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Executive dysfunction after stroke – possibilities and limitations of diagnosis

Ernest M. Tyburski
,
Monika Mak
,
Jacek Kurpisz
,
Agnieszka Samochowiec
,
Andrzej Potemkowski

Adv Psychiatry Neurol 2018; 27 (2): 135-145
Data publikacji online: 2018/07/06
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INTRODUCTION

Some of the quite common consequences of cerebral stroke are cognitive disorders, which may include deficits within perception, attention, memory, language and the ability to handle complex tasks [1, 2]. Along with cognitive disturbances, there are reports of premorbid personality changes involving a loss of interests and plans, a change within values or self-esteem or general inability to fulfil social roles [3]. There may also appear certain affective disturbances, i.e. emotional lability, increased anxiety, irritability or impulsivity, inappropriate affect or depressive states [4]. The aforementioned disorders may stem from organic brain damage or constitute a psychological response to the disability [5].
Stroke is characterised by fast and focal development of neurologic symptoms reflecting a loss of brain function due to a sudden loss of blood circulation or an intracranial haemorrhage [6]. Most strokes are ischaemic, constituting approximately 80% of all cases, and about 15% are haemorrhagic [7]. Stroke is one of the most common causes of disability, including disability resulting from neuropsychological disorders. Approximately 70% of stroke patients require third party care [8]. In this patient group, it is of major importance to make an immediate and accurate diagnosis of the disability and implement effective therapeutic methods. Complex neuropsychological consequences of a stroke call for such an individualised approach, involving planned and intentional interventions of both the caregivers and professionals, and thus improving the quality and effects of patients’ return to functional autonomy. With regard to the diagnostic process, it is especially important to discuss the executive dysfunction in patients with post-stroke symptoms as well as possibilities and limitations of their diagnosis.

CHARACTERISTICS OF EXECUTIVE FUNCTIONS

The notion of executive functions has become one of the fundamental concepts in modern neuroscience [9]. Based on clinical observations and scientific research, it has been concluded that the frontal lobes are particularly involved in the regulation of complex human behaviours [10]. Theoretical background of executive functions is associated with research conducted by Luria [11]. In his model of the human brain, he distinguishes three functional systems: (a) a unit for arousal and attention (limbic and reticular activation system); (b) a unit for receiving, analysing and storing information (posterior neocortex); and (c) a unit for planning, organising and regulating behaviour and cognition (frontal lobes). This concept defines regulation as the ability to alter an operation during the performance of a particular task, which often occurs with the participation of language processes [12]. Control, in turn, is understood as the ability to compare the effects of an action to the original intent. Solving a problem requires an analysis of initial conditions, development of a specific plan (strategy), implementation of relevant operations and, finally, a comparison of the result to the input data [13]. Clinical neuropsychology promotes Lezak’s approach [14], according to which executive functions form a system that allows successful completion of a purposeful action. These functions comprise four processes: (a) volition; (b) planning; (c) purposive action; and (d) effective performance. Proper performance of each of them depends on the completion of the previous one. Currently, executive functions are understood as mental abilities responsible for, among others, the following: (1) anticipation and focus of attention; (2) self-monitoring and impulse control; (3) initiation of activity; (4) working memory; (5) mental flexibility and the ability to make use of feedback; (6) planning and organisation; and (7) the choice of effective problem-solving strategies [15]. They also form a central executive system that allocates cognitive resources, monitors, controls and inhibits other cognitive processes and behavioural responses, thus contributing to a better adaptation to the environment [16]. They enable modification of initiated actions and customisation of responses, depending on the changing situational context [9]. Cognitive and behavioural control are believed to be particularly significant executive domains [17, 18]. Complex nature of executive function was also demonstrated in research on healthy individuals, involving factor analyses of various measures of executive performance. For example, based on the factor analysis of 19 neuropsychological tests in 200 healthy people, Testa, Bennett and Ponsford [19] distinguished 6 relatively independent factors: prospective working memory, setshifting and interference management, task analysis, response inhibition, strategy generation and regulation, self-monitoring and set-maintenance. In turn, Miyake et al. [20] distinguish three main executive domains (shifting, updating, and inhibition), suggesting their relative independence but also certain common characteristics.
A part of stroke patients experience typical executive dysfunction symptoms, such as ineffective performance despite sufficient knowledge about a task [21]. Some other symptoms of executive deficits include: hypersensitivity to external stimuli, perseverations, rigidity of thought, difficulty in planning and anticipating consequences of actions, adynamia or disinhibition. Some patients constantly make mistakes carrying out particular tasks, even when they detect and verbalise the principle behind it. Such difficulties are a manifestation of the dissociation between thinking and action [22]. The prevalence of executive dysfunction after stroke ranges from 18.5% to 39%, depending on definitions and instruments used for its evaluation [23, 24]. Executive dysfunction after stroke is often associated with the location of the damage.

