|Year : 2016 | Volume
| Issue : 1 | Page : 35-45
Elucidating the neuropsychological profile of apathetic syndrome and disinhibition syndrome in a brain-injured population in Oman
Samir Al-Adawi1, Aziz Al-Naamani1, Yahya Al-Farsi2, Musthafa M Essa3, David T Burke4, May El-Bouri1, Kerry Amstrong5, Jason Edwards5, Sura Al-Muscati1, Aida Saihi MacFarland1, Ali Al Maashani6
1 Department of Behavioral Medicine, College of Medicine and Health Sciences, Sultan Qaboos University, Muscat, Oman
2 Department of Family Medicine and Public Health, College of Medicine and Health Sciences, Sultan Qaboos University, Muscat, Oman
3 Department of Food Science and Nutrition, College of Agricultural and Marine Sciences, Sultan Qaboos University, Muscat, Oman
4 Department of Rehabilitation Medicine, Emory University Medical School, Atlanta, Georgia, USA
5 Centre for Accident Research and Road Safety - Queensland, Queensland University of Technology, Brisbane, Queensland, Australia
6 Department of Neurosurgery, Khoula Hospital, Ministry of Health, Oman
|Date of Submission||05-Aug-2015|
|Date of Acceptance||07-Aug-2015|
|Date of Web Publication||12-Jan-2016|
Department of Behavioral Medicine College of Medicine and Health Sciences Sultan Qaboos University, Muscat
Source of Support: None, Conflict of Interest: None
| Abstract|| |
Objective: The purpose of this study was to compare the neuropsychological performance of two frontal dysexecutive phenotypes - disinhibited&' syndrome (DS) and &'apathetic&' syndrome (AS) following a traumatic brain injury in a non-western population, Oman. Methods: The study compared the performance of DS and AS in neuropsychological measures including those tapping into verbal reasoning ability/working memory/attention planning/goal-directed behavior and affective ranges. Results: The present analysis showed that DS and AS participants did not differ on indices measuring working memory/attention and affective ranges. However, the two cohorts differed significantly in measures of planning/goal-directed behaviour. Conclusion: This study lays the groundwork for further scrutiny in delineating the different characteristics of what has been previously labelled as frontal dysexecutive phenotype. This study indicates that DS and AS are marked with specific neuropsychological deficits.
Keywords: Apathetic syndrome, cognitive measures, disinhibition syndrome, executive functioning, neuropsychology, Oman, traumatic brain injury
|How to cite this article:|
Al-Adawi S, Al-Naamani A, Al-Farsi Y, Essa MM, Burke DT, El-Bouri M, Amstrong K, Edwards J, Al-Muscati S, MacFarland AS, Al Maashani A. Elucidating the neuropsychological profile of apathetic syndrome and disinhibition syndrome in a brain-injured population in Oman. Int J Nutr Pharmacol Neurol Dis 2016;6:35-45
|How to cite this URL:|
Al-Adawi S, Al-Naamani A, Al-Farsi Y, Essa MM, Burke DT, El-Bouri M, Amstrong K, Edwards J, Al-Muscati S, MacFarland AS, Al Maashani A. Elucidating the neuropsychological profile of apathetic syndrome and disinhibition syndrome in a brain-injured population in Oman. Int J Nutr Pharmacol Neurol Dis [serial online] 2016 [cited 2021 Mar 7];6:35-45. Available from: https://www.ijnpnd.com/text.asp?2016/6/1/35/173787
| Introduction|| |
Neurocognitive disorders, previously not featured in psychiatric nomenclatures such as the Diagnostic and Statistical Manual of Mental Disorders (DSM), have made a resurgence in the new edition of the DSM-5. This highlights the view that a symptom checklist approach or Krepelian descriptive psychiatry is being supplanted with an approach that would hinge strongly on how psychological processes and behaviors are intimately related to the structure and function of the brain. The imminent erosion of the hegemony of a descriptive approach has coincided with the emergence of behavioral neuroscience, the information processing view of the mind, cognitive psychology and cognitive science. Within such developments, there is a need to “dissect” the neurocognitive functioning of some of the broader syndromes such as frontal lobe syndrome or its modern counterpart, executive dysfunction, also termed the frontal dysexecutive phenotype. As yet, some of the existing literature has not delineated the cognitive profile of Apathetic Syndrome (AS) or its orthogonal counterpart, Disinhibition Syndrome (DS). The frontal lobe, with its reciprocal projections and various subcortical structures, has been labelled as the locus of “higher mental functions” or “neural architectures of reason” and as the center for those activities which characterize humanity. Clinical evidence and animal research have suggested that there are five frontal-subcortical circuits, which link specific regions in the frontal lobe with the thalamus and basal ganglia., The first is a motor circuit originating in the supplementary motor area, which runs through the ventral caudate to the globus pallidus and thalamus. The second is the oculomotor circuit, which originates in the frontal eye fields and has connections with caudate nucleus, globus pallidus, substantia nigra and thalamus. The third is the dorsolateral prefrontal circuit which originates from the convexity of the frontal lobe and projects to the caudate nucleus, globus pallidus, subthalamic nucleus, and substantia nigra. The fourth is the lateral orbitofrontal circuit, which projects to the ventromedial cortex. The fifth is the anterior cingulate circuit, which projects to the cingulate gyrus to the striatum, nucleus accumbens, olfactory tubercle, and putamen. When the integrity of the frontal-subcortical region is compromised, neurobehavioral impairments have been reported. The consensus is that the critical roles of the frontal cortex and its reciprocal subcortical structure are planning, temporal organization of behavior, strategy formation, and response monitoring. On these grounds, these functions have been termed as “executive function” to describe the functions of the intact frontal cortex and “dysexecutive syndrome” to describe the deficits resulting when it is damaged.
