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• W1969138215 abstract "Back to table of contents Previous article Next article DepartmentsFull AccessImprovement in Athletic Performance as an Early Symptom of Behavioral Variant Frontotemporal DementiaSimon Ducharme, M.D., M.Sc., Bradford C. Dickerson, M.D., Bruce H. Price, M.D.Simon DucharmeSearch for more papers by this author, M.D., M.Sc., Bradford C. DickersonSearch for more papers by this author, M.D., Bruce H. PriceSearch for more papers by this author, M.D.Published Online:29 Apr 2015https://doi.org/10.1176/appi.neuropsych.14060136AboutSectionsPDF/EPUB ToolsAdd to favoritesDownload CitationsTrack Citations ShareShare onFacebookTwitterLinked InEmail To the Editor: Symptoms of behavioral variant frontotemporal dementia (bvFTD) include complex personality changes and socioaffective dysfunction.1 In the early stages, these symptoms are often subtle and are difficult to identify in the clinic. Athletic activities elicit psychological traits that are often inhibited in day-to-day life (e.g., risk taking, aggression) and draw on complex cognitive and emotional skills. Consequently, sports could magnify behavioral, cognitive, and emotional dysregulation. We report the first case of bvFTD in which the earliest behavioral change was improved athletic performance as a result of decreased use of risk-averse strategies and increased flow.Case ReportA 49-year-old woman was assessed at the Behavioral Neurology and Neuropsychiatry Clinic of McLean Hospital for an 18-month history of progressive executive dysfunction. Her organization skills had become too impaired for her to work as an event planner or prepare meals. Behavioral symptoms included mild apathy and slight disinhibition (e.g., uncharacteristically getting angry at other drivers). There was no clear loss of empathy/sympathy, compulsive/repetitive behavior, or hyperorality. She was easily distractible and had inconsistent problems with recall of recent and remote information. There were no sensory, motor, or gait symptoms. Her family history indicated that her father had late-onset Alzheimer’s disease. The patient scored 11 on 30 on the Montreal Cognitive Assessment (z score=−4.2)2 and 4 on 18 on the Frontal Assessment Battery (z score=−27.4).3 Both tests revealed major impairments in working memory, executive function, and phonemic fluency (zero words in 1 minute). Language and visuospatial skills were relatively preserved. Retrieval of memory deficits and mild storage decay were present in this patient, but encoding was relatively preserved. Her elemental neurological examination was normal, with no limb/orobuccal apraxia. A brain MRI scan obtained 6 months prior showed nonspecific mild volume loss. Possible bvFTD1 was suspected based on the severity of her frontal systems deficits; however, behavioral changes (apathy and disinhibition) were subtle.A retrospective analysis conducted with the patient’s family revealed that early behavioral changes were seen when the patient was playing tennis, a sport in which she was proficient. According to her long-time playing partners, the patient’s performance improved after the onset of her illness. Although she could not monitor the game (e.g., keep score), her play was outstanding once the ball was in play. One explanation was a loss of risk-averse strategies. In tennis, a player has two chances to place a serve within the proper boundaries. The first serve is hit with maximal strength to win the point, and players typically rely on a weaker but safer second serve after a miss. The patient had used that strategy for decades, but all of her serves were now first serves delivered at full power. Despite this, she did not commit more double faults (two consecutive missed serves) because of the improved accuracy of her first serves. In addition, her playing partners described an increased sense of flow4 (i.e., she was playing with complete focus and enjoyment, without worrying about the score, the opponent, the outcome, or her physical discomfort). On a less positive note, the patient demonstrated an inability to restrain her game when playing casually against a weaker opponent, highlighting a loss of social inhibitory skills that had once been routine for her.Sixteen months after the initial assessment, a brain MRI scan revealed predominant bilateral prefrontal atrophy in the polar, medial, and dorsal regions, in addition to lesser parietal and lateral temporal volume loss (Figure 1). A fluorodeoxyglucose–positron emission tomography scan showed marked anterior frontal hypometabolism, in addition to reduced activity in the temporal and parietal lobes bilaterally. A frontotemporal dementia genetic workup was normal, and the patient was homozygous for APOE-ε3. She was diagnosed with probable bvFTD, and she refused CSF biomarker testing to rule out the possibility of atypical predominantly frontal Alzheimer’s disease. Over time, the patient became more apathetic, lost capacity for empathy, and developed an increased craving for sweet food, supporting the diagnosis of bvFTD.FIGURE 1. T1-Weighted Brain MRI Scan Obtained 3 Years After the Estimated Onset of Symptomsaa(Top) The MRI scan (left, sagittal; right, axial) shows diffuse volume loss with predominant severe atrophy in bilateral polar, medial, and dorsal prefrontal areas. (Bottom) Red and yellow depict brain areas in which cortical thickness measured with FreeSurfer software was significantly thinner in this patient than in a group of healthy control