EXECUTIVE DYSFUNCTION AND LOCATION OF STROKE

To date, there have been a number of reports on various specific executive symptoms resulting from lesions to different brain areas in stroke patients [22]. Assessment of such disorders is no easy task, considering the complexity of cerebral vascularisation and disassociation in severity of different deficits. Depending on lesion location, i.e. whether stroke was located in the frontal (anterior vascularisation), rear (posterior vascularisation) or subcortical portions of the brain (various blood vessels), patients were normally divided into frontal – non-frontal – subcortical groups and thus compared in their performance of neuropsychological tests [25]. Studies regarding executive dysfunction, depending on location of pathology in the brain, were selected from PubMed, PsychINFO and Google Scholar databases. As shown in Table 1, their results are inconsistent.
Some studies demonstrate larger executive dysfunction, involving impairment in critical thinking and planning [26, 27], verbal working memory and verbal mental flexibility [27, 30], cognitive and motor inhibition [28, 30] and non-verbal mental flexibility [30], in patients with stroke located in the frontal rather than the rear areas of the brain. Other reports, however, do not confirm such findings, indicating no difference between the groups in terms of cognitive inhibition, verbal and non-verbal mental flexibility, critical thinking, verbal working memory and planning [27, 29, 31, 32, 34]. In addition, Pohjasvaara et al. [35] and Zinn et al. [36] reported greater executive dysfunction, manifested in basic and complex activities of daily living, in patients with stroke located in the frontal areas of the brain.
Research analyses also indicate that patients with lesions located in the frontal lobes compared to those with pathology in the subcortical structures struggle with similar executive difficulties within e.g. cognitive and motor inhibition [28], critical thinking, verbal and non-verbal mental flexibility [30, 34].
In turn, patients with pathology in the rear areas of the brain compared with patients with lesions located in subcortical structures are characterised by smaller deficits in executive functioning [28, 30].
Furthermore, there is evidence of executive dysfunction in patients with stroke located in the basal ganglia, in terms of verbal working memory and critical thinking [37] and in the insula in terms of non-verbal mental flexibility [38].
Relevant data was also provided by Vataja et al. [39], who demonstrated that stroke patients with executive deficits compared to those without them (with scores below 1.5 SD compared to the controls in SCWT, TMT, WCST) were characterised by brain lesions located in different brain areas: frontal, rear and subcortical. In addition, certain executive dysfunctions in various processes, i.e. cognitive inhibition, visual set shifting, nonverbal mental flexibility, were demonstrated in patients with stroke only in the subcortical brain structures [40–42].

