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Apathy in Parkinson's Disease: Clinical Features, Neural Substrates, Diagnosis, and Treatment Article Apathy in Parkinson's disease: clinical features, neural substrates, diagnosis, and treatment PAGONABARRAGA, Javier, et al. Reference PAGONABARRAGA, Javier, et al. Apathy in Parkinson's disease: clinical features, neural substrates, diagnosis, and treatment. The Lancet Neurology, 2015, vol. 14, no. 5, p. 518-531 DOI : 10.1016/S1474-4422(15)00019-8 PMID : 25895932 Available at: http://archive-ouverte.unige.ch/unige:95955 Disclaimer: layout of this document may differ from the published version. 1 / 1 Review Apathy in Parkinson’s disease: clinical features, neural substrates, diagnosis, and treatment Javier Pagonabarraga, Jaime Kulisevsky, Antonio P Strafella, Paul Krack Lancet Neurol 2015; 14: 518–31 Normal maintenance of human motivation depends on the integrity of subcortical structures that link the prefrontal Movement Disorders Unit, cortex with the limbic system. Structural and functional disruption of diff erent networks within these circuits alters the Neurology Department, maintenance of spontaneous mental activity and the capacity of aff ected individuals to associate emotions with complex Sant Pau Hospital and stimuli. The clinical manifestations of these changes include a continuum of abnormalities in goal-oriented behaviours Biomedical Research Institute, Barcelona, Spain known as apathy. Apathy is highly prevalent in Parkinson’s disease (and across many neurodegenerative disorders) and (J Pagonabarraga PhD, can severely aff ect the quality of life of both patients and caregivers. Diff erentiation of apathy from depression, and Prof J Kulisevsky PhD); discrimination of its cognitive, emotional, and auto-activation components could guide an individualised approach to the Universitat Autònoma de treatment of symptoms. The opportunity to manipulate dopaminergic treatment in Parkinson’s disease allows Barcelona, Barcelona, Spain (J Pagonabarraga, researchers to study a continuous range of motivational states, from apathy to impulse control disorders. Parkinson’s Prof J Kulisevsky); Centro de disease can thus be viewed as a model that provides insight into the neural substrates of apathy. Investigación en Red-Enfermedades discriminate its cognitive, emotional, and auto-activation Neurodegenerativas, Madrid, Introduction Spain (J Pagonabarraga, Apathy is a behavioural syndrome that consists of a set of subdomains. Prof J Kulisevsky); Universitat simul taneous behavioural, aff ective, and cognitive In this Review, we focus on apathy in Parkinson’s Oberta de Catalunya, features. Apathy can be defi ned as a state of decreased disease, discussing its prevalence, clinical relevance, Barcelona, Spain motivation that manifests as a decrease in goal-directed pheno menology, neuropsychological correlates, and (Prof J Kulisevsky); Morton and Gloria Shulman Movement behaviours, and can be variably characterised by reduced response to treatments. We propose a model with the Disorder Unit, E.J. Safra interests or emotions that cannot be attributed to aim of linking the separate subdomains of apathy with Parkinson Disease Program, diminished level of consciousness, cognitive impairment, diff erent neurobiological correlates, thus providing an Toronto Western Hospital and 1,2 Research Institute, UHN, ON, or emotional distress. The observable phenomenon of operative framework for the clinical classifi cation of Canada (Prof A P Strafella PhD); apathy is related to four subdomains: decrease in apathetic syndromes and the selection of appropriate Research Imaging Centre, emotional resonance (reward defi ciency syndrome), treatments. Campbell Family Mental Health depression, decrease in cognitive interests (executive Research Institute, CAMH, University of Toronto, ON, dysfunction), and absence of spontaneous activation of Syndromes and substrates of apathy 3,4 Canada (Prof A P Strafella); mental processes (auto-activation defi cit). In psychology, Conceptual issues Movement Disorder Unit, subdomains are defi ned as each one of the discrete Motivation is a psychological feature that arouses an Department of Psychiatry and components that contribute diff erentially to the organism to act towards a desired goal, both eliciting and Neurology, CHU de Grenoble, 12 Joseph Fourier University, manifestation of a cognitive or behavioural syndrome or sustaining goal-directed behaviours. Motivation in 5 Grenoble, France construct. The contribution of these subdomains of healthy human beings acts as an inner drive elicited by (Prof P Krack PhD); and INSERM, apathy can vary from patient to patient, so their physical needs (eg, eating and drinking), but also by Unit 836, Grenoble Institut des discrimination in particular patients could guide an pleasurable and aversive stimuli, as coded by