Abstract
The functional neuroanatomical mechanisms underpinning cognition in the normal older brain remain poorly defined, but have important implications for understanding the neurobiology of aging and the impact of neurodegenerative diseases. Auditory processing is an attractive model system for addressing these issues. Here, we used fMRI of melody processing to investigate auditory pattern processing in normal older individuals. We manipulated the temporal (rhythmic) structure and familiarity of melodies in a passive listening, ‘sparse’ fMRI protocol. A distributed cortico-subcortical network was activated by auditory stimulation compared with silence; and within this network, we identified separable signatures of anisochrony processing in bilateral posterior superior temporal lobes; melodic familiarity in bilateral anterior temporal and inferior frontal cortices; and melodic novelty in bilateral temporal and left parietal cortices. Left planum temporale emerged as a ‘hub’ region functionally partitioned for processing different melody dimensions. Activation of Heschl’s gyrus by auditory stimulation correlated with the integrity of underlying cortical tissue architecture, measured using multi-parameter mapping. Our findings delineate neural substrates for analyzing perceptual and semantic properties of melodies in normal aging. Melody (auditory pattern) processing may be a useful candidate paradigm for assessing cerebral networks in the older brain and potentially, in neurodegenerative diseases of later life.
Highlights
The functional neuroanatomical substrates of cognitive function in the normal older brain are of considerable interest but remain poorly understood
Brain mechanisms of sound processing are likely to be sensitive to the effects of normal aging: available psychoacoustic and functional neuroimaging evidence suggests that aspects of auditory scene analysis, auditory object encoding and the processing of complex auditory patterns are altered in older listeners (Kovacevic et al, 2005; Snyder and Alain, 2007; Hailstone et al, 2009; Wong et al, 2009; Peelle et al, 2010; Rimmele et al, 2012; Cliff et al, 2013; Profant et al, 2015; Sikka et al, 2015)
FMRI Data: Auditory Stimulation Auditory stimuli compared to the silence baseline ([FI + FA + UI + UA] > silence) engaged a distributed brain network including subcortical auditory structures and cerebellum together with bi-hemispheric cortical regions including medial and lateral Heschl’s gyrus (HG), planum temporale (PT), posterior superior temporal gyrus (STG) and temporo-parietal junction and extending dorsally to premotor cortices, supplementary motor area (SMA) and inferior frontal gyrus (Figure 2a and Table 1A)
Summary
The functional neuroanatomical substrates of cognitive function in the normal older brain are of considerable interest but remain poorly understood. While speech is the paradigm for information processing in complex auditory signals, other patterned, complex sounds are likely to make comparable demands on cognitive and neural resources in the older brain. Paramount among these is music: a complex auditory stimulus with separable perceptual and associative dimensions (Peretz et al, 1994; Peretz and Coltheart, 2003). Music is a case in point: it is likely that at least some aspects of memory for music are relatively spared in Alzheimer’s disease, candidate functional neuroanatomical mechanisms have been extrapolated from the younger brain (Jacobsen et al, 2015), while other neurodegenerative diseases are characterized by distinct profiles of impairment and resilience of particular musical functions (Omar et al, 2012; Hardy et al, 2016)
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