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Title: a Review of the Perceptual and Attentional-Executive Characteristics of Dementia with Lewy Bodies Relative to Alzheimer A

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Title: a Review of the Perceptual and Attentional-Executive Characteristics of Dementia with Lewy Bodies Relative to Alzheimer A Title: A review of the perceptual and attentional-executive characteristics of dementia with Lewy bodies relative to Alzheimer’s and Parkinson’s disease Authors: Lauren Revie 1, Anthony Bayer 2, Christoph Teufel1, Claudia Metzler-Baddeley1 Affiliation: 1Cardiff University Brain Research Imaging Centre, School of Psychology, Cardiff University, Maindy Road, Cardiff, CF24 4HQ 2University Hospital Llandough, Penlan Road, Penarth, Cardiff, CF64 2XX Corresponding author: Lauren Revie Cardiff University Brain Research Imaging Centre (CUBRIC) Maindy Road Cardiff Wales United Kingdom CF24 4HQ [email protected] Declaration of interest: The authors have no declaration of interest to declare. Funding: This work was funded by the School of Psychology Open Competition Studentship, Cardiff University, awarded to LR as part of a doctoral programme of study. 1 Abstract Dementia with Lewy bodies (DLB) is the second most prevalent neurodegenerative dementia disorder, after Alzheimer’s disease (AD). DLB is characterised clinically by cognitive fluctuations, visual hallucinations, rapid-eye-movement sleep behaviour disorder, and Parkinsonism. Differentiating DLB from AD and related disorders of Parkinson’s disease (PD) and Parkinson’s disease with dementia (PDD) can be difficult at early disease stages due to overlapping clinical and pathological features. Nevertheless, it has been shown that visuoperceptual, attention and executive deficits, relative to memory impairments, are especially prominent in the early stages of DLB compared with AD or PD. The importance of these impairments is reflected in the recent revision of the diagnostic consensus guidelines of DLB. As the last reviews of cognitive impairments in DLB were conducted over a decade ago (Collerton, Burn, McKeith & O’Brien, 2003; Metzler-Baddeley, 2007; Ralph, 2001), we provide an up-to-date review of the literature into perceptual and attention- executive functions in DLB. There is a need for better controlled studies into cognitive deficits, their neural correlates, and relationships to clinical symptoms in DLB, that go beyond standard clinical assessments. Evidence regarding visuoperception suggests that low-level functions may be relatively preserved while mid- and higher-level functions, that require the recruitment of attention and executive functions are disproportionally affected in DLB. Cognitive fluctuations and visual hallucinations may arise from a desynchronization of top-down attention and bottom-up sensory networks. Keywords: dementia with Lewy bodies, perception, attention, executive, memory, Lewy body disease, Alzheimer’s disease, Parkinson’s disease 2 INTRODUCTION Dementia with Lewy bodies (DLB) is the second most prevalent form of neurodegenerative dementia after Alzheimer’s disease (AD). Its mean prevalence in clinical (secondary care) dementia populations is 7.5% (Vann Jones & O’Brien, 2014). In the most recent consensus criteria, DLB is characterised by four core clinical features (McKeith et al., 2017). First, cognitive fluctuations which occur in up to 90% of patients and are characterised by variabilities in their level of arousal and cognitive performance. This ranges from episodes of stupor and confusion, to periods of alertness and responsiveness (O’Dowd et al., 2019). Second, complex visual hallucinations, which occur in up to 80% of patients, and typically consist of perception of people, animals and objects, motion, and scenery that are not present (Onofrj et al., 2013). Complex hallucinations in DLB are commonly associated with apathy and anxiety and are typically reported by patients as being unpleasant experiences (Mosimann et al., 2006). The third core symptom in DLB is Parkinsonism, which involves disordered movement such as shuffling gait and rigidity. Finally, the fourth core symptom in DLB is rapid-eye-movement sleep behaviour disorder (RBD), involving the violent ‘acting’ of dreams, and prominent movement and speech during sleep (Ferman et al., 2011). Features which must also be present for a diagnosis of DLB include: a progressive cognitive decline of sufficient magnitude to impact on daily life, and impairment on tests of visuoperceptual, attentional and executive functioning in early disease stages (McKeith et al., 2017). Moreover, with the progression of the disease, memory impairments also become more prominent. Patients with DLB have pathological inclusions in neurons in the neocortex, midbrain and limbic system that are called ‘Lewy bodies.’ These inclusions consist of ubiquitinated, misfolded α- synuclein, and are also characteristic features of Parkinson’s disease (PD), and Parkinson’s disease with dementia (PDD). Together, these three disorders form the ‘Lewy body spectrum’ (Kövari, Horvath, & Bouras, 2009). The location of the deposition of Lewy bodies in the brain is closely 3 associated with the presentation of Lewy body disease symptoms. For instance, PD patients present mainly with brainstem and midbrain Lewy body pathology, which co-occurs with clinical motor symptoms. With the progression of PD, patients may go on to develop significant cognitive impairments resulting in PDD, which is associated with the spread of Lewy body pathology to the neocortex (Braak et al., 2003). In fact, the clinical phenotypes of PDD and DLB are very similar, and the only diagnostic difference at present is the chronology of the onset of motor symptoms within a 12-month period (Jellinger & Korczyn, 2018; McKeith et al., 2017). Despite consensus guidelines which specify the symptom profile of DLB (McKeith et al., 2017) and availability of assessment toolkits to aid diagnosis (Thomas et al., 2018a), DLB is clinically under- diagnosed, as evidenced by a persisting disparity between in-vivo and post-mortem diagnosis rates (; Arnaoutoglou, O’Brien, & Underwood, 2019, McKeith et al., 2000). Due to the presentation of cognitive and memory impairments, DLB patients can be misdiagnosed as having Alzheimer’s disease (AD; Hohl, Tiraboschi, Hansen, Thal, & Corey-Bloom, 2000) and DLB and AD pathology often co-occur (Thomas et al., 2018b). Moreover, a differential diagnosis between DLB and PDD due to concurrent presentation with both motor and cognitive symptoms can also be challenging (Hely et al., 2008). These issues have important implications for management. Cholinesterase inhibitor treatment is more effective in DLB than AD (Aarsland, Mosimann, & McKeith, 2004; Noufi, Khoury, Jeyakumar, & Grossberg, 2019). Furthermore, it is more beneficial in treating DLB symptoms than typical dopaminergic treatment that may be prescribed due to misdiagnosis as PDD, or PD, but will only produce a motor response in about one third of DLB patients (Molloy et al., 2005). Most importantly, DLB patients exhibit severe adverse reactions to antipsychotic medication that may be prescribed for the management of psychiatric symptoms in AD patients. Thus, an accurate early diagnosis is helpful for appropriate disease management and treatment to maintain the patients’ quality of life. In addition, recent research has indicated that individuals who receive a later diagnosis of DLB tend to present with symptoms which may not be initially associated with DLB, such as 4 amnestic presentation, which was linked to lower survival probability (Moylett et al. 2019). In the future, the emergence of disease-modifying drugs will demand the identification of specific pathology so that treatments can be targeted appropriately. Previous literature reviews have summarised research on the cognitive profile of DLB (Collerton, Burn, McKeith, & O’Brien, 2003; Metzler-Baddeley, 2007; Ralph, 2001). As described above the most prominent cognitive impairments in DLB, especially at early stages, occur in the visuoperceptual, attention and executive domain. The recent revision of the DLB consensus guidelines for diagnosis has emphasised the importance of a detailed assessment and understanding of the nature of these cognitive deficits to aid differential diagnosis of DLB from AD and PDD (McKeith et al., 2017). As previous reviews were published over ten years ago (Collerton, Burn, McKeith, & O’Brien, 2003; Metzler-Baddeley, 2007; Simard, 2000), an up-to-date perspective on the cognitive profile in DLB is therefore timely. Much of the work concerning DLB in recent years has focused on pathology (Kon, Tomiyama, & Wakabayashi, 2019), genetics (Orme, Guerreiro, & Bras, 2018), determining prodromal or early stage biomarkers (Cagnin et al., 2013; Donaghy & McKeith, 2014; Fujishiro et al., 2013; Outeiro et al., 2019), and both pharmacological (Hershey & Coleman-Jackson, 2019) and non-pharmacological interventions (Connors et al., 2018). Some neuroimaging evidence regarding structural and functional differences in DLB also exist, which largely align with the previously established supportive features of DLB, such as a link between visual impairments and occipital hypo-metabolism (Perneczky et al., 2008). These aspects have been reviewed recently by others (Mak, Su, Williams, & O’Brien, 2014; Watson, Blamire, & O’Brien, 2009; Yousaf, Dervenoulas, Valkimadi, & Politis, 2019). Papers have been also published by Aarsland, (2016) and Jurek et al., (2018) which provide readers with an up to date and detailed summary of the clinical symptom profile in DLB. In addition, a recent systematic review by Eversfield & Orton (2018) discussed hallucination prevalence in DLB. 5 Methods This review focused on studies into visuoperceptual, attentional and executive impairments, as these are the most prominent cognitive features
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