Frontotemporal lobar degeneration changes neuronal beta-frequency dynamics during the mismatch negativity response
The consequences of frontotemporal lobar degeneration include changes in prefrontal cortical neurophysiology, with abnormalities of neural dynamics reported in the beta frequency range (14–30 Hz) that correlate with functional severity. We examined beta dynamics in two clinical syndromes associated...
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| Format: | Article |
| Language: | English |
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Elsevier
2024-01-01
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| Series: | NeuroImage: Clinical |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S2213158224001128 |
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| author | Alistair Perry Laura E. Hughes Natalie E. Adams Michelle Naessens Niels A. Kloosterman Matthew A. Rouse Alexander G. Murley Duncan Street P. Simon Jones James B. Rowe |
| author_facet | Alistair Perry Laura E. Hughes Natalie E. Adams Michelle Naessens Niels A. Kloosterman Matthew A. Rouse Alexander G. Murley Duncan Street P. Simon Jones James B. Rowe |
| author_sort | Alistair Perry |
| collection | DOAJ |
| description | The consequences of frontotemporal lobar degeneration include changes in prefrontal cortical neurophysiology, with abnormalities of neural dynamics reported in the beta frequency range (14–30 Hz) that correlate with functional severity. We examined beta dynamics in two clinical syndromes associated with frontotemporal lobar degeneration: the behavioral variant of frontotemporal dementia (bvFTD) and progressive supranuclear palsy (PSP). Whilst these two syndromes are partially convergent in cognitive effects, they differ in disease mechanisms such as molecular pathologies and prefrontal atrophy. Whether bvFTD and PSP also differ in neurophysiology remains to be fully investigated. We compared magnetoencephalography from 20 controls, 23 people with bvFTD and 21 people with PSP (Richardson’s syndrome) during an auditory roving oddball paradigm. We measured changes in low and high total beta power responses (14–22 and 22–30 Hz respectively) over frontotemporal cortex in the period of the mismatch negativity response (100–250 ms post-stimulus). In controls, we found increased 14–22 Hz beta power following unexpected sensory events (i.e. increased deviant versus standard response), from right prefrontal cortex. Relative to controls, PSP reversed the mismatch response in this time–frequency window, reflecting reduced responses to the deviant stimuli (relative to standard stimuli). Abnormal beta at baseline in PSP could account for the reduced task-modulation of beta. Across bvFTD and PSP groups, the beta response to deviant stimuli (relative to standard stimuli) correlated with clinical severity, but not with atrophy of the prefrontal source region. These findings confirm the proposed importance of higher-order cortical regions, and their beta-power generators, in sensory change detection and context-updating during oddball paradigms. The physiological effects are proposed to result from changes in synaptic density, cortical neurotransmitters and subcortical connections, rather than merely atrophy. Beta-power changes may assist clinical stratification and provide intermediate outcomes for experimental medicine studies of novel therapeutic strategies. |
| format | Article |
| id | doaj-art-fb0bc11b9ec4436c85e0049fd7bb33ad |
| institution | Kabale University |
| issn | 2213-1582 |
| language | English |
| publishDate | 2024-01-01 |
| publisher | Elsevier |
| record_format | Article |
| series | NeuroImage: Clinical |
| spelling | doaj-art-fb0bc11b9ec4436c85e0049fd7bb33ad2024-11-29T06:23:39ZengElsevierNeuroImage: Clinical2213-15822024-01-0144103671Frontotemporal lobar degeneration changes neuronal beta-frequency dynamics during the mismatch negativity responseAlistair Perry0Laura E. Hughes1Natalie E. Adams2Michelle Naessens3Niels A. Kloosterman4Matthew A. Rouse5Alexander G. Murley6Duncan Street7P. Simon Jones8James B. Rowe9MRC Cognition and Brain Sciences Unit, University of Cambridge, Cambridge, United Kingdom; Department of Clinical Neurosciences and Cambridge University Hospitals NHS Trust, University of Cambridge, United KingdomMRC Cognition and Brain Sciences Unit, University of Cambridge, Cambridge, United Kingdom; Department of Clinical Neurosciences and Cambridge University Hospitals NHS Trust, University of Cambridge, United KingdomDepartment of Clinical Neurosciences and Cambridge University Hospitals NHS Trust, University of Cambridge, United KingdomMRC Cognition and Brain Sciences Unit, University of Cambridge, Cambridge, United Kingdom; Department of Clinical Neurosciences and Cambridge University Hospitals NHS Trust, University of Cambridge, United