One approach to delineate different types of dysexecutive syndrome is via neuroimaging and anatomical data.,, Within such a framework, Duffy and Campbell  have described three major “frontal lobe syndromes” that, in modern parlance, constitute a dysexecutive syndrome. The “orbitofrontal” or “disinhibited” syndrome (DS) has the core features of disinhibition, impulsivity, emotional lability, poor insight, poor judgement, and distractibility. The “frontal convexity” or “apathetic”
syndrome (AS) features apathy, indifference, psychomotor retardation, stimulus boundness, poor word list generation, poor abstraction and categorization, and a segmented approach to visuospatial analysis. The “medial” or “akinetic”
frontal syndrome features a paucity of spontaneous gestures and movement, sparse verbal output, weakness, loss of sensation of the lower extremities, and incontinence. However, reliance on invasive neuroimaging and anatomical data to tap the presence of dysexecutive syndrome may not be viable in clinical situations where rapid screening is essential if not paramount. There are a number of measures that have been shown to be sensitive in tapping the presence of frontal lobe damage, most predominantly DS and AS 
as well as neurocognitive functioning.
Conversely, the third frontal lobe syndrome, “akinetic” frontal syndrome, is characterized most significantly in ambulatory behavior and neuropsychological batteries appear to be less sensitive. The question remains whether DS and AS are accompanied by specific neurocognitive profiles. Both AS and DS are common in brain-injured populations., Each year, according to the World Bank, road traffic mishaps kill 1.2 million people, and 10 million others are rendered disabled. In many instances, it is the youngest or the most productive members of the society who is either maimed or killed with all social and economic consequences that this may entail. Oman, a country of approximately 3 million people situated on the southern tip of the Arabian peninsula, has one of the highest rates of road traffic crashes in the world. This provides fertile ground to explore neurocognitive functioning in non-Western populations, as there is a dearth of studies in this area.
The purpose of this study is to examine how clinically observed DS and AS patients fare in tests indexing cognition and affective range. The related aim of this study is to delineate the cognitive profile that demarcates these two syndromes–disinhibition versus apathetic.
| Materials and Methods|| |
The participants were patients who had sustained a traumatic brain injury (TBI) and who were referred to a state-run tertiary care facility for evaluation and treatment. Each consenting participant was examined as to whether he/she HAD sustained a single incident of TBI and had no neurological or psychiatric illnesses prior to sustaining the TBI. TBI is defined here as an injury to the brain tissues caused by an external mechanical force as evidenced by a loss of consciousness, posttraumatic cognitive and behavioral changes, or an objective neurological finding that can reasonably be attributed to TBI on physical, cognitive, and behavioral status examinations. Patients attending the outpatient clinic for posttraumatic follow-up with complaints of depression, changes in personality, cognitive deficits, and posttraumatic physical impairments were included in the analysis. Exclusion criteria consisted of preinjury and psychiatric or neurological history other than those resulting from TBI. In addition, non-Omani patients and those who were known to have sensory or cognitive impairment that would preclude completion of the protracted assessment were excluded from the sample.
Consenting participants were invited to participate in an anonymous survey and interview for assessment of their neuropsychological functioning. This invitation was extended during routine outpatient visits for those who fulfilled the criteria for the presence of posttraumatic AS or DS as defined below. The sample size has been estimated using THE EPI Info version 6.0 computer program (Atlanta, Georgia, USA). With a type 1 error of 5% (alpha = 0.05) and 95% level of significance, it was estimated that 52 subjects would be required for the study to detect an 80% difference in odds ratio (OR) with sufficient power of 80%. Therefore, the target was set to reach 52 participants in order to achieve the objectives of the study.
Informed consent was obtained. The study was approved by both the Ethic Committee for Human and Clinical Research and the Medical Research Committee (Project No. MED 99-4) of the College of Medicine, Sultan Qaboos University.
The participant caregivers gave their input for evaluation as a measurement of AS and DS. These informants were either family members or relatives who interacted with the patient on a regular basis, as is often part of the extended household common in Oman. For both evaluations, the principal investigator sat with the informants and read out each item. The investigator sought clarification on responses that were not clear. There was a strong rationale for informant-rated versions for quantifying AS and DS. Previous studies have alluded to the view that informant-rated versions have acceptable reliability and validity  because informant-rated versions cirumvent reported “ego-dystonic” behavior and the tendency for those with a TBI to fall prey to denial of illness or anosognosia.
Assessment of disinhibited syndrome
The items employed to elicit the presence of DS were identified from the literature including ,, those items that tap into (1) short attention span, easily distracted and unable to concentrate; (2) impulsive, irritable, easily angered; (3) restless and hyperactive; (4) rapid, loud, or excessive talking; (5) sudden changes of mood; and (6) social inappropriateness or lack of conformity to social convention. Two independent teams of caregivers (informant-rated versions) were asked to state whether characteristics of the patient were representative of DS. These characteristics were evaluated as being one of the following: (i) absent: the behavior is not present; (ii) present to a slight degree; (iii) present to a moderate degree; and (iv) present to an extreme degree in their loved ones. Each item was rated on a scale of 0 to 3. A composite score for a patient ranged between 0 and 18. Higher scores indicated a heightened level of DS. As as there is no “gold-standard” measure for DS, we determined that it was not feasible to establish a cutoff point for DS from the presently defined characteristics. Thus, the subjects whose cutoff score was ≥9 were invited for neuropsychological testing as described below. The interrater reliability was established among the two independent teams of caregivers to standards of 90% agreement on the six items of the DS score. The overall percentage agreement between the raters on the selected parameters (test-retest reliability) was found to be 86% (Cohen&'s kappa = 0.81, and the Cronbach&'s alpha = 0.84). Therefore, the global psychometric assessment of the questionnaire indicated that the overall reliability was high. This instrument is thereby labeled here as the “Disinhibited Evaluation Scale.”
