocentric neglectis assessed on the basis of the tendency to miss apple targets in the section of the sheet. Allocentric neglect is measured as number of false positive responses (canceledapples with opening on the right or left side). In addition,visual and tactile extinction were included in the assessment to assess difficulty with attending to two competitivestimuli at the same time as an aspect of neglect syndrome.The extinction phenomenon is particularly detrimentalwhen multiple stimuli compete at once for attention, particularly in ADL context (Driver and Vuilleumier 2001). Inthe visual extinction task the examiner sat across from thepatient with the arms lifted on either side of the head (1 maway with the hands approximately 20 cm from the nose).The examiner moved the index finger on the right/lefthand or bilaterally for a brief moment, and the participantwas asked to fixate on examiners nose and point out whichfinger/s was bent. In the tactile part of this assessment, theparticipant was asked to keep the eyes closed and sitstraight on the chair. The examiner used an identical protocol to the visual extinction test and tapped twice on thedorsal surface of the patient’s thigh (left/right/bilaterally).For visual and tactile extinction scales, the extinction indexwas calculated as difference between the right and leftextinction score, and quantified as a difference between thebimanual and unilateral performance (Chechlacz et al.2013).The experimental procedure took an hour to administer, but had to be completed within two sessions for somepatients. In addition, the Aachen aphasia test (Huberet al. 1984) was administered to LBD patients in order toassess their level of language comprehension. This testcomprises assessment of spontaneous speech and comprehension, retention, and written language, and was conducted by a speech therapist of the Hospital BogenhausenMunich in a separate session. For analysis, token test(TT), naming, comprehension, repetition, and writtenlanguage percent rank (PR) scores were included. In addition, presence of hemiparesis, hemianopia, and neglectwas retrieved from the medical records in the hospital.In this study we used two error taxonomies to describethe behavior of patients. First one consisting of moredetailed taxonomy system that classifies types of actionerrors (Table 2). Further, error types were grouped intothree global categories; sequencing errors, conceptualerrors, and spatio-temporal errors (Bienkiewicz et al.2014) in order to examine correlations between the neuropsychological syndromes and the difficulties exhibitedby patients. Sequencing errors included action: addition,anticipation, omission, perplexity and perseveration.Some of the error categories originally classified as ingredient omission or ingredient substitution were classifiedas conceptual errors. In addition, the conceptual errorBrain and Behavior, doi: 10.1002/brb3.371 (4 of 14)Table 2. Error taxonomy used to classify error typesError typeDefinitionsExampleAdditionAdding an extracomponent action thatis not required in theaction sequenceAdding instant coffeeto cup 2AnticipationPerforming an actionearlier than usualTurning the kettle onbefore pouringwater into the kettleExecutionAn error in the executionof the taskDropping thesweetener dispenseronto the tableIngredientomissionFailing to add aningredient required tocomplete the task goalFailing to put sugarinto cup 1MisestimationUsing grossly too muchor too little of somesubstancePouring half of themilk jug contentsinto cup 2MislocationAn action that isappropriate to theobject in hand but isperformed in completelythe wrong placePouring some liquidfrom the bottle ontothe table rather thaninto the glassIngredientsubstitutionAn intended actioncarried out with anunintended ingredientPouring coffeegrounds instead ofsugar into cup 2PerplexityA delay or hesitation inperforming an actionPicking up a tea bagand then pausing foran extended amountof time beforeplacing it into a cupPerseverationThe unintentionalrepetition of a step orsubtaskAdding more thanone tea bag to a cupObjectsubstitutionAn intended actioncarried out with anunintended objectPour heated waterinto non-cup 1objectQualityThe action was carriedout, but not in anappropriate wayPutting the tea bagand the paper labelinto a cupSequencePerforming an actionmuch later than usualSwitch kettle on afterpreparing both cupsof teaSequenceomissionAn action sequence inwhich one step orsubtask is notperformed, despite thelack of any intention toomit the step or subtaskTurning on the kettleon without havinginserted waterError taxonomy was adapted
The complexity of the relationship between neuropsychological deficits and impairment in everyday tasks after stroke Marta M. N. Bienkiewicz1, Marie-Luise Brandi1,2, Charmayne Hughes1, Anna Voitl1 & Joachim Hermsdorfer 1 1Department of Sport and Health Sciences, Institute of Human Movement Scien
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