The functional neuroanatomy of musical memory in Alzheimer's disease

Catherine F Slattery,Jennifer L Agustus,Ross W Paterson,Oliver Mccallion,Alexander J.M Foulkes,Kirsty Macpherson,Amelia M Carton,Emma Harding,Hannah L Golden,Kankamol Jaisin,Catherine J Mummery,Jonathan M Schott,Jason D Warren

doi:10.1016/j.cortex.2019.02.003

Abstract

BackgroundMemory for music has attracted much recent interest in Alzheimer's disease but the underlying brain mechanisms have not been defined in patients directly. Here we addressed this issue in an Alzheimer's disease cohort using activation fMRI of two core musical memory systems. MethodsWe studied 34 patients with younger onset Alzheimer's disease led either by episodic memory decline (typical Alzheimer's disease) or by visuospatial impairment (posterior cortical atrophy) in relation to 19 age-matched healthy individuals. We designed a novel fMRI paradigm based on passive listening to melodies that were either previously familiar or unfamiliar (musical semantic memory) and either presented singly or repeated (incidental musical episodic memory). ResultsBoth syndromic groups showed significant functional neuroanatomical alterations relative to the healthy control group. For musical semantic memory, disease-associated activation group differences were localised to right inferior frontal cortex (reduced activation in the group with memory-led Alzheimer's disease); while for incidental musical episodic memory, disease-associated activation group differences were localised to precuneus and posterior cingulate cortex (abnormally enhanced activation in the syndromic groups). In post-scan behavioural testing, both patient groups had a deficit of musical episodic memory relative to healthy controls whereas musical semantic memory was unimpaired. ConclusionsOur findings define functional neuroanatomical substrates for the differential involvement of musical semantic and incidental episodic memory in major phenotypes of Alzheimer's disease. The complex dynamic profile of brain activation group differences observed suggests that musical memory may be an informative probe of neural network function in Alzheimer's disease. These findings may guide the development of future musical interventions in dementia.

Highlights

Despite considerable interest, the neural mechanisms underlying musical memory in Alzheimer's disease (AD) remain contentious
Twenty-four patients presented with an amnestic clinical syndrome of mAD (Dubois et al, 2014) and 10 patients presented with a syndrome meeting research criteria for posterior cortical atrophy (PCA) (Tang-Wai et al, 2004)
The patient groups did not differ significantly in symptom duration, but the mAD group had lower mean Mini-Mental State Examination score than the PCA group (p 1⁄4 .04). These syndromic groups showed the anticipated profiles of multi-domain cognitive impairment: relative to published norms, patients with mAD had deficits of verbal episodic memory, naming, arithmetic, visual processing and executive function while patients with PCA had markedly impaired visuoperceptual and visuospatial skills but relatively preserved episodic memory and verbal skills; comparing syndromic groups, the mAD group had significantly worse verbal episodic memory performance than the PCA group, and the PCA group had significantly worse visuoperceptual skills than the mAD group

Summary

Introduction

The neural mechanisms underlying musical memory in Alzheimer's disease (AD) remain contentious. The processing of unfamiliarity (novelty) in music and other sensory stimuli activates a distributed network of brain areas overlapping those implicated in musical semantic and episodic memory, including mesial temporal lobes and temporoparietal, inferior frontal, insula and anterior cingulate cortices (Downar, Crawley, Mikulis & Davis, 2002; Herdener et al, 2010; Hunkin et al, 2002). This emerging picture of the functional neuroanatomy of musical memory aligns with neuroanatomical and neuropathological studies of AD pathogenesis. The complex dynamic profile of brain activation group differences observed suggests that musical memory may be an informative probe of neural network

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Conclusion