Assessment of apathetic syndrome
The presence of AS was determined via the Apathy Evaluation Scale (AES). AES has been shown to have psychometric validity in various clinical populations with negativistic features including poverty of action and mental processes.,, The AES consists of 18 items covering interest, initiation of activity, motivation, insight, and emotionality. This scale is administered in three different forms: self report, informant report, and clinical interview. For the present study, AS was quantified using the informant report version. AES has been previously validated for the Omani population. Each item is rated on a scale of 1 to 4. A composite score for a patient ranges between 18 and 72. Higher scores indicate a heightened-apathetic state. For this study, a cutoff score of 34 or greater was used to define the presence of AS.
Estimate of general intellectual ability
Raven&'s Standard Progressive Matrices was administered to estimate the participant&'s current intellectual ability. The test requires neither language nor academic skills and is labeled as a “culture free” test. It consists of 60 items grouped into five sets. Each item contains a pattern problem with one part removed and between six and eight pictured inserts of which one contains the missing fragment. The subject points to the pattern he/she selects as correct.
Two measures, Digit Span and Buschke Selective Reminding Test were utilized to tap into working memory and attention.
Digit Span  measures verbal/auditory attention and short-term memory. The scale has two components: Digit Forward and Digit Backward. Both tests consisted of seven pairs of random number sequences that the examiner reads aloud. It has been argued that a lower score on the Digit Span Test is usually due to impairment of attention/concentration and working memory.
The Buschke Selective Reminding Test  examines the rate of learning new information, which requires the integrity of working memory and attentional capacity. The subject recalls as many words as he/she can in any order from a list of 12 items just read to him/her. After each trial, the examiner repeats all the items which the subject omitted in that recall trial. This technique has been suggested to provide a means of assessing encoding, retention, and retrieval of information, which have been suggested to be integral parts of attention and working memory. The scoring utilized in this study has been detailed elsewhere.
Planning and goal-directed behavior
For the present purpose, three measures (Verbal Fluency, Tower of London and Wisconsin Card-Sorting test) were employed to detect planning and other indices of goal-directed behavior.
The controlled Oral Word Association test or Verbal Fluency  examines lexical ability, executive control ability, and initiation speed of verbal responses. Neuropsychological underpinnings of verbal fluency have been linked to the integrity of the dorsolateral prefrontal cortex, which, in turn, has been associated with executive functioning., Subjects are asked to produce as many different words as possible that begin with each of three specific letters, with 30 seconds to generate responses per letter. In this study, the letters were derived from the Arabic alphabet, “taa,” “raa,” “waaw,”as described elsewhere. Subjects are told explicitly not to repeat the same word twice, and not to say the same word with a different ending (for example, fish, fishing, fisherman). Following instruction, examples, and a demonstration to ensure that the subject understands the task requirements, he/she is given each letter in turn. The total score for verbal fluency is thus the total number of different acceptable words produced across the three 30-s periods.
Tower of London is a neuropsychological test that was operationalized here to index deficits in planning and the temporal organization of behavior. Participants were asked to formulate a plan to move colored beads that are stacked on three poles to achieve a predetermined realignment on three adjacent poles, in the minimum possible number of moves. For the present purpose, the test was scored according to Bull et al. The total score was the sum of all correctly solved trials up to a maximum of 25 moves. After two consecutive failures, the test was abandoned. If the subject successfully solved 1-1, 2-2, 3-3, 4-4, and 5-move trials, he/she achieved a total score of 25. This is defined here as the number of correctly solved problems (number solved). In addition to the number of correctly solved problems, “planning time” was also recorded. There were nine trials and for each trial, the participant was timed in seconds in order to gauge how long it took for him/her to initiate the first move. This was operationalized here as “planning time” and has been reported in seconds. There is no difference between total time for those who finished all the trials and those who did not. To account for this difference, the total number of seconds is divided by the number of trials completed.
The Modified Wisconsic Card Sorting Test was included as a test for planning and cognitive flexibility. The test involves deducing response strategies in order to complete abstract sets as well as maintaining these strategies and/or changing them depending on the feedback that comes from the examiner. The present score was calculated according to the scoring system of Nelson. Accordingly, two indices were recorded: the number of categories achieved and perseverative error, as described elsewhere. Perseveration exists when one persists in using a rule that was initially correct, even after he/she has received feedback on it being no longer accurate.
Hospital Anxiety and Depression Scale (hads) was employed to assess emotional functioning for the present study. The HADS is a 14-question self-report questionnaire used to measure symptoms associated with anxiety and depression. The Arabic language version of HADS, which has also been used by many authors for different Arabic speaking populations,, was used for the present purpose with a scoring protocol that has been described elsewhere.
In order to assess the association between those with AS versus DS and their neuropsychological performance, a series of crude and adjusted multilinear regression models were conducted. The strength of association was measured by obtaining the standardized beta (β) coefficient and its 95% confidence interval (CI). The dependent variable was subsequently defined as neuropsychological tests. In crude models, the status (AS vs DS) was the only predictor variable. In the adjusted models, the predictor variables included the status (AS vs DS) and other important confounding factors: Gender, age, educational level, and time since injury. The underlying assumptions such as normality and homoscedasticity were investigated by executing histograms of the distribution of the dependent variable in each model. Also, tests of fit such as log-likelihood ratio test and Pearson Chi squared test were performed.