THE DYSEXECUTIVE SYNDROME AND THE FRONTAL LOBE SYNDROME

Various executive function deficits and their characteristics are currently a subject that is widely discussed in neuropsychology. Many researchers and practitioners highlight the complicated nature of executive dysfunction and postulate the need to establish a typology of its different subunits [43]. Among the first ones to introduce the concept of the dysexecutive syndrome to the world literature were Baddeley and Wilson [44]. In their scientific and clinical activity, they wanted to change and replace the diagnostic unit known as the frontal lobe syndrome [45], especially since the previous approach assuming frontal lobe pathology to be a necessary and sufficient condition to trigger executive dysfunction proved to be outdated in light of later research. The last three decades have provided empirical evidence that malfunctioning brain structures outside of the frontal lobes may induce various executive symptoms, and, on the other hand, that frontal lobe damage does not always lead to such dysfunction [46]. In addition, many patients with different neurological and mental health problems exhibit considerable variation in terms of symptoms known as the dysexecutive syndrome [47]. Presented below are descriptions of both syndromes to indicate some of the most important differences between them.
Frontal lobe syndrome is a psychiatric diagnostic unit characterised by a number of changes within personality and emotional function [48]. A classic example of a patient with the frontal lobe syndrome is the case of Phineas Gage, who manifested all sorts of behavioural and emotional changes [49]. From the neurological point of view, a patient with the frontal lobe syndrome is a patient with symptoms in the form of jocular attitude or aboulia, lack of criticism and concurrent neurological symptoms [49, 50]. There are three main types of frontal lobe syndromes, depending on the location of the damage. The first one is the orbitofrontal syndrome, characterised by impulsive behaviour, disinhibition, lack of insight, irritability and emotional lability. The second one is the medial frontal syndrome, marked by apathy, loss of interest, lack of motivation, initiative or drive and self-negligence. The third one is the frontal convexity syndrome, which includes impairment within memory, abstract thinking and mental set changes, lack of problem-solving strategies, and depression [51].
In contrast, dysexecutive syndrome involves a wide variety of different executive disturbances due not only to lesions to the frontal areas but also other brain regions, such as parietal lobes, anterior cingulate cortex, subcortical structures (e.g. the thalamus or striatum) and the cerebellum [52]. Therefore, it seems incorrect to use the term “frontal lobe syndrome,” as current state of knowledge concerning other brain areas suggests that their damage may result in a similar clinical picture.

SELECTED COMPONENTS OF THE DYSEXECUTIVE SYNDROME

The dysexecutive syndrome has been suggested to include a variety of symptoms, which often dissociate, with some processes being impaired, and others remaining intact [53]. The syndrome is thus of a heterogeneous nature. Depending on the theoretical concept, there are several classifications of executive dysfunction. Presented below are four selected models of dysexecutive syndromes.
One of the more interesting models, proposed by Godefroy and Stuss involves distinguishing of two subunits [54]: the behavioural dysexecutive syndrome and the cognitive dysexecutive syndrome. The former includes the following: (a) limited activity (apathy and aspontaneity) or general agitation (disinhibition and impulsivity); (b) stereotyped behaviour and perseverations; (c) excessive environmental dependency (e.g. utilisation behaviour – performance of motor activity associated with the correct function of the object despite the absence of explicit instructions). Other reported symptoms are difficulties in social behaviour, anosognosia or inappropriate sexual behaviour. In turn, the cognitive type includes as follows: (a) problems within initiation and inhibition of actions and reduced focus of attention; (b) difficulty in maintaining and shifting of mental sets; (c) planning and problem-solving deficits; and (d) impaired information generation. Associated deficits may be problems within working memory and the ability to rapidly refresh information, impaired learning strategies and deficits within the so-called social intelligence (the ability to predict human behaviour based on the analysis of their thoughts, beliefs and intentions).
A similar model, involving a distinction into two subunits, was developed by Jodzio [55]. The first subunit includes a dominant planning disorder and includes the following: (a) difficulty within the choice of purposeful actions; (b) planning deficits; (c) mental set perseverations; (d) mental set rigidity; (e) obsessiveness and rigidity of thought; and (f) adynamia. The other one is characterised by dominant control deficits and involves as follows: (a) difficulty in action initiation; (b) control deficits; (c) perseverations; (d) mental set instability; (e) compulsivity and impulsivity of actions; and (f) disinhibition. According to Jodzio, those symptoms do not form a complete list of all executive deficits. Manifestations of the disorder can be observed on a continuum from the cognitive (mental) to the behavioural symptoms (action).
The third classification is one by Ardila [56]. He distinguishes the metacognitive and the motivational/emotional executive dysfunction syndromes. The former manifests itself through the following: (a) inability to create task performance strategies; (b) difficulties in complex problem solving; (c) difficulties in consequence anticipation; (d) perseverations and (e) deficits within temporal organisation. The latter one entails: (a) deficits within cognitive and emotional control; (b) difficulty within basic impulse inhibition; (c) inappropriate social behaviour; (d) disregard of important events and inability to respond to social cues; and (e) personality changes.
Due to depression being a common comorbidity of executive deficits in stroke patients suffering damage to frontostriatal and limbic pathways, Baune et al. [57] proposed the so-called depression-executive dysfunction syndrome. Their model is characterised by disturbances in sequencing, organising, planning, abstracting, reduced interest in activities, and psychomotor retardation but less pronounced vegetative symptoms than those reported in depressed elderly patients without significant executive dysfunction [4].
Both clinical observations and research findings [58] support the aforementioned classification systems. All four of them take into account cognitive and behavioural aspects of executive function. The last two consider also emotional deficits. A summary of the described dysexecutive syndromes is presented in Table 2. All presented models comprise similar theoretical approaches to particular aspects of executive dysfunction observed in stroke patients.

