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Brain Mechanisms Underlying Apathy Campbell Le Heron,1,2,3 Clay B Holroyd,4 John Salamone,5 Masud Husain1,2,6,7

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Brain Mechanisms Underlying Apathy Campbell Le Heron,1,2,3 Clay B Holroyd,4 John Salamone,5 Masud Husain1,2,6,7 Cognitive neurology J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp-2018-318265 on 26 October 2018. Downloaded from REVIEW Brain mechanisms underlying apathy Campbell Le Heron,1,2,3 Clay B Holroyd,4 John Salamone,5 Masud Husain1,2,6,7 ► Additional material is ABSTRact mutism, athymhormia and autoactivation deficit published online only. To view The past few decades have seen growing interest in the (see online supplementary table 1 for proposed please visit the journal online (http:// dx. doi. org/ 10. 1136/ neuropsychiatric syndrome of apathy, conceptualised diagnostic criteria). Apathetic patients often report jnnp- 2018- 318265). as a loss of motivation manifesting as a reduction of that they “can’t be bothered,” that activities “don’t goal-directed behaviour. Apathy occurs frequently, and seem worth it,” or that they “just don’t know” why 1 Nuffield Department of Clinical with substantial impact on quality of life, in a broad they no longer engage in behaviours they used to do Neurosciences, University of range of neurological and psychiatric conditions. Apathy Oxford, Oxford, UK (box 2). However a mechanistic understanding of 2Department of Experimental is also consistently associated with neuroimaging this syndrome remains elusive. Psychology, University of Oxford, changes in specific medial frontal cortex and subcortical Although prevalence estimates vary widely Oxford, UK structures, suggesting that disruption of a common 3 depending on assessment tools and the clinical New Zealand Brain Research systems-level mechanism may underlie its development, Institute, Christchurch, New population studied, there is no doubt that apathy Zealand irrespective of the condition that causes it. In parallel is a common accompaniment to a broad range of 4Department of Psychology, with this growing recognition of the clinical importance brain disorders (table 1). A number of neurodegen- University of Victoria, Victoria, of apathy, significant advances have been made in erative, vascular, inflammatory, infectious and trau- British Columbia, Canada understanding normal motivated behaviour in humans 5 matic brain pathologies have been associated with Department of Psychological and animals. These developments have occurred at Sciences, University of the development of apathy, while it is also a compo- Connecticut, Storrs, Connecticut, several different conceptual levels, from work linking nent of the negative symptoms of schizophrenia USA neural structures and neuromodulatory systems to and anhedonia associated with major depressive 6Division of Clinical Neurology, specific aspects of motivated behaviour, to higher order disorder. It can be the first clinical marker of a John Radcliffe Hospital, Oxford computational models that aim to unite these findings University Hospitals Trust, developing condition, as in Parkinson’s disease within frameworks for normal goal-directed behaviour. Oxford, UK (PD), and in some conditions (eg, Huntington’s 7W ellcome Trust Centre for In this review we develop a conceptual framework for disease) apathy has been shown to closely track copyright. Integrative Neuroimaging, understanding pathological apathy based on this current disease progression (s2). Importantly, its presence Oxford, UK understanding of normal motivated behaviour. We first is associated with worsened quality of life for both introduce prominent theories of motivated behaviour— Correspondence to which often involves sequences of actions towards a patients and their families/caregivers, highlighting Dr Campbell Le Heron, New 3 4 goal that needs to be maintained across time. Next, the clinical significance of this syndrome. Indeed, Zealand Brain Research the presence of apathy may negate the otherwise Institute, Christchurch 8011, we outline the behavioural effects of disrupting these New Zealand; campbell. processes in animal models, highlighting the specific positive effects of interventions targeting other leheron@ ndcn. ox. ac. uk aspects of disease, such as deep brain stimulation effects of these manipulations on different components 5 of motivated behaviour. Finally, we relate these findings for the motor symptoms of PD. Received 10 July 2018 1 to clinical apathy, demonstrating the homologies Since the work of both Marin and Levy and Revised 13 September 2018 2 Accepted 24 September 2018 between this basic neuroscience work and emerging Dubois, apathy has generally been considered behavioural and physiological evidence from patient as divisible into three core components, each of http://jnnp.bmj.com/ studies of this syndrome. which could contribute to (or be the manifestation of) reduced goal-directed behaviour/motivation. These are an affective/emotional component, a behavioural activation component and a cogni- INTRODUCTION tive component. Furthermore, Levy and Dubois2 The importance of outcomes for motivating proposed that these components may relate to behaviour has long been