Hearing and Dementia

J Neurol (2016) 263:2339–2354 DOI 10.1007/s00415-016-8208-y NEUROLOGICAL UPDATE Hearing and dementia 1 1 1 1 Chris J. D. Hardy • Charles R. Marshall • Hannah L. Golden • Camilla N. Clark • 1,4 5,6 2,3,6 Catherine J. Mummery • Timothy D. Griffiths • Doris-Eva Bamiou • Jason D. Warren1,6 Received: 27 April 2016 / Revised: 13 June 2016 / Accepted: 14 June 2016 / Published online: 2 July 2016 Ó The Author(s) 2016. This article is published with open access at Springerlink.com Abstract Hearing deficits associated with cognitive and conclude with a bedside approach to assessing and impairment have attracted much recent interest, motivated managing auditory dysfunction in dementia. by emerging evidence that impaired hearing is a risk factor for cognitive decline. However, dementia and hearing Keywords Hearing Á Auditory Á Dementia Á Alzheimer’s impairment present immense challenges in their own right, disease Á Frontotemporal dementia Á Progressive aphasia Á and their intersection in the auditory brain remains poorly Lewy body disease understood and difficult to assess. Here, we outline a clinically oriented, symptom-based approach to the assessment of hearing in dementias, informed by recent Introduction progress in the clinical auditory neuroscience of these diseases. We consider the significance and interpretation of Although hearing impairment is not generally regarded hearing loss and symptoms that point to a disorder of as a cardinal feature of dementia, hearing in patients auditory cognition in patients with dementia. We identify with dementia is a focus of growing clinical interest. key auditory characteristics of some important dementias Recent evidence suggests that hearing loss may predict or accelerate cognitive deterioration [1–3], and alterations of hearing may manifest as complex cognitive and behavioural symptoms relevant to the differential diag- nosis of dementias [4–10]. Interventions targeting auditory processes (most notably, music) have gained wide currency [4, 11]. However, the organisation of the & Jason D. Warren human auditory brain is complex and incompletely [email protected] understood. Moreover, neuropsychological frameworks 1 Department of Neurodegenerative Disease, Dementia for characterising hearing disorders produced by brain Research Centre, UCL Institute of Neurology, University disease and practical tools for assessing auditory func- College London, Queen Square, London WC1N 3BG, UK tions suitable for use in cognitively impaired patients are 2 Department of Neuro-otology, National Hospital for often lacking. Neurology and Neurosurgery, Queen Square, London, UK In this review, we outline a clinically oriented, symp- 3 UCL Ear Institute, University College London, London, UK tom-based approach to hearing in dementia, informed by recent progress in the clinical auditory neuroscience of 4 Cognitive Disorders Clinic for the Deaf, National Hospital for Neurology and Neurosurgery, Queen Square, London, UK these diseases. We consider the problem of hearing loss (impaired detection of sound and how this interacts with 5 Auditory Group, Institute of Neuroscience, The Medical School, University of Newcastle upon Tyne, cognitive function) and symptoms that point to a disorder Newcastle upon Tyne, UK of auditory cognition (impaired understanding or beha- 6 Central Auditory Disorders Clinic, National Hospital for vioural responses to sound). We identify key auditory Neurology and Neurosurgery, Queen Square, London, UK characteristics of some important dementias. We conclude 123 2340 J Neurol (2016) 263:2339–2354 with a bedside approach to assessing and managing audi- [15]. However, ‘dementia’ designates a syndrome of tory dysfunction in dementia. acquired, progressive, socially and/or occupationally significant cognitive and/or behavioural decline: this defini- tion embraces over a hundred highly diverse diseases, the The auditory brain and dementia most common of which is Alzheimer’s disease (AD) [4, 16–18]. Here, we focus on major neurodegenerative Neuropsychology of hearing causes of dementia in mid to later life, collectively char- acterised by pathogenic protein spread over large-scale Hearing (considered broadly as the function of the human cerebral networks and distinctive profiles of regional brain auditory brain and its peripheral end organs) has been atrophy and clinical deficits (summarised in Table 2). aligned with other complex neuropsychological processes Brain networks targeted by these diseases overlap the based on studies of the normal brain and focal brain temporal, parietal, frontal, and subcortical circuitry that damage [12, 13]. Together, this evidence suggests a hier- supports auditory cognition (Tables 1, 2): this is key to archical organisation that differentiates categories and anticipating