DIAGNOSTICS OF EXECUTIVE DYSFUNCTION

Diagnosis of executive function disorders is a complex process that may be a challenge both in the theoretical and technical contexts [58]. Diagnostic difficulties may arise not only because of the different etiopathogenetic circumstances and complex clinical characteristics of executive dysfunction, but also because of the need to take into account the age of patients. It has been empirically confirmed that the natural aging process leads to the shrinking of neurons, especially within the frontal lobes, which translates into weaker performance in tests measuring executive functions [59–61]. The profile of cognitive deficits in post-stroke patients depends on the location of vascular lesions and they may manifest themselves in the form of cortical, subcortical, or mixed symptoms [62].
Description of the deficit profile in the dysexecutive syndrome requires a wider perspective, extending beyond the classification of symptoms into the cortical and subcortical ones. In addition, executive disorders do not often constitute an isolated symptom (although they may dominate the clinical picture), but rather co-occur with other cognitive deficits (impaired attention, memory, language, and visual-spatial functions).
Studies on post-stroke patients often report their scores in the Mini-Mental State Examination (MMSE), but this test is insensitive to executive dysfunction and does not capture more subtle cognitive deficits [63]. Due to this very fact, a better tool facilitating the process of screening for executive dysfunction in stroke patients is the Birmingham Cognitive Screen (BCoS) [64]. This battery assesses five cognitive domains: (a) attention and executive function; (b) language; (c) memory; (d) number skills; and (e) praxis.
The most common standard tests used to measure executive functions are the following: the Wisconsin Card Sorting Test, the Tower of London, the Stroop Colour Word Test, the Trail Making Test, and Verbal Fluency Test, or the Go No Go Task [2, 22]. A short description of those tools is presented in Table 3. Quantitative results obtained from the use of those methods can, however, provide a false clinical picture, because their design often deviates from the real life problems patients may not be able to cope with [70]. Therefore, there is now a tendency to create tools resembling everyday life challenges, i.e. ones of greater ecological accuracy. Among these, the most popular ones are: the Six Elements Test, the Multiple Errands Test, and the Executive Function Performance Test. Their descriptions can be found in Table 4. They are based on tasks measuring different types of executive function, including planning, thinking and acting strategies, and do not often require general knowledge but rather spontaneity and thinking flexibility [74]. Research tools based on virtual reality are also a new diagnostic method. Development of virtual methods was based on a different methodological approach than paper-pen or computer assisted tests, one of the fundamental concepts associated with the use of virtual reality in neuropsychology is immersion, i.e. the ability of computer-generated environment to elicit a feeling of presence in virtual reality [75, 76]. The tool that is most commonly used in working with patients is the so-called head-mounted display (HMD), which allows the projection of three-dimensional (3D) graphics. Through tracking head movement, the tool allows its users to naturally interact with electronic environment [77]. This means that they can navigate, see from different perspectives, and manipulate its contents [78]. Virtual tests are currently used in experimental studies to evaluate neuropsychological deficits including executive dysfunction in patients after stroke, but they may soon become useful in clinical practice [79–81].
In the literature, different rules appear to facilitate the selection of a specific diagnostic approach, such as: (a) time requirements, i.e. using as many methods to collect as much data on the executive functions within a specified time; (b) the test selection factors, understood as ways of administration, cost, accuracy or range of clinical applications; (c) the use of diagnostic hypotheses formulated on the basis of the collected qualitative and quantitative data from the medical history, the results of previous assessments, observation and interview; and (d) theoretical foundations of the research procedures, i.e. selection of methods in accordance with the chosen theoretical approach [82].
Either a functional or ecological approach to neuropsychological diagnostics of executive dysfunction in stroke patients seems a more accurate choice than functional localisation or differential diagnosis [55]. This is due to limitations of localisation diagnosis, according to which a function is linked to a specific area of the brain. To that end, tools designed to measure executive performance are not limited to investigating only the functions of the frontal lobes [83]. On the other hand, due to the heterogeneous nature of executive functions, and the fact that various degrees of executive dysfunction are observed in patients with different medical conditions, it seems insufficient to use methods of differential diagnosis, the aim of which would be to describe a single set of symptoms. Functional diagnosis has the greatest potential to fully describe the functioning of human mental processes, both the impaired and the preserved ones. Functional psychological assessment is therefore a more accurate approach, as it enables implementation of more effective therapy or neuropsychological rehabilitation.
Apart from quantitative data, proper diagnostics of executive dysfunction requires also qualitative description of patients’ performance and errors. Some practitioners and researchers suggest that the best way to draw conclusions concerning executive function is to create a general patient profile based on all test scores as well as interview and observation data [84]. In stroke patients, who often have limited mobility, the administration of standard psychometric methods can be much more difficult or even impossible. Therefore, it is often suggested to apply simple clinical/experimental techniques based on the Lurian [83] approach (e.g. simple finger opposition task, Fist-Edge-Palm Test, and the Reciprocal Motor Programme Test) to obtain qualitative data on mental function disorders. In addition, good diagnosis of executive dysfunction involves more general questions concerning future plans or their implementation [55].