All statistical analyses were performed using the Statistical Package for Social Sciences (SPSS) software (version 20.0, IBM, Chicago, Illinois, USA), and a cutoff P value of < 0.05 was used for all tests of statistical significance.
| Results|| |
After assessment of the two syndromes, 30 patients identified as having AS and 24 with DS (54 total) were recruited for neuropsychological assessment. From the sample, 37 participants (68.52%) were male and over 80% of the participants were aged below 35 years. Close to half (46.30%) of the participants had an education level higher than secondary school. The majority of participants either had a Glasgow Coma Scale score in the severe range at the time of injury (42.59%) or had an unknown score (46.30%). Nearly half (44.44%) of the participants had incurred the injury within the 6 months prior to testing and over half (57.41%) had sustained a diffuse injury. The majority (79.63%) were not on a psychotropic medication. For further details, see [Table 1].
|Table 1: Demographic and clinical characteristics of the participant with apathetic vs. disinhibited syndrome, Oman, 2013|
Click here to view
In order to compare between the demographic and clinical variables of each group, Fisher&'s exact test was used [See [Table 1]. There were significantly more AS participants aged 26–35 years and significantly more DS participants aged 15–25 years. Furthermore, there were a greater number of participants with only a primary education with DS, likely reflecting the higher number of those who were of a younger age. The only other significant difference between each participant group was the length of time since injury. Those with AS were more likely to have been injured in the past 6 months and those with DS were more likely to have been injured in the 6–12 months prior to the study.
Independent samples t-tests were used to compare the mean scores for participants with each condition [See [Table 2]. For the Digit Span tests, Verbal Fluency, Tower of London (planning time), and affective range (anxiety), Levene&'s tests for equality of variance were significant and thus, equal variance was not assumed for these tests. Participants with DS scored higher on Digit Span–Digit Forward [t (28.58) = 3.36, P &< 0.001)], Buschke Selective Reminding Test [t (52) = 3.32, P = 0.002)], and Verbal Fluency (t (34.28) = 4.14, P < 0.001. Further, those with DS showed more perseverative errors (Wisconsin Card Sorting Test) [t (52) = 5.49, P < 0.001]. Finally, those with AS took longer to plan for the Tower of London [t (46.32) = -4.49, P < 0.001)].
|Table 2: Indices of neurocognitive and affective functioning among participants with an apathetic syndrome and disinhibited syndrome, Oman, 2013|
Click here to view
[Table 3] shows assessment of the association between the status (being AS vs DS) and neuropsychological performance as a result of multilinear regression analyses. Therefore, the models estimated the change in the mean unit scale of each neuropsychological test by a change in unit of status (AS vs DS) as a dichotomous variable. [Table 3] shows the standardized β coefficient for each model and its 95% CI. The crude linear regression models suggested the presence of a significant association between the frontal syndrome of the participant and some neuropsychological tests. After adjusting for confounders, the significant association (P < 0.05) was observed between frontal syndrome and the following neuropsychological tests: Verbal fluency, planning time (Tower of London), perseverativeerrors (Wisconsin Card-Sorting Test), and number of categories solved (Wisconsin Card Sorting Test).
|Table 3: Crude and adjusted analyses of the association between the status (apathetic syndrome versus disinhibited syndrome) and neuropsychological performance, Oman, 2013|
Click here to view
| Discussion|| |
It has been proposed that when the integrity of the nervous system is compromised, there is a high chance for the emergence of intransigent sequelae including personality changes that manifest as “behavioral inhibition” and conversely, “behavioral activation.”,, In neuropsychiatric parlance, such impairments are a hallmark of impaired goal-directed behavior which, on the one hand, could manifest with characteristics such as a “poverty of will” marked with negativistic symptoms or AS. On the opposite spectrum of AS, some brain-injured populations are marked by the tendency to act impulsively and without thinking, and are likely to be seen as disinhibited. These impairments present a serious barrier to management, rehabilitation, and vocational adjustment, possibly more so than with other deficits. AS is likely to simulate or intensify other cognitive and emotional impairments as well as exacerbate difficulty with activities involved with daily living., Similarly, individuals with disinhibition are prone to the fallout of risky behavior. There is also indication that the presence of disinhibition or its accompanying condition, executive dysfunction, in a brain-injured population tends to have poor prognostic indicators compared, for example, to those with a preponderance of amnesiac features. AS has been indicated to be impervious to available pharmacotherapy.
Symptoms akin to both AS and DS have been documented in various populations around the world. The incidence of conditions similar to AS has been shown to vary from 18% to 90% for various neuropsychiatric and neurological populations.,,, On the other hand, the magnitude of DS has not been well established, because of the overlap of the symptoms of DS, with other neurobehavioral symptoms such as mania, hyperactivity disorders, executive dysfunction or fontal lobe syndrome; however. it has been noted to be common.
The neurocognitive profiles of DS and AS have been previously documented ,, but limited to brain-injured populations from Western Europe and North America. In order to fill the gap in the literature, this study compares neurocognitive functioning of participants with AS and DS following a single incidence of a TBI, the majority of which were due to road traffic crashes. One of the fallouts of the recent affluence in Oman is the rising tide of road traffic mishaps. There is a dearth of studies that have explored the performance of road traffic crash victims on neuropsychological batteries.
