Introduction
The auditory brain and dementia
Neuropsychology of hearing
Auditory cognitive operation | Clinical correlates | Neuropsychological tests | Procedurea
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Feature detection | Cortical deafnessb, tinnitusc
| Sound detection Gap-in-noise detection AM/FMd detection Spatial lateralisation | Detection of any sound (e.g., tone) behaviourally/EP [83] Detection of short silent interval in white noise burst [76] Detection of modulation (vibrato) of intensity/pitch in carrier tone [76] Detection of right-left sound shift based on inter-aural phase/intensity cues [76] | PAC, lat HG, PT, pSTG, subcortical circuits |
Feature analysis | Word deafnesse, dystimbriaf, amusiag
| Phoneme discrimination MBEA pitch/temporal subtests | Discrimination of sound pairs/sequences differing in pitch, temporal or timbral characteristics [49, 79, 84] Labelling of features in a single sound (e.g., tone glide direction ‘up’ or ‘down’) [7] | lat HG, pSTG/STS, aSTG, subcortical circuits |
Scene analysis | Auditory disorientation | SSI-ICM Speech-in-noiseh
Spatial localisation Dichotic listening | Identification of a sentence spoken over background message same ear [34] Identification of words against background noise/multi-talker babble Attention to one of two stimuli played simultaneously via each ear [23] | PT/pSTG, IPL, PFC, hippocampus, subcortical circuitsi
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Object representation (apperceptive processing) | Auditory apperceptive agnosias, musical and verbal hallucinations | Melody discrimination Distorted melodies Voice discrimination Accent processing | Identification of an altered familiar melody [85] Discrimination of (unfamiliar) speakers [57] | PT, pSTG/STS, IPL, aSTG |
Object recognition (semantic processing) | Auditory associative agnosias (including phonagnosia) | Environmental sound, melody, voice recognition | Recognition of familiar sounds, tunes, voices; conventionally assessed by naming the target but can be assessed by forced-choice or matching cross-modally (e.g., sound–picture) [56] or within-modality (perceptually dissimilar sound excerpts, categorisation based on semantic characteristic) [7, 49, 54, 55], familiarity decision [56] in patients with aphasia | aSTG, TP, insula |
Emotional valuation | Receptive dysprosodia, auditory anhedonia, Musicophilia | Emotion recognition Emotional response | Behavioural rating of valence, arousal; autonomic indices [68] | MTL, insula, OFC, ACC, mesolimbic/striatal circuits |
Working memory/attentionj
| Auditory neglect/inattention | Compare sequential sounds Oddball detection Dichotic listening |
n-back tasks (e.g., [77]) Sustained attention with detection of target deviants behaviourally/EP [87] Attention to one of two stimuli played simultaneously via each ear [75] | Fronto–parieto–temporal, subcortical circuits |
The burden of dementia
Disease/syndrome | Core clinical phenotype | Key auditory symptoms | Auditory cognitive processesa
| Pathological neuroanatomyb
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Perc | App | Sem | Em | Wm/Att | ||||
Episodic, topographical memory loss, parietal deficits | Difficulty tracking sound objects and information in busy acoustic environments, auditory disorientation, increased sound sensitivity |
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| PCC, precuneus, temporo-parietal cortices | |
PCA
c [9] | Visuo-perceptual, visuo-spatial, other parietal deficits |
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Anomia, phonemic and verbal working memory deficits | − |
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Fluctuating executive, attentional deficits, bradyphrenia, visual hallucinations, parkinsonism | Auditory hallucinations |
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| Cortico–subcortical circuits | |||
FTLD: sporadic/undefined | ||||||||
Socio-emotional, executive dysfunction with disinhibition, apathy, obsessionality, other behavioural abnormalities | Sound aversion, phonagnosia, altered attentive processing of auditory stimuli | − | − |
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| Auditory and multimodal association cortex in ant TL, OFC, insula, ACC, striatal circuits | |
Vocabulary loss, visual agnosia due to impaired semantic memory, behavioural changes similar to bvFTD | Musicophilia, tinnitus; phonagnosia/nonverbal sound agnosia | − |
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| − | Auditory/multimodal association cortex in ant TL, OFC, insula | |