subjects (p≤0.01, for visualization purposes).DiscussionTo our knowledge, this is the first report of altered sports-related behavior secondary to bvFTD. There are reports of preserved golf skills in a patient with short-term amnestic deficits secondary to Alzheimer’s disease5 and in a patient with bvFTD and semantic deficits.6 In our case, implicit procedural skills and semantic memory for tennis were preserved, but the patient lost monitoring skills as a result of distractibility and executive deficits. The preservation of her motor abilities is striking in light of her significant frontoparietal atrophy, which is probably explained by the relative sparing of the primary motor/sensory strip and basal ganglia (Figure 1). The preservation of semantic memory is consistent with the limited left temporal pole involvement.The improvement of her game was attributable to a loss of self-doubt and inhibitions that can stifle performance in sports, which relates to the concept of flow.4 Flow is the state of experience of total absorption by an activity, accompanied by feelings of control, joy, and time distortion.4 A player experiencing flow will be perceived as playing effortlessly, intuitively described as “playing out of his or her mind.” Sports psychologists try to help athletes reach this mental state, in which one enjoys the game without being overly concerned with the opponent and consequences of winning/losing. Negative self-inhibiting cognitions most likely involve the dorsolateral prefrontal cortex, and it has been hypothesized that flow could be related to decreased frontal activity.7 Although there are inherent limitations to studying this subjective state with neuroimaging,8 this case provides some support for this hypothesis. This patient’s severe bilateral dorsolateral prefrontal cortex atrophy seems to prevent her from engaging in self-defeating cognition. In addition, flow is associated with a transient dissociative loss of self-awareness,4 which parallels the sustained loss of self-awareness in bvFTD. It is conceivable that atrophy in medial frontal areas involved in social cognitive skills9 and risk/reward analyses (orbitofrontal cortex)10 are responsible for her lack of consideration for the opponent and her loss of the fear of losing.As demonstrated by this case, athletic activities can provide a real-life experiment to detect early social cognitive deficits (e.g., respect for rules/norms, risk/benefit assessments, and theory of mind). We argue that behavioral changes in sports and games should be explored during the clinical assessment of bvFTD. Finally, this case provides a heuristic lesion-based model of the neurobiology underlying flow.4From the Behavioral Neurology and Neuropsychiatry Clinic (SD, BHP), Dept. of Neurology, McLean Hospital, Belmont, MA; Depts. of Psychiatry (SD) and Neurology (SD, BCD, BHP), Massachusetts General Hospital, Harvard Medical School, Boston, MA; Dept. of Psychiatry (SD), McGill University Health Centre, Montreal, QC (Canada); and McConnell Brain Imaging Centre (SD), Montreal Neurological Institute, Montreal, QC (Canada).Correspondence: Simon Ducharme, M.D., M.Sc.; e-mail: [email protected]Dr. Ducharme’s fellowship was supported by the Sidney R. Baer, Jr. Foundation, the Fonds de Recherche du Québec-Santé, and the McGill University Health Centre Research Institute (Frank McGill Travel Fellowship).Dr. Dickerson has served as a consultant for Pfizer, Inc., and En Vivo, Inc. The other authors report no competing interests.References1 Rascovsky K, Hodges JR, Knopman D, et al.: Sensitivity of revised diagnostic criteria for the behavioural variant of frontotemporal dementia. Brain 2011; 134:2456–2477Crossref, Medline, Google Scholar2 Rossetti HC, Lacritz LH, Cullum CM, et al.: Normative data for the Montreal Cognitive Assessment (MoCA) in a population-based sample. Neurology 2011; 77:1272–1275Crossref, Medline, Google Scholar3 Appollonio I, Leone M, Isella V, et al.: The Frontal Assessment Battery (FAB): normative values in an Italian population sample. Neurol Sci 2005; 26:108–116Crossref, Medline, Google Scholar4 Hunter J, Csikszentmihalyi M: The phenomenology of body-mind: the contrasting cases of flow in sports and contemplation. Anthropol Consciousness 2000; 11:5–24Crossref, Google Scholar5 Schacter DL: Amnesia observed: remembering and forgetting in a natural environment. J Abnorm Psychol 1983; 92:236–242Crossref, Medline, Google Scholar6 Venneri A, Shanks MF: Preservation of golf skills in a case of severe left lobar frontotemporal degeneration. Neurology 2001; 57:521–524Crossref, Medline, Google Scholar7 Dietrich A: Neurocognitive mechanisms underlying the experience of flow. Conscious Cogn 2004; 13:746–761Crossref, Medline, Google Scholar8 Klasen M, Weber R, Kircher TTJ, et al.: Neural contributions to flow experience during video game playing. Soc Cogn Affect Neurosci 2012; 7:485–495Crossref, Medline, Google Scholar9 Amodio DM, Frith CD: Meeting of minds: the medial frontal cortex and social cognition. Nat Rev Neurosci 2006; 7:268–277Crossref, Medline, Google Scholar10 Kringelbach ML, Rolls ET: The functional neuroanatomy of the human orbitofrontal cortex: evidence from neuroimaging and neuropsychology. Prog Neurobiol 2004; 72:341–372Crossref, Medline, Google Scholar FiguresReferencesCited byDetailsCited byNone Volume 27Issue 2 Spring 2015Pages e163-e164 Metrics PDF download History Published online 29 April 2015 Published in print 1 April 2015" @default.
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