Firstly, the present study suggests that the two cohorts did not differ in the test tapping non-verbal intellectual functioning, the Raven&'s Standard Progressive Matrices. This rules out the confounding factor that the two groups might differ in intellectual ability which, in turn, has an implication for their performance in the cognitive measures. Raven&'s Standard Progressive Matrices is equipped to gauge verbal reasoning ability which, in turn, encapsulates fluid intelligence, “Spearman&'s g” or general intelligence. There is evidence that both AS and DS are associated with social deficits characterized by impaired quality of life, occupational incompetency or performing less well scholastically. This cross-cultural study concurs with other studies that social deficits common in post concussion in those diagnosed with DS and AS are independent of intellectual ability.
The second interrelated intent of this study was to examine the difference in performance on neurocognitive measures that are sensitive for indices of working memory, short term memory, concentration and attention. On the whole, the two cohorts did not significantly differ in such measures except for Digit Span-Digit Forward. Previous studies have indicated that there are distinctive cognitive mechanisms involved in processing Digit Forward compared to Digit Backward. Attention and short term memory have always been associated with Digit Forward, while working memory has been associated with Digit Backward. A previous study has indicated that Digit Backward, which taps into a complex type of working memory would be more impacted in those with AS. However, this was not the case for the present study. Further studies are, therefore, warranted.
The third objective of this study was to examine whether indices of planning- and goal-directed behavior differentiate between brain-injured populations with AS and DS. The present study indicated that the two groups differed significantly in indices operationalized to tap into planning and goal-directed behavior. These indices include the Controlled Oral Word Association Test-Verbal Fluency Tower of London- planning time and two indices of Wisconsin Card Sorting Test–total number of categories achieved and perseverative errors. Verbal Fluency measures the ideational fluency as well as executive functioning, which, in turn, has been linked to the integrity of the frontal-subcortical structure that is involved in planning- and goal-directed behavior. As verbal fluency examines the initiation and speed of verbal responses, it should be expected that participants in the study with AS will be marked by a poverty of verbal output and therefore, perform poorly in Verbal Fluency. The present finding is consistent with such a view. On the other hand, those with DS are marked with impulsivity and therefore, have “excess” verbal output  though there is a concern regarding the accuracy of the verbal output. This could arise due to difficulty in keeping track of the responses that have already been made. Consistent with such a formulation, those with AS appear to have poorer verbal output compared to those with DS. If the centrality of “initiation” is the factor, it should be expected that planning time would also be invariably affected. Consistent with such a view, the results for planning time in the Tower of London task were slower for those with AS compared to those with DS. In the available literature, there is a strong indication that perseverative errorsin the Wisconsin Card Sorting Taskmeasures deficits in task-switching  but there are some suggestions of high perseveration being common in those conditions marked with negativistic features and defective dopaminergic and frontal-subcortical functions. This directly indicates perseverative errors as one of the characteristics of poverty of “willed action,” a view previously reported by Frith. This implies that poverty of action reflects an impairment of volition so that patients find it hard to generate new behavior and either do little to change their behavior or resort, to the simpler behavior of repeating earlier responses as is apparent in the case of perseverative error or the tendency to confabulate. A disruption of “willed action,” critical for initiating and organizing behavior could therefore, offer another account of apparent deficits in those with AS following acquired brain injuries. In preclinical literature, animals with neurotoxic lesions of the dopaminergic projection into the nucleus accumbens have been reported to have an impairment of spontaneous alternation behavior  and this has recently been linked to the fronto-striato-thalamic circuit in humans. In contrast, this study found that scores for the total number of categories achieved, which taps into conceptual skills, executive functioning, set-shifting, and working memory, tend to be more impacted in those with DS. This would imply that the tendency of those with DS is to “act without thinking” and this has a negative repercussion on these cognitive domains.
Psychiatric disorders such as anxiety and depression are common among brain-injured populations. The rate of distress mimicking clinical depression appears to vary from 18% to 90% for various neuropsychiatric and neurological populations., Similarly, spectrums of anxiety disorders have also been shown to be common at 18% and 60% for this population., The question remains as to whether the presence of anxiety and depression could be a defining feature for the diagnosis of DS and AS. The present studies indicate neither anxiety nor depression as elicited by the Hospital Anxiety and Depression Scale associated with DS or AS. This discounts the role of these two types of emotions in differential DS and AS. Speculations are warranted for what appears to be the conspicuous absence of emotional distress in a cross-cultural population such as that in Oman. It has been hypothesized that many negative social experiences in Oman are ascribed to external agents such as the evil eye, spirit infestation, or ensorcellement. Due to cultural patterning, phonotypical presentations of affective range have been noted to be markedly different from those observed in Western populations. Future studies should be employed with measures that are cross-culturally sensitive in identifying affective range.
It is worthwhile to highlight the limitations of the present study. One such limitation is that the characteristic symptoms of DS were drawn from the available literature. The psychometric properties of DS should be established. The instrument that has been widely employed to elicit the presence of impulsivity, Barratt Impulsiveness Scale, may have been utilized in the study. However, one of the drawbacks of the Barratt Impulsiveness Scale is that it is a self-report questionnaire. In order to have ecological validity, the presence of disinhibition in the study was solicited from the caregiver. This circumvents the contesting issue of “ego-dystonic” tendencies in brain-injured participants. In addition, the differences between the length of time since injury in the AS participants and the DS participants are significant. As AS participants were more likely to have been injured in the past 6 months and DS participants were more likely to have been injured in the 6–12 months prior to the study, it may indicate that the emergence of DS and AS are an integral part of the natural history of the two conditions. Longitudinal studies should therefore, be contemplated in order to address this particular limitation. Although there is a perceived gender bias in the results as there were more males than females, this difference is not significant. Road traffic injuries are the major cause of morbidity and mortality for males worldwide  and a similar trend has been reported in Oman.