Speech production deficits, agrammatism | Agnosia for environmental sounds, accents, word deafness |
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| Peri-Sylvian networks | |
FTLD: genetic | ||||||||
Similar bvFTD, may have associated parkinsonism | Altered hedonic responses to sound |
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| Ant TL/fronto–subcortical network | |||
Similar bvFTD or PNFA, may have associated motor neuron features | Auditory hallucinations | − |
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| Cortico–thalamo–cerebellar network | ||
Similar bvFTD or mixed aphasia, often prominent parietal signs | Limited information |
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| − | − |
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| Distributed intra-hemispheric networks | |
Executive deficits, bradyphrenia in context parkinsonism, supranuclear gaze palsy, limb dystonia – apraxia | Agnosia for environmental sounds, disordered voice emotion processing | − |
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| Cortico–subcortical circuits, IFG | |||
Executive and behavioural changes with chorea | Attentive processing of auditory stimuli |
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| Cortico–subcortical circuits | ||||
Usually rapid global dementia with prominent myoclonus, ataxia; wide phenotypic variation (especially genetic forms) | Occasionally tinnitus, cortical deafness, auditory hallucinations, increased sound sensitivity |
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| Primary auditory cortex |
Hearing loss and dementia
Epidemiological evidence
The role of peripheral hearing
The role of ‘central’ auditory processing
Syndromes of dementia and hearing loss
Disease | Aud | Cogn | Associated features | Diagnostic investigations |
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Inflammatory | ||||
Antiphospholipid syndrome [108] | F; C, RCa
| F | Headache, seizures, chorea, myelopathy, optic neuritis, vestibulopathy | Antibody profile with compatible clinical phenotype |
Multiple sclerosis [109] | U; RCa
| Fb
| Diverse: vertigo, optic neuritis, various brainstem, cerebral, spinal signs | Compatible clinical and MRI features of CNS demyelination, (McDonald criteria), supported by CSF unmatched oligoclonal bands |
Neuro-Behçet’s [110] | F; RCa
| Uc
| Vestibulopathy, uveitis, headache, brainstem signs, hemiparesis, cerebral venous thrombosis; oral/genital ulcers | None specifically; International Study Group criteria (with pathergy test) for systemic disease |
Neurosarcoidosis [111] | U; RCa
| F | Vestibulopathy, cranial nerve palsies, seizures, aseptic meningitis, myelopathy, peripheral neuropathy, pituitary dysfunction | Contrast MRI sensitive but not specific; whole body PET, biopsy involved peripheral tissue |
Susac’s syndrome [112] | T; Ca,d
| T | Retinal artery occlusions; migraine, ataxia, vertigo, long tract signs | MRI (callosal ‘snowball’ lesions); retinal fluoroscein angiography (multifocal distal arteriolar occlusions) |
Infectious | ||||
Cryptococcal meningitis [113] | U; RCa
| F | Headache, papilloedema, seizures, vestibulopathy, cranial nerve palsies; more common in immunocompromised patients | CSF Cryptococcal antigen |
Neuroborreliosis [114] | U; RCe
| Uf
| Lymphocytic meningitis with cranial palsies, vestibulopathy | Lyme serology |
Neurosyphilis [115] | U; RCa,g
| T | Chorioretinitis, Argyll Robertson pupils, vestibulopathy, cranial nerve palsies and brainstem signs, myelopathy (tabes dorsalis), brain infarcts | Treponemal serology (blood and CSF) |
Genetic | ||||
CADASIL [116] | U; Ca
| T | Migraine, stroke, psychiatric disturbance | Characteristic MRI with marked anterior temporal/external capsule white matter involvement Notch3 mutations |
MELAS/other mitochondrial syndromes [117] | T/F; C | T/F | Migraine, seizures, stroke-like episodes, ophthalmoplegia, myopathy, lactic acidosis, diabetes mellitus | Various mitochondrial DNA mutations |
HSAN IE [118] | T; C, RC?h
| T | Sensory and autonomic neuropathy, optic neuropathy, narcolepsy |
DNMT1 mutations |
IBMPFD [119] | U; RC? | T | Frontotemporal dementia with inclusion body myositis, Paget’s disease of bone |
VCP mutations |
Niemann-Pick type C [120] | F; RC | Tc
| Ataxia, supranuclear gaze palsy, dystonia, psychiatric features, cataplexy, seizures, splenomegaly | Skin fibroblast studies (accumulation of unesterified cholesterol), genotyping |
Oculo-leptomeningeal amyloidosis [121] | F; RC?a