reward- Neurosciences, Grenoble, France (Prof P Krack) individualised approach to the treatment of symptoms based and punishment-based learning, which attach Correspondence to: that lead to diminished goal-directed behaviours. motivational importance to otherwise neutral environ- 13–15 Prof Paul Krack, CHU de Awareness of the importance of neuropsychiatric and mental stimuli. The notion of apathy as a clinical Grenoble, Pavillon de cognitive symptoms, including apathy, in the manage- syndrome was built from original case reports and lesional Neurologie, BP217, ment of patients with Parkinson’s disease has increased studies describing patients with fairly well preserved 38043 Grenoble Cedex 9, France [email protected] in the past decade. An eff ort has been made to describe cognition who showed a striking absence of observable mood disorders in Parkinson’s disease in more detail in spontaneous active behaviours, but who were still capable an attempt to distinguish apathy from depression,6,7 of reacting and behaving almost normally in response to recognising that the emotional expression of apathy external stimulation.16,17 Many descriptive epithets have largely overlaps with anhedonia, which is also a part of been ascribed to this unique combination of an absence of depression.8 Isolated apathy, which is not related to self-initiated goal-directed actions—giving the patient the cognitive impairment or depression, has been recorded aspect of indiff erence, fl attening of aff ect, or emptiness of at early and advanced stages of Parkinson’s disease.9,10 mind—and diminished responsiveness to stimuli. The Apathy can be regarded as an independent nosological diff erent terms used to describe the features of apathy can entity caused by dysfunction of diff erent but interrelated be regarded as describing a continuum of severity of subdomains and neural circuits, and it is increasingly reduced motivated behaviours, up to the most severe recognised as a syndrome with distinct targets for forms of akinetic mutism, abulia, athymhormia, or auto- pharma cotherapy.11 Validated scales assessing specifi c activation defi cits. At present, decreased goal-directed cognitive, motivational, and depressive symptoms can be behaviours in neurodegenerative diseases are generally used to diff erentiate apathy from depression, and categorised as apathy, irrespective of their severity. 518 www.thelancet.com/neurology Vol 14 May 2015 Review Discrimination of apathetic syndromes to guide treatment mesostriatal, mesolimbic, and mesocortical dopaminergic Apathy is a clinically relevant and potentially treatable pathways, as in Parkinson’s disease.26,27 impairment of motivated human behaviour. Identi- When apathy coexists with depression, reduction in fi cation of the diff erent components of apathy could help motivated behaviours is associated with a dysfunctional to determine the treatment approach for individual network that is shown by hyperactivity of the subgenual patients.18 Four major subdomains of goal-directed cingulate cortex (BA25), and hypometabolism of both the behaviour variably contribute (in isolation or, more dorsolateral prefrontal cortex and the dorsal anterior frequently, in combination) to apathy: reward defi ciency cingulate cortex (BA24b).28–30 With recovery from syndrome, depression, executive dysfunction, and auto- depression, metabolism in the dorsal anterior cingulate activation failure (fi gure 1). cortex is restored and goal-directed behaviours Reward defi ciency syndrome refers to a state of improve.31,32 Apathy in the context of executive dysfunction emotional blunting or absence of emotional resonance, is related to decreased activity in a network that which prevents an individual from attaching motivational encompasses the dorsolateral prefrontal cortex, lateral values and pleasure to environmental or inner stimuli.12 aspects of the caudate nucleus and putamen, the anterior Blunted aff ect in isolated apathy should be clinically cingulate cortex, and the posterior parietal cortex.33 diff erentiated from apathy caused by negative aff ect. In Finally, auto-activation defi cit has been reported in major depression, sadness is accompanied by a patients with bilateral lesions involving subcortical substantial reduction in eff ortful and sustained positively structures that disconnect the medial and lateral motivated behaviours.19 A large overlap between apathy prefrontal cortex and the supplementary motor area from and depression exists, with a series of common features. the limbic system.22,23,34 This connection is basically driven However, some emotions and thoughts are more specifi c by the caudate nucleus and the anterior cingulate cortex,35 to depression, so their presence or absence helps to which has a major role in regulating the expression of separate depression from apathy
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