It is important to note the current study was not equipped to establish the severity of the observed cognitive measures. Many of the measures employed have not been standardized for the present population. Therefore, a concerted effort is needed to establish the application of these measures to an Omani population. Further, both AS and DS tend to have overlapping symptomology and both lack central features. There is no biological marker for AS or DS. This study is limited, as are other studies, that have employed descriptive symptoms without central features. Furthermore, the characteristics of AS and DS being protean, are likely to lay emphasis on behaviors and attitudes that may essentially be limited to the European and North American cultural groups. On this ground, this study may have committed what Kleiman has called “categories of fallacy.”
Finally, the results of the regression models should be interpreted with caution. Despite the goodness-of-fit for the models and the underlying assumptions of independence, normality, and homoscedasticity, the statistical stability of the obtained results might have been affected due to the small sample size. This is evident with the relatively wide range of 95% CI, which reflected a relatively high standard error (SE) of the adjusted odds ratios.
| Summary|| |
This study was initiated to delineate the cognitive profile that demarcates these two syndromes, DS versus AS, among the survivors of a TBI in Oman. Three interrelated measures were utilized for this brain-injured population in Oman. First, neither verbal reasoning ability nor indices of affective functioning differed among these diagnostic entities. Similar trends were observed for indices of working memory/attention except for the Digit Forward Test. Conversely, a comparison indicates statistical differences in the performance on indices of planning- and goal-directed behavior except for results in the Tower of London–number solved. To our knowledge, this the first study that has utilized cognitive measures to differentiate the underpinning of the cognitive processes that are characterized by these two conditions.
We thank the clinical teams of both Khoula Hospital and Sultan Qaboos University Hospital for their continuing support in the study. We are also indebted to the men and women who have voluntarily acted as subjects for the present research, tolerating patiently this quest for understanding neurocognitive function.
Financial support and sponsorship
We acknowledge that this study was supported by a research grant from the Research Council, Oman (Grant # RC/AGR/FOOD/11/01).
Conflicts of interest
There are no conflicts of interest.
| References|| |
De Bruin JP. Evolution of prefrontal cortex: Comparative aspects of its behavioral functions. In: Greenspan RJ, Kyraciou CP, editors. Flexibility and Constraint in Behavioral Systems. Chichester: John Wiley and Sons; 1994. p. 185-92.
Mayberg H. Depression and frontal-subcortical circuits: Focus on prefrontal-limbic interactions. In: Lichter DG, Cummings JL, editors. Frontal-Subcortical Circuits in Psychiatric and Neurological Disorders. New York, NY: Guilford Press; 2001. p. 177-206.
Bonelli RM, Cummings JL. Frontal-subcortical circuitry and behavior. Dialogues Clin Neurosci 2007;9:141-51.
Levy R, Dubois B. Apathy and the functional anatomy of the prefrontal cortex-basal ganglia circuits. Cereb Corte×2006;16:916-28.
Godefroy O, Azouvi P, Robert P, Roussel M, LeGall D, Meulemans T; Groupe de Réflexion sur l&'Evaluation des Fonctions Exécutives Study Group. Dysexecutive syndrome: Diagnostic criteria and validation study. Ann Neurol 2010;68:855-64.
Ramos-Zúñiga R, González-de la Torre M, Jiménez-Maldonado M, Villaseñor-Cabrera T, Bañuelos-Acosta R, Aguirre-Portillo L, et al
. Postconcussion syndrome and mild head injury: The role of early diagnosis using neuropsychological tests and functional magnetic resonance/spectroscopy. World Neurosurg 2013;82:828-35.
Cummings JL. Frontal-subcortical circuits and human behavior. Arch Neurol 1993;50:873-80.
Cummings AS, Mega MS. Neuropsychiatry and Behavioral Neuroscience. Ch. 15: Apathy and Other Personality Disorders. New York: Oxford University Press. p. 228-33.
Duffy JD, Campbell JJ 3rd
. The regional prefrontal syndromes: A theoretical and clinical overview. J Neuropsychiatry Clin Neurosci 1994;6:379-87.
Lane-Brown AT, Tate RL. Measuring apathy after traumatic brain injury: Psychometric properties of the Apathy Evaluation Scale and the Frontal Systems Behavior Scale. Brain Inj 2009;23:999-1007.
Al-Adawi S, Powell JH, Greenwood RJ. Motivational deficits after brain injury: A neuropsychological approach using new assessment techniques. Neuropsychology 1998;12:115-24.
Koponen S, Taiminen T, Portin R, Himanen L, Isoniemi H, Heinonen H, et al
. Axis I and II psychiatric disorders after traumatic brain injury: A 30-year follow-up study. Am J Psychiatry 2002;159:1315-21.
Orlovska S, Pedersen MS, Benros ME, Mortensen PB, Agerbo E, Nordentoft M. Head injury as risk factor for psychiatric disorders: A nationwide register-based follow-up study of 113,906 persons with head injury. Am J Psychiatry 2014;171:463-9.
World Health Organization. WHO Global Status Report on Road Safety 2013: Supporting a Decade of Action. Geneva: World Health Organization; 2013.
Al-Reesi H, Ganguly SS, Al-Adawi S, Laflamme L, Hasselberg M, Al-Maniri A. Economic growth, motorization, and road traffic injuries in the Sultanate of Oman, 1985-2009. Traffic Inj Prev 2013;14:322-8.
Sandra Kooij JJ, Marije Boonstra A, Swinkels SH, Bekker EM, de Noord I, Buitelaar JK. Reliability, validity, and utility of instruments for self-report and informant report concerning symptoms of ADHD in adult patients. J Atten Disord 2008;11:445-58.
Sbordone RJ, Seyranian GD, Ruff RM. Are the subjective complaints of traumatically brain injured patients reliable? Brain Inj 1998;12:505-15.