INTERVENTIONS FOR EXECUTIVE DYSFUNCTION AFTER STROKE

Even though early spontaneous improvement within certain neuropsychological domains (especially up to six months) after stroke may occur in a substantial proportion of patients [85], executive deficits are known to persist over time [86]. Those lead to functional dependency [35], limit patients’ ability to return to work [87] and affect their social functioning [88]. Executive functions are, therefore, of great concern to clinicians and researchers involved in cognitive rehabilitation following a stroke. In line with the latest guidelines, neuropsychological rehabilitation should be based on research using standardised therapeutic methods, the application of which is aimed at functional improvement in significant life domains [89]. Different therapeutic approaches are suggested [90]. Some are oriented toward targeted remediation of specific executive processes, e.g. through computer-based training (Cogmed QM, AixTent or RehaCom) [91–93]. Others focus on teaching patients to use their residual skills more efficiently or to compensate for their difficulties through the use of various strategies, such as cognitive strategies to improve problem solving. External compensatory mechanisms, such as electronic paging systems or environmental modifications are also used in an attempt to improve accomplishment of daily activities. Two recent systematic reviews demonstrated that stroke patients may possibly benefit from specific executive function training and learn compensatory strategies to reduce the consequences of executive impairment. Poulin et al. [24] describe 10 studies confirming effectiveness of remedial and compensatory interventions in executive deficit reduction. In turn, upon analysis of 20 papers, van de Ven et al. [94], concluded that most reported good effects of computer-based cognitive training on functional improvement in stroke patients. Unluckily, most studies suffered certain methodological limitations (e.g. lack of an active control group or no adjustment for multiple testing), thus hampering differentiation of training effects and spontaneous recovery, retest effects and placebo effects.

CONCLUSIONS

Post-stroke executive dysfunctions are an important clinical and social problem. The loss of skills to perform complex tasks or impairment of planning and anticipating might adversely affect the social and professional functioning of patients and their quality of life. In the diagnostics of executive dysfunction, it is important to use a variety of neuropsychological methods, especially those of confirmed ecological validity, to properly recognise the underlying causes of the observed deficits and recommend effective forms of therapy. <.h3>Conflict of interest/Konflikt interesu Absent./Nie występuje.

Financial support/Finansowanie

This paper was supported by a grant from the Faculty of Humanities, University of Szczecin no. 504-3000-240-764/2012./Praca finansowana z grantu Wydziału Humanistycznego Uniwersytetu w Szczecinie nr 504-3000-240-764/2012.

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