and understanding the disorders of hearing that stages of auditory information processing (Table 1). Pro- accompany particular dementia syndromes. cessing of sound begins in the ascending auditory pathways extending from cochlea to primary auditory cortex in Heschl’s gyrus: this is not a passive relay but involves Hearing loss and dementia considerable signal transformation [12]. While the termi- nology of hearing disorders is problematic, in consideration Epidemiological evidence of disease associations, it is useful to attempt to distinguish between peripheral (predominantly cochlear or auditory Significant hearing loss (operationally, [20 dB elevation nerve), subcortical (ascending auditory pathway), and of threshold for pure tone detection) affects around 40 % cortical auditory dysfunction. Auditory cognition—pro- of those aged over 65 [19] and has important links to cessing beyond sound detection leading to auditory per- cognitive impairment and dementia. Age-related hearing ception and understanding—is mediated by distributed loss (presbycusis) commonly results from cochlear dys- networks involving auditory cortex and its cerebral con- function, though age-related alterations in more central nections; disorders affecting these networks produce auditory pathways may also be relevant and have proba- characteristic symptoms and syndromes of auditory cog- bly been under-recognised [20]. The balance of epidemi- nitive dysfunction (summarised in Table 1). ological evidence across populations suggests that hearing As a framework for analysing disorders of auditory loss is associated with cognitive decline and constitutes a cognition, it is useful to consider complex sounds (speech, risk factor for development of dementia in older adults, voices, music, and environmental noises) as ‘auditory though the strength of this association is somewhat vari- objects’ that must be disambiguated from the auditory able [20, 21]. One meta-analysis concluded that cognitive background and organised into coherent perceptual repre- and hearing impairment are correlated and that hearing sentations [13]. The processing of such sound objects loss impacts on multiple domains of cognition [21]; this is entails perceptual analysis (encoding of acoustic features, not simply attributable to hearing loss confounding such as pitch, rhythm, and timbre) leading to semantic speech-based cognitive tasks [20] and has been observed processing (extraction of associated meaning, leading to in those with and without dementia [22]. Hearing sound recognition) [13, 14]. In the world at large, sounds loss *25 dB has an effect on cognitive deterioration are embedded in auditory scenes that must be actively equivalent to around 7 years of ageing [1] and risk of deconstructed to identify and track sounds of interest [10]: dementia increases with increasing severity of hearing this, in turn, requires the representation of sound location impairment [2]. and movement (auditory spatial analysis) and abstraction of identifying sound characteristics under varying listening The role of peripheral hearing conditions (auditory apperceptive processing). Many sounds also have emotional and behavioural relevance. While the association between hearing loss and cognitive decline appears robust, the mechanism remains unre- The burden of dementia solved. Hearing impairment might accelerate cognitive decline by compounding sensory and social isolation, Dementia is arguably the most significant public health increasing cognitive load, and thereby exhausting com- problem confronting ageing societies, with an estimated pensatory cognitive reallocation, or constitute a non- 800,000 sufferers currently in the United Kingdom alone specific marker of frailty [20]. However, the association 123 J Neurol (2016) 263:2339–2354 2341 Table 1 An outline of core operations in auditory cognition and their clinical and neuroanatomical correlates Auditory Clinical correlates Neuropsychological Procedurea Neuroanatomical cognitive tests correlates [13, 82] operation Feature detection Cortical deafnessb, Sound detection Detection of any sound (e.g., tone) behaviourally/EP [83] PAC, lat HG, PT, c tinnitus Gap-in-noise detection Detection of short silent interval in white noise burst [76] pSTG, subcortical circuits AM/FMd detection Detection of modulation (vibrato) of intensity/pitch in carrier Spatial lateralisation tone [76] Detection of right-left sound shift based on inter-aural phase/ intensity cues [76] Feature analysis Word deafnesse, Phoneme Discrimination of sound pairs/sequences differing in pitch, lat HG, pSTG/STS, dystimbriaf, amusiag discrimination temporal or timbral characteristics [49, 79, 84] aSTG, subcortical MBEA pitch/temporal Labelling of features in a single

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