GABAergic cortical network physiology in frontotemporal lobar degeneration
Open accessAbstract
The clinical syndromes caused by frontotemporal lobar degeneration are heterogeneous, including the behavioural variant frontotemporal dementia (bvFTD) and progressive supranuclear palsy. Although pathologically distinct, they share many behavioural, cognitive and physiological features, which may in part arise from common deficits of major neurotransmitters such as γ-aminobutyric acid (GABA). Here, we quantify the GABAergic impairment and its restoration with dynamic causal modelling of a double-blind placebo-controlled crossover pharmaco-magnetoencephalography study. We analysed 17 patients with bvFTD, 15 patients with progressive supranuclear palsy, and 20 healthy age- and gender-matched controls. In addition to neuropsychological assessment and structural MRI, participants undertook two magnetoencephalography sessions using a roving auditory oddball paradigm: once on placebo and once on 10 mg of the oral GABA reuptake inhibitor tiagabine. A subgroup underwent ultrahigh-field magnetic resonance spectroscopy measurement of GABA concentration, which was reduced among patients. We identified deficits in frontotemporal processing using conductance-based biophysical models of local and global neuronal networks. The clinical relevance of this physiological deficit is indicated by the correlation between top-down connectivity from frontal to temporal cortex and clinical measures of cognitive and behavioural change. A critical validation of the biophysical modelling approach was evidence from parametric empirical Bayes analysis that GABA levels in patients, measured by spectroscopy, were related to posterior estimates of patients’ GABAergic synaptic connectivity. Further evidence for the role of GABA in frontotemporal lobar degeneration came from confirmation that the effects of tiagabine on local circuits depended not only on participant group, but also on individual baseline GABA levels. Specifically, the phasic inhibition of deep cortico-cortical pyramidal neurons following tiagabine, but not placebo, was a function of GABA concentration. The study provides proof-of-concept for the potential of dynamic causal modelling to elucidate mechanisms of human neurodegenerative disease, and explains the variation in response to candidate therapies among patients. The laminar- and neurotransmitter-specific features of the modelling framework, can be used to study other treatment approaches and disorders. In the context of frontotemporal lobar degeneration, we suggest that neurophysiological restoration in selected patients, by targeting neurotransmitter deficits, could be used to bridge between clinical and preclinical models of disease, and inform the personalized selection of drugs and stratification of patients for future clinical trials.
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This approach has been used to study pathophysiology of non-AD dementias and confirmatory studies of drug interventions.
“This approach has been used to study the pathophysiology of non‐AD dementias, 18 , 19 and confirmatory studies of drug interventions. 5 , 18”
From Alzheimer's disease and its progression reduce pyramidal cell gain and connectivity (2025) · cites this paper as [18]
The Introduction describes dynamic causal modelling used to study network physiology in frontotemporal dementia and progressive supranuclear palsy, supporting the non-AD dementia portion. It also describes a placebo-controlled tiagabine experiment, but the Discussion says tiagabine was a pharmacological probe, not a clinical treatment, and that the study was not a clinical trial. It therefore does not support describing this work as a confirmatory study of a drug intervention. (LLM, conf=0.86)
Experimental — accuracy not yet measuredSix of the eight regions are based on prior studies that established a frontotemporal network responsible for generating the mismatch negativity response.
“Six of these regions are based on a series of prior studies of mismatch negativity generation with healthy adults and those with non‐AD dementia, 4 , 18 , 24 , 25 which established a frontotemporal network (primary auditory, superior temporal, and inferior frontal regions) responsible for generating the mismatch negativity response.”