Amato S, Resan M, Mion L. The feasibility, reliability, and clinical utility of the agitated behavior scale in brain-injured rehabilitation patients. Rehabil Nurs 2012;37:19-24.
King N, Crawford S, Wenden FJ, Moss NE, Wade DT. The Rivermead post concussion symptoms questionnaire: A measure of symptoms commonly experienced after head injury and its reliability. J Neurol 1995;242:587-92.
Marin RS, Biedrzycki RC, Firinciogullari S. Reliability and validity of the Apathy Evaluation Scale. Psychiatry Res 1991;38:143-62.
Santangelo G, Barone P, Cuoco S, Raimo S, Pezzella D, Picillo M, et al
. Apathy in untreated, de novo
patients with Parkinson&'s disease: Validation study of Apathy Evaluation Scale. J Neurol 2014;261:2319-28.
Yuen GS, Bhutani S, Lucas BJ, Gunning FM, AbdelMalak B, Seirup JK, et al
. Apathy in late-life depression: Common, persistent, and disabling. Am J Geriatr Psychiatry 2015;23:488-94.
Marshall GA, Donovan NJ, Lorius N, Gidicsin CM, Maye J, Pepin LC, et al
. Apathy is associated with increased amyloid burden in mild cognitive impairment. J Neuropsychiatry Clin Neurosci 2013;25:302-7.
Al-Adawi S, Dorvlo AS, Burke DT, Huynh CC, Jacob L, Knight R, et al
. Apathy and depression in cross-cultural survivors of traumatic brain injury. J Neuropsychiatry Clin Neurosci 2004;16:435-42.
Rushton JP, Skuy M, Fridjhon P. Jensen effects among African, Indian, and White engineering students in South Africa on Raven&'s standard progressive matrices. Intelligence 2002;30:409-23.
Kazem AM, Alzubiadi AS, Yousif YH, Aljamali FA, Al-Mashdany SI, Alkharusi HA, et al
. Psychometric properties of Raven&'s colored progressive matrices for Omani children aged 5 through 11 years. Soc Behav Pers 2007;35:1385-98.
Al-Adawi S, Al-Zakwani I, Obeid YA, Zaidan Z. Neurocognitive functioning in women presenting with undifferentiated somatoform disorders in Oman. Psychiatry Clin Neurosci 2010;64:555-64.
Lezak MD, Howieson DB, Bigler ED, Tranel D. Neuropsychological Assessment. 5th
ed. Oxford: Oxford University Press; 2012.
Buschke H, Fuld PA. Evaluating storage, retention, and retrieval in disordered memory and learning. Neurology 1974;24:1019-25.
Benton AL. Differential behavioral effects in frontal lobe disease. Neuropsychologia 1968;6:53-60.
Nishimura Y, Takizawa R, Koike S, Kinoshita A, Satomura Y, Kawasaki S, et al
. Association of decreased prefrontal hemodynamic response during a verbal fluency task with EGR3 gene polymorphism in patients with schizophrenia and in healthy individuals. Neuroimage 2014;85:527-34.
Krueger CE, Laluz V, Rosen HJ, Neuhaus JM, Miller BL, Kramer JH. Double dissociation in the anatomy of socioemotional disinhibition and executive functioning in dementia. Neuropsychology 2011;25:249-59.
Al-Ghatani AM, Obonsawin M, Al Moutaery KR. Normative data for the two equivalent forms of the Arabic verbal fluency test. Pan Arab J Neurosurg 2009;13:57-65.
Phillips LH, Wynn VE, McPherson S, Gilhooly KJ. Mental planning and the Tower of London task. Q J Exp Psychol A 2001;54:579-97.
Bull R, Espy KA, Senn TE. A comparison of performance on the Towers of London and Hanoi in young children. J Child Psychol Psychiatry 2004;45:743-54.
Nelson HE. A modified card sorting test sensitive to frontal lobe defects. Cortex 1976;12:313-24.
Hotz G, Helm-Estabrooks N. Perseveration. Part II: A study of perseveration in closed-head injury. Brain Inj 1995;9:161-72.
Malasi TH, Mirza IA, el-Islam MF. Validation of the hospital anxiety and depression scale in Arab patients. Acta Psychiatr Scand 1991;84:323-6.
Al-Adawi S, Dorvlo AS, Al-Naamani A, Glenn MB, Karamouz N, Chae H, et al
. The ineffectiveness of the Hospital Anxiety and Depression Scale for diagnosis in an Omani traumatic brain injured population. Brain Inj 2007;21:385-93.
Al-Asmi A, Dorvlo AS, Burke DT, Al-Adawi S, Al-Zaabi A, Al-Zadjali HA, et al
. The detection of mood and anxiety in people with epilepsy using two-phase designs: Experiences from a tertiary care centre in Oman. Epilepsy Res 2012;98:174-81.
Gray JA. The Neuropsychology of Anxiety: An Enquiry into the Function of the Septo-Hippocampal System. 2nd
ed. Oxford: Oxford University Press; 1982.
Alloy LB, Bender RE, Whitehouse WG, Wagner CA, Liu RT, Grant DA, et al
. High Behavioral Approach System (BAS) sensitivity, reward responsiveness, and goal-striving predict first onset of bipolar spectrum disorders: A prospective behavioral high-risk design. J Abnorm Psychol 2012;121:339-51.
Wagner AK, Postal BA, Darrah SD, Chen X, Khan AS. Deficits in novelty exploration after controlled cortical impact. J Neurotrauma 2007;24:1308-20.
Starkstein SE, Petracca G, Chemerinski E, Kremer J. Syndromic validity of apathy in Alzheimer&'s disease. Am J Psychiatry 2001;158:872-7.