| F | Seizures, stroke-like episodes, headache, ataxia, myelo-radiculopathy, subarachnoid haemorrhage, ocular amyloid | Abnormal meningeal enhancement on contrast MRI Transthyretin mutations |
Refsum disease [122] | F; RC | U | Retinitis pigmentosa, anosmia, polyneuropathy | Raised plasma phytanic acid
PHYH mutation |
Spinocerebellar ataxias: [83] | F; C, RCi
| F | Truncal/limb ataxia, bulbar deficits, proprioceptive impairment, neuropathy, variably prominent across group | Various mutations (most frequently, trinucleotide repeat expansions) |
Friedreich’s ataxia [123] | Cardiomyopathy, diabetes mellitus (adult onset milder) |
FXN expansions | ||
SCA13 [124] | Gait/limb ataxia, dysarthria, hyperreflexia, vibration sense loss |
KCNC3 mutations | ||
Wolfram’s syndrome [125] | T; RC | Fj
| Optic atrophy, diabetes |
WFS1 mutations |
Other | ||||
Prion diseases [126] | U; RC | T | Rapid neurological decline, often with prominent myoclonus and ataxia | Increased cortical/basal ganglia signal on DWI/FLAIR MRI with compatible clinical phenotype; rarely prion gene mutation (E200K) |
Superficial siderosis [127] | T; RCk
| F | Cerebellar ataxia, pyramidal signs, bladder dysfunction, anosmia, anisocoria; may have history compatible with chronic subarachnoid bleeding | Haemosiderin rimming brain/spinal cord on susceptibility-weighted MRI |
Symptoms of altered auditory cognition in dementia
Impaired perception of sound features
Impaired perception of auditory scenes and objects
Impaired recognition of sounds
Auditory hallucinations
Abnormal auditory behaviours
A practical approach to the patient with dementia and altered hearing
Domain | Question | Key process probed | Significance |
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Background | Previous occupation? | Previous cognitive/auditory function, noise exposure | Correct interpretation of hearing tests |
Previous level of musical training and interest, early language development and education? | Prior auditory expertise | Correct interpretation of hearing tests | |
Course | When was hearing impairment first noticed? | Duration of impairment (relative to cognitive decline) | Nature of underlying disease process |
Has this deteriorated, fluctuated or improved since onset? | Tempo of impairment | Nature of underlying disease process | |
Symptoms | |||
Sound detection | Is there a lack of reaction to sounds? | Impaired sound detection | May signify deafness (any cause) |
Is there a tendency to turn up the volume of radio or TV or to ask people to speak louder? | Impaired sound detection | May signify deafness (any cause) | |
Is there a complaint that increasing volume makes sounds suddenly seem too loud? | Impaired sound detection | May signify cochlear pathology (‘loudness recruitment’) | |
Abnormal auditory perception: deficient | Is there particular difficulty following conversations in background noise or over a noisy telephone line? | Auditory scene analysis | May signify a cerebral disorder (e.g., Alzheimer’s disease) in absence of significant hearing loss |
Is there difficulty locating sounds (e.g., an alarm or mobile, a person speaking in same the room)? | Auditory scene analysis | May signify a cerebral disorder in absence of significant hearing loss | |
Is there particular difficulty understanding speech versus other sounds? | Feature analysis | May signify word deafness | |
Is there more difficulty understanding less familiar accents? | Apperceptive processing | May signify a cerebral disorder in absence of significant hearing loss | |
Is there more difficulty understanding a person’s tone of voice (e.g., angry or upset)? | Apperceptive and emotional processing | May signify a frontotemporal dementia in appropriate context | |
Has there been any problem recognising familiar voices, music or other sounds? | Semantic processing | May signify auditory agnosia or semantic dementia, in appropriate context | |
Abnormal auditory perception: excessive | Is there a persistent complaint of buzzing or ringing in the ears? | Tinnitus | May be peripheral or central in origin |
Are other sounds ever heard when no sounds are present? | Formed hallucinations | May signify Lewy body disease, in appropriate context | |
Abnormal auditory behaviour | Is there intolerance to moderately loud sounds or particular sounds? | Hyperacusis | May signify a frontotemporal dementia in appropriate context |
Has there been any change in liking for or interest in music or other sounds? | Auditory hedonic processing | May signify a frontotemporal dementia in appropriate context |