KingdomInstitut für Psychologie I, Universität zu Lübeck, Germany; Max Planck Institute for Human Development, Berlin, GermanyMRC Cognition and Brain Sciences Unit, University of Cambridge, Cambridge, United KingdomDepartment of Clinical Neurosciences and Cambridge University Hospitals NHS Trust, University of Cambridge, United KingdomDepartment of Clinical Neurosciences and Cambridge University Hospitals NHS Trust, University of Cambridge, United KingdomDepartment of Clinical Neurosciences and Cambridge University Hospitals NHS Trust, University of Cambridge, United KingdomMRC Cognition and Brain Sciences Unit, University of Cambridge, Cambridge, United Kingdom; Department of Clinical Neurosciences and Cambridge University Hospitals NHS Trust, University of Cambridge, United Kingdom; Corresponding author at: Department of Clinical Neurosciences, University of Cambridge, Herchel Smith Building, Forvie Site, Robinson Way, Cambridge Biomedical Campus, Cambridge CB2 0SZ, United Kingdom.The consequences of frontotemporal lobar degeneration include changes in prefrontal cortical neurophysiology, with abnormalities of neural dynamics reported in the beta frequency range (14–30 Hz) that correlate with functional severity. We examined beta dynamics in two clinical syndromes associated with frontotemporal lobar degeneration: the behavioral variant of frontotemporal dementia (bvFTD) and progressive supranuclear palsy (PSP). Whilst these two syndromes are partially convergent in cognitive effects, they differ in disease mechanisms such as molecular pathologies and prefrontal atrophy. Whether bvFTD and PSP also differ in neurophysiology remains to be fully investigated. We compared magnetoencephalography from 20 controls, 23 people with bvFTD and 21 people with PSP (Richardson’s syndrome) during an auditory roving oddball paradigm. We measured changes in low and high total beta power responses (14–22 and 22–30 Hz respectively) over frontotemporal cortex in the period of the mismatch negativity response (100–250 ms post-stimulus). In controls, we found increased 14–22 Hz beta power following unexpected sensory events (i.e. increased deviant versus standard response), from right prefrontal cortex. Relative to controls, PSP reversed the mismatch response in this time–frequency window, reflecting reduced responses to the deviant stimuli (relative to standard stimuli). Abnormal beta at baseline in PSP could account for the reduced task-modulation of beta. Across bvFTD and PSP groups, the beta response to deviant stimuli (relative to standard stimuli) correlated with clinical severity, but not with atrophy of the prefrontal source region. These findings confirm the proposed importance of higher-order cortical regions, and their beta-power generators, in sensory change detection and context-updating during oddball paradigms. The physiological effects are proposed to result from changes in synaptic density, cortical neurotransmitters and subcortical connections, rather than merely atrophy. Beta-power changes may assist clinical stratification and provide intermediate outcomes for experimental medicine studies of novel therapeutic strategies.http://www.sciencedirect.com/science/article/pii/S2213158224001128NeurophysiologyFrontotemporal lobar degenerationBeta-bandMagnetoencephalographyTime-frequencyMismatch negativity |
| spellingShingle | Alistair Perry Laura E. Hughes Natalie E. Adams Michelle Naessens Niels A. Kloosterman Matthew A. Rouse Alexander G. Murley Duncan Street P. Simon Jones James B. Rowe Frontotemporal lobar degeneration changes neuronal beta-frequency dynamics during the mismatch negativity response NeuroImage: Clinical Neurophysiology Frontotemporal lobar degeneration Beta-band Magnetoencephalography Time-frequency Mismatch negativity |
| title | Frontotemporal lobar degeneration changes neuronal beta-frequency dynamics during the mismatch negativity response |
| title_full | Frontotemporal lobar degeneration changes neuronal beta-frequency dynamics during the mismatch negativity response |
| title_fullStr | Frontotemporal lobar degeneration changes neuronal beta-frequency dynamics during the mismatch negativity response |
| title_full_unstemmed | Frontotemporal lobar degeneration changes neuronal beta-frequency dynamics during the mismatch negativity response |
| title_short | Frontotemporal lobar degeneration changes neuronal beta-frequency dynamics during the mismatch negativity response |
| title_sort | frontotemporal lobar degeneration changes neuronal beta frequency dynamics during the mismatch negativity response |
| topic | Neurophysiology Frontotemporal lobar degeneration Beta-band Magnetoencephalography Time-frequency Mismatch negativity |
| url | http://www.sciencedirect.com/science/article/pii/S2213158224001128 |
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