Abstract
Despite considerable recent interest, the biological basis and clinical diagnosis of behavioural variant frontotemporal dementia (bvFTD) pose unresolved problems. Mentalising (the cognitive capacity to interpret the behaviour of oneself and others in terms of mental states) is impaired as a prominent feature of bvFTD, consistent with involvement of brain regions including ventro-medial prefrontal cortex (PFC), orbitofrontal cortex and anterior temporal lobes. Here, we investigated mentalising ability in a cohort of patients with bvFTD using a novel modality: music. We constructed a novel neuropsychological battery requiring attribution of affective mental or non-mental associations to musical stimuli. Mentalising performance of patients with bvFTD (n = 20) was assessed in relation to matched healthy control subjects (n = 20); patients also had a comprehensive assessment of behaviour and general neuropsychological functions. Neuroanatomical correlates of performance on the experimental tasks were investigated using voxel-based morphometry of patients' brain magnetic resonance imaging (MRI) scans. Compared to healthy control subjects, patients showed impaired ability to attribute mental states but not non-mental characteristics to music, and this deficit correlated with performance on a standard test of social inference and with carer ratings of patients' empathic capacity, but not with other potentially relevant measures of general neuropsychological function. Mentalising performance in the bvFTD group was associated with grey matter changes in anterior temporal lobe and ventro-medial PFC. These findings suggest that music can represent surrogate mental states and the ability to construct such mental representations is impaired in bvFTD, with potential implications for our understanding of the biology of bvFTD and human social cognition more broadly.
Highlights
Frontotemporal lobar degeneration (FTLD) refers to a group of diseases collectively characterised by atrophy of the frontal and temporal lobes
BvFTD is often associated with damage involving anterior temporal lobe regions that represent social concepts underpinning normal mentalising (Zahn et al, 2009): these anterior temporal areas interact with medial prefrontal cortex (PFC) during moral reasoning (Fumagalli and Priori, 2012), while anterior temporal lobe damage has been implicated in the pathogenesis of cognitive and affective theory of mind’ (ToM) deficits in another FTLD syndrome, semantic dementia (Duval et al, 2012)
These findings move beyond previous work demonstrating that the ability to label simple emotions in music is impaired in behavioural variant frontotemporal dementia (bvFTD) as part of a more general multimodal impairment of emotion processing (Omar et al, 2011; Hsieh et al, 2012): the deficit demonstrated here lay with attribution of more complex feeling states to music, and the deficit was at least partly specific for the attribution of mental states versus other, non-mental representations within the domain of music
Summary
Frontotemporal lobar degeneration (FTLD) refers to a group of diseases collectively characterised by atrophy of the frontal and temporal lobes. Neuroimaging studies in healthy individuals have linked the ability to mentalise with a network of brain regions, in particular ventro-medial PFC and frontal pole, OFC (Gallagher and Frith, 2003; Carrington and Bailey, 2009; Moll et al, 2011; Abu-Akel and Shamay-Tsoory, 2011) and the anterior temporal lobes (Fumagalli and Priori, 2012). BvFTD is often associated with damage involving anterior temporal lobe regions that represent social concepts underpinning normal mentalising (Zahn et al, 2009): these anterior temporal areas interact with medial PFC during moral reasoning (Fumagalli and Priori, 2012), while anterior temporal lobe damage has been implicated in the pathogenesis of cognitive and affective ToM deficits in another FTLD syndrome, semantic dementia (Duval et al, 2012)
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