From Alzheimer's disease and its progression reduce pyramidal cell gain and connectivity (2025) · cites this paper as [18]
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Self-citationShaw, A. D., Chandler, H. L., Hamandi, K., Muthukumaraswamy, S. D., Hammers, A., & Singh, K. D. (2021) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2021.04.005 · Cited by 6 · see citing works
Self-citationAponte, E. A., Schöbi, D., Stephan, K. E., & Heinzle, J. (2019) · Biological Psychiatry Cognitive Neuroscience and Neuroimaging · doi:10.1016/j.bpsc.2019.10.011 · Cited by 4 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Malpetti, M., Jones, P. S., Cope, T. E., Holland, N., Naessens, M., Rouse, M. A., Rittman, T., Savulich, G., Whiteside, D. J., Street, D., et al. (2023) · Annals of Neurology · doi:10.1002/ana.26543 · Cited by 53 · see citing works
Self-citationNeurophysiological consequences of synapse loss in progressive supranuclear palsy
Adams, N. E., Jafarian, A., Perry, A., Rouse, M. A., Shaw, A. D., Murley, A. G., Cope, T. E., Bevan-Jones, W. R., Passamonti, L., Street, D., et al. (2023) · Brain · doi:10.1093/brain/awac471 · Cited by 21 · see citing works
Self-citationEvidence and implications of abnormal predictive coding in dementia
Kocagoncu, E., Klimovich-Gray, A., Hughes, L. E., & Rowe, J. B. (2021) · Brain · doi:10.1093/brain/awab254 · Cited by 3 · see citing works
Self-citationAlzheimer's disease and its progression reduce pyramidal cell gain and connectivity
Lanskey, J. H., Jafarian, A., Karadag, M., Kocagoncu, E., Williams, R. S., Yadav, P., Quinn, A. J., Pitt, J., Thayanandan, T., Lowe, S., et al. (2025) · Alzheimer's & Dementia · doi:10.1002/alz.70805 · Cited by 2 · see citing works
“We used a canonical microcircuit model for evoked responses 23 with healthy adults and those with non-AD dementia, 4,18,24,25 which establishedafrontotemporalnetwork(primaryauditory,superiortem-poral, and inferior frontal regions) responsible for generating the mismatch negativity response.”
Self-citation
- Authors
- Adams, N. E., Hughes, L. E., Rouse, M. A., Phillips, H. N., Shaw, A. D., Murley, A. G., Cope, T. E., Bevan-Jones, W. R., Passamonti, L., Street, D., Holland, N., Nesbitt, D., Friston, K., & Rowe, J. B.
- Affiliations
- University of Cambridge (GB)
- MRC Cognition and Brain Sciences Unit (GB)
- Wellcome Centre for Human Neuroimaging (GB)
- Corresponding author
- Rowe, James B
- ORCID
- Venue
- Brain
- Publisher
- Oxford University Press (OUP)
- Published
- 2021-03-12
- Volume
- 144
- Issue
- 7
- Pages
- 2135-2145
- ISSN
- 0006-8950 (ISSN-L)
- 1460-2156
- PMC
- PMC8370432
- OpenAlex
- W3134821755
- Cited by
- 47
- References
- 82
- Citations by year
- 2026: 4 · 2025: 9 · 2024: 9 · 2023: 10 · 2022: 11 · 2021: 4
- FWCI
- 6.05
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Brain (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- ORCA Online Research @Cardiff (Cardiff University) (acceptedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Figshare (submittedVersion, cc-by)
- Open Research Exeter (University of Exeter) (submittedVersion, cc-by)
- Apollo (University of Cambridge) (submittedVersion, cc-by)
- Apollo (cc-by)
- Funders
- Wellcome Trust (103838)
- National Institute for Health Research Cambridge Biomedical Research Centre (BRC-1215-20014)
- Medical Research Council (MC_U105597119, MC_U_00005/12, SUAG/004/91365, SUAG/051 G101400)
- Association of British Neurologists
- Holt Fellowship
- National Institute for Health Research
- Department of Health and Social Care
- Topics
- Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Keywords
- frontotemporal lobar degeneration, behavioral variant frontotemporal dementia, progressive supranuclear palsy, GABAergic dysfunction, tiagabine, GABA reuptake inhibition, dynamic causal modeling, GABA levels, treatment response variability
- MeSH terms
- Tiagabine, Aged, Cerebral Cortex, Double-Blind Method, Female, gamma-Aminobutyric Acid, Humans, Magnetic Resonance Imaging, Male, Models, Neurological, Nerve Net, Synaptic Transmission, Magnetic Resonance Spectroscopy, Supranuclear Palsy, Progressive, Magnetoencephalography, Cross-Over Studies, Frontotemporal Dementia, GABA Uptake Inhibitors
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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