recognised. Philosopher disruption of distinct frontal cortex-basal ganglia on September 26, 2021 by guest. Protected and physician John Locke ascribed a crucial role circuits. Many questionnaires used to assess apathy for reinforcers (pleasure and pain) for motivating include subscales that purport to map onto these actions, writing that without these perceptions separate components.6 This approach has undoubt- … we should have no reason to prefer one thought edly been important in advancing understanding or action to another … and so we should neither of the apathetic syndrome. However it remains © Author(s) (or their stir our bodies, nor employ our minds, but let our unclear how these components map onto under- employer(s)) 2018. Re-use thoughts (if I may so call it) run adrift … In which lying normal neurobiological systems, the disrup- permitted under CC BY. state man … would be a very idle, inactive creature, tion of which are the presumed underlying drivers Published by BMJ. and pass his time only in a lazy lethargic dream. (s1) of apathy in the first place.7 Furthermore these To cite: Le Heron C, Holroyd This description resonates with much of the components have not been extensively studied in CB, Salamone J, et al. J phenotype of apathy, a neuropsychiatric syndrome humans or animal models. Therefore in this review Neurol Neurosurg Psychiatry Epub ahead of print: [please conceptualised as a loss of motivation that mani- we prefer to develop a framework for apathy based 1 2 include Day Month Year]. fests in reduced goal-directed behaviour —see on current understanding of the processes under- doi:10.1136/jnnp-2018- box 1 for key definitions. Other terms often used lying normal motivated behaviour—processes we 318265 to describe this syndrome include abulia, akinetic review in more detail below. Le Heron C, et al. J Neurol Neurosurg Psychiatry 2018;0:1–11. doi:10.1136/jnnp-2018-318265 1 Cognitive neurology J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp-2018-318265 on 26 October 2018. Downloaded from B ox 1 Key terms and abbreviations B ox 2 Transcript of an interview with a patient with significant apathy in the context of cerebral small vessel ► Apathy: a syndrome of impaired motivation and consequent disease reduced goal-directed behaviour. ► Motivation: a construct that encompasses the reasons and Doctor: “If I was a fly on the wall watching you at home, what processes underlying behaviour directed towards or away would I see you doing?” from environmental stimuli. Patient: “I suppose sitting, watching television which drives him ► Goal-directed behaviour: actions towards an outcome, in mad, … (pauses) …, I did use to book-read but I don’t seem which the current outcome value for the organisms, as well to be doing that much these days. Um, and that’s basically it, as the costs associated with the action, are accounted for. really.” ► Habitual behaviour: actions that occur in response to a Doctor: “So watching the television?” (Patient nods). “Anything particular stimulus, without explicit reference to the outcome else?” or costs of the action. Such ‘stimulus-response’ systems are Patient: “I can’t think of anything, really.” shaped by learning systems which compute whether an Doctor: “In the past, would that have been you?” action results in a better or worse than predicted outcome, Patient: “No”. making the same action more or less likely to be repeated on Doctor: “What would we have seen if we had been a fly on the subsequent exposure to the stimulus. wall a few years back?” ► Reward: this term has a clear meaning when used as a noun Patient: “Me buzzing around, doing things, going out shopping, (ie, food reward) or a verb referring to actions (to reward coming back, you know, being busy all the time. And I’ve just someone). However, when used as a neurobehavioural slowed down and more or less come to a halt. I just don’t know process, this term has no standard usage and can be quite what is stopping me really.” ambiguous. In some contexts, it is used as a synonym for Doctor: “You said you used to enjoy reading. So what’s stopping pleasure. In others, it is used as a synonym for reinforcement. you reading?” Thus, overuse of the term reward can be confusing. In this Patient: “Absolutely nothing. It’s just that I can’t be bothered I paper, when used, reward refers to a reinforcer. suppose. It’s easier to watch a screen than read a book. I keep ► Reinforcer: the positive (reward) or negative (punishment) threatening to pick up a book but I just don’t get there.” outcome of an action that informs goal-directed behaviour Doctor: “What else did you use to do in the past? You said you and also shapes subsequent habitual behaviours. used to run the house?” ► Effort: physical or mental work or activity done to achieve a Patient: “I used to sew. I used to sew all my daughter’s clothing. particular end or goal; vigorous exertion of power. Knit. But, it seems to all have gone … I don’t do any of that now copyright. ► Instrumental: the phase of motivated behaviour during and I don’t know why.” which an organism is approaching a motivational stimulus Doctor: “Would you like to?” or behaving so as to deliver that stimulus or increase its Patient: (pauses) … “Umm.
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