Njomboro P, Humphreys GW, Deb S. Exploring social cognition in patients with apathy following acquired brain damage. BMC Neurol 2014;14:18.
Al-Adawi S, Braidy N, Essa M, Al-Azri F, Hussain S, Al-Sibani N, et al
. Cognitive profiles in patients with multi-infarct dementia: An Omani study. Dement Geriatr Cogn Dis Extra 2014;4:271-82.
Lane-Brown A, Tate R. Interventions for apathy after traumatic brain injury. Cochrane Database Syst Rev 2009;CD006341.
Starkstein SE, Pahissa J. Apathy following traumatic brain injury. Psychiatr Clin North Am 2014;37:103-12.
Kant R, Duffy J, Pivovarnik A. Prevalence of apathy following head injury. Brain Inj 1998;12:87-92.
Andersson S, Krogstad J, Finset A. Apathy and depressed mood in acquired brain damage: Relationship to lesion localization and psychophysiological reactivity. Psychol Med 1999;29:447-56.
Isella V, Melzi P, Grimaldi M, Iurlaro S, Piolti R, Ferrarese C, et al
. Clinical, neuropsychological, and morphometric correlates of apathy in Parkinson&'s disease. Mov Disord 2002;17:366-71.
McPherson S, Fairbanks L, Tiken S, Cummings JL, Back-Madruga C. Apathy and executive function in Alzheimer&'s disease. J Int Neuropsychol Soc 2002;8:373-81.
Al-Sharbati M, Al-Adawi S, Ganguly S, Al-Lawatiya S, Al-Mshefri F. Hyperactivity in a sample of Omani schoolboys. J Atten Disord 2008;12:264-9.
Andersson S, Bergedalen AM. Cognitive correlates of apathy in traumatic brain injury. Neuropsychiatry Neuropsychol Behav Neurol 2002;15:184-91.
Sebastian A, Jung P, Krause-Utz A, Lieb K, Schmahl C, Tüscher O. Frontal dysfunctions of impulse control-a systematic review in borderline personality disorder and attention-deficit/hyperactivity disorder. Front Hum Neurosci 2014;8:698.
Hiscock M, Inch R, Gleason A. Raven&'s progressive matrices performance in adults with traumatic brain injury. Appl Neuropsychol 2002;9:129-38.
Frazier TW, Demaree HA, Youngstrom EA. Meta-analysis of intellectual and neuropsychological test performance in attention-deficit/hyperactivity disorder. Neuropsychology 2004;18:543-55.
Nishimura Y, Takahashi K, Ohtani T, Ikeda-Sugita R, Kasai K, Okazaki Y. Dorsolateral prefrontal hemodynamic responses during a verbal fluency task in hypomanic bipolar disorder. Bipolar Disord 2015;17:172-83.
Uran P, Kılıç BG. Comparison of neuropsychological performances and behavioral patterns of children with attention deficit hyperactivity disorder and severe mood dysregulation. Eur Child Adolesc Psychiatry 2015;24:21-30.
Kopp B, Lange F. Electrophysiological indicators of surprise and entropy in dynamic task-switching environments. Front Hum Neurosci 2013;7:300.
Joseph R. Frontal lobe psychopathology: Mania, depression, confabulation, catatonia, perseveration, obsessive compulsions, and schizophrenia. Psychiatry 1999;62:138-72.
Frith CD. The positive and negative symptoms of schizophrenia reflect impairments in the perception and initiation of action. Psychol Med 1987;17:631-48.
Taghzouti K, Louilot A, Herman JP, Le-Moal M, Simon H. Alternation behavior, spatial discrimination, and reversal disturbances following 6-hydroxydopamine lesions in the nucleus accumbens of the rat. Behav Neural Biol 1985;44:354-63.
van Schouwenburg MR, Onnink AM, ter Huurne N, Kan CC, Zwiers MP, Hoogman M, et al
. Cognitive flexibility depends on white matter microstructure of the basal ganglia. Neuropsychologia 2014;53:171-7.
Meader N, Moe-Byrne T, Llewellyn A, Mitchell AJ. Screening for poststroke major depression: A meta-analysis of diagnostic validity studies. J Neurol Neurosurg Psychiatry 2014;85:198-206.
Mauri M, Paletta S, Colasanti A, Miserocchi G, Altamura AC. Clinical and neuropsychological correlates of major depression following post-traumatic brain injury, a prospective study. Asian J Psychiatr 2014;12:118-24.
Patton JH, Stanford MS, Barratt ES. Factor structure of the Barratt impulsiveness scale. J Clin Psychol 1995;51:768-74.
Gore FM, Bloem PJ, Patton GC, Ferguson J, Joseph V, Coffey C, et al
. Global burden of disease in young people aged 10-24 years: A systematic analysis. Lancet 2011;377:2093-102.
Kleinman A. Anthropology and psychiatry. The role of culture in cross-cultural research on illness. Br J Psychiatry 1987;151:447-54.
[Table 1], [Table 2], [Table 3]
|This article has been cited by|
||Methylphenidate improves executive functions in patients with traumatic brain injuries: a feasibility trial via the idiographic approach
| ||Samir Al-Adawi,Aziz Al-Naamani,Sanjay Jaju,Yahya M. Al-Farsi,Atsu S. S. Dorvlo,Ali Al-Maashani,Sara S. H. Al-Adawi,Ahmed A. Moustafa,Nasser Al-Sibani,Musthafa M. Essa,David T. Burke,M. Walid Qoronfleh |
| ||BMC Neurology. 2020; 20(1) |
|[Pubmed] | [DOI]|