Melody Processing Characterizes Functional Neuroanatomy in the Aging Brain
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...
| Main Authors: | , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2018-11-01
|
| Series: | Frontiers in Neuroscience |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/article/10.3389/fnins.2018.00815/full |
| _version_ | 1819048782211317760 |
|---|---|
| author | Jennifer L. Agustus Hannah L. Golden Martina F. Callaghan Rebecca L. Bond Elia Benhamou Julia C. Hailstone Nikolaus Weiskopf Jason D. Warren |
| author_facet | Jennifer L. Agustus Hannah L. Golden Martina F. Callaghan Rebecca L. Bond Elia Benhamou Julia C. Hailstone Nikolaus Weiskopf Jason D. Warren |
| author_sort | Jennifer L. Agustus |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-12-21T11:21:43Z |
| format | Article |
| id | doaj.art-67bb511993cc4808a5801740dd4cad85 |
| institution | Directory Open Access Journal |
| issn | 1662-453X |
| language | English |
| last_indexed | 2024-12-21T11:21:43Z |
| publishDate | 2018-11-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Neuroscience |
| spelling | doaj.art-67bb511993cc4808a5801740dd4cad852022-12-21T19:05:46ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2018-11-011210.3389/fnins.2018.00815328553Melody Processing Characterizes Functional Neuroanatomy in the Aging BrainJennifer L. Agustus0Hannah L. Golden1Martina F. Callaghan2Rebecca L. Bond3Elia Benhamou4Julia C. Hailstone5Nikolaus Weiskopf6Jason D. Warren7Dementia Research Centre, Department of Neurodegenerative Disease, UCL Queen Square Institute of Neurology, University College London, London, United KingdomDementia Research Centre, Department of Neurodegenerative Disease, UCL Queen Square Institute of Neurology, University College London, London, United KingdomWellcome Trust Centre for Neuroimaging, UCL Queen Square Institute of Neurology, University College London, London, United KingdomDementia Research Centre, Department of Neurodegenerative Disease, UCL Queen Square Institute of Neurology, University College London, London, United KingdomDementia Research Centre, Department of Neurodegenerative Disease, UCL Queen Square Institute of Neurology, University College London, London, United KingdomDementia Research Centre, Department of Neurodegenerative Disease, UCL Queen Square Institute of Neurology, University College London, London, United KingdomDepartment of Neurophysics, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, GermanyDementia Research Centre, Department of Neurodegenerative Disease, UCL Queen Square Institute of Neurology, University College London, London, United KingdomThe 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.https://www.frontiersin.org/article/10.3389/fnins.2018.00815/fullagingcomplex soundfMRImusicsemantictemporal |
| spellingShingle | Jennifer L. Agustus Hannah L. Golden Martina F. Callaghan Rebecca L. Bond Elia Benhamou Julia C. Hailstone Nikolaus Weiskopf Jason D. Warren Melody Processing Characterizes Functional Neuroanatomy in the Aging Brain Frontiers in Neuroscience aging complex sound fMRI music semantic temporal |
| title | Melody Processing Characterizes Functional Neuroanatomy in the Aging Brain |
| title_full | Melody Processing Characterizes Functional Neuroanatomy in the Aging Brain |
| title_fullStr | Melody Processing Characterizes Functional Neuroanatomy in the Aging Brain |
| title_full_unstemmed | Melody Processing Characterizes Functional Neuroanatomy in the Aging Brain |
| title_short | Melody Processing Characterizes Functional Neuroanatomy in the Aging Brain |
| title_sort | melody processing characterizes functional neuroanatomy in the aging brain |
| topic | aging complex sound fMRI music semantic temporal |
| url | https://www.frontiersin.org/article/10.3389/fnins.2018.00815/full |
| work_keys_str_mv | AT jenniferlagustus melodyprocessingcharacterizesfunctionalneuroanatomyintheagingbrain AT hannahlgolden melodyprocessingcharacterizesfunctionalneuroanatomyintheagingbrain AT martinafcallaghan melodyprocessingcharacterizesfunctionalneuroanatomyintheagingbrain AT rebeccalbond melodyprocessingcharacterizesfunctionalneuroanatomyintheagingbrain AT eliabenhamou melodyprocessingcharacterizesfunctionalneuroanatomyintheagingbrain AT juliachailstone melodyprocessingcharacterizesfunctionalneuroanatomyintheagingbrain AT nikolausweiskopf melodyprocessingcharacterizesfunctionalneuroanatomyintheagingbrain AT jasondwarren melodyprocessingcharacterizesfunctionalneuroanatomyintheagingbrain |