An integrated measure of GABA to characterize post-stroke plasticity.

[en] Stroke is a major cause of death and chronic neurological disability. Despite the improvements in stroke care, the number of patients affected by stroke keeps increasing and many stroke survivors are left permanently disabled. Current therapies are limited in efficacy. Understanding the neurobiological mechanisms underlying post-stroke recovery is therefore crucial to find new therapeutic options to address this medical burden. Long-lasting and widespread alterations of γ-aminobutyric acid (GABA) neurotransmission seem to play a key role in stroke recovery. In this review we first discuss a possible model of GABAergic modulation of post-stroke plasticity. We then overview the techniques currently available to non-invasively assess GABA in patients and the conclusions drawn from this limited body of work. Finally, we address the remaining open questions to clarify GABAergic changes underlying post-stroke recovery, we briefly review possible ways to modulate GABA post stroke and propose a novel approach to thoroughly quantify GABA in stroke patients, by integrating its concentration, the activity of its receptors and its link with microstructural changes.

Disciplines :

Neurology

Author, co-author :

Paparella, Ilenia ; Université de Liège - ULiège > GIGA > GIGA CRC In vivo Imaging - Sleep and chronobiology

Vandewalle, Gilles ; Université de Liège - ULiège > GIGA > GIGA CRC In vivo Imaging - Sleep and chronobiology

Stagg, Charlotte J; Wellcome Centre for Integrative Neuroimaging, FMRIB, Nuffield Department of Clinical Neurosciences, University of Oxford, Medical Research Council Brain Network Dynamics Unit, Oxford, UK

Maquet, Pierre ; Centre Hospitalier Universitaire de Liège - CHU > > Service de neurologie

Language :

English

Title :

An integrated measure of GABA to characterize post-stroke plasticity.

Publication date :

03 July 2023

Journal title :

NeuroImage: Clinical

eISSN :

2213-1582

Publisher :

Elsevier BV, Netherlands

Volume :

Pages :

103463

Peer reviewed :

Peer Reviewed verified by ORBi

Additional URL :

https://api.elsevier.com/content/article/PII:S2213158223001523?httpAccept=text/xml

Available on ORBi :

since 11 August 2023

Statistics

Number of views

98 (19 by ULiège)

Number of downloads

61 (6 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

Bibliography

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., GABAergic cortical network physiology in frontotemporal lobar degeneration. Brain 144:7 (2021), 2135–2145, 10.1093/brain/awab097.
Ahdab, R., Ayache, S.S., Brugières, P., Farhat, W.H., Lefaucheur, J.P., The Hand Motor Hotspot is not Always Located in the Hand Knob: A Neuronavigated Transcranial Magnetic Stimulation Study. Brain Topogr. 29:4 (2016), 590–597, 10.1007/s10548-016-0486-2.
Andersson, J.D., Matuskey, D., Finnema, S.J., Positron emission tomography imaging of the γ-aminobutyric acid system. Neuroscience Letters 691 (2019), 35–43.
Antonenko, D., Schubert, F., Bohm, F., Ittermann, B., Aydin, S., Hayek, D., Grittner, U., Flöel, A., tDCS-induced modulation of GABA levels and resting-state functional connectivity in older adults. J. Neurosci. 37:15 (2017), 4065–4073, 10.1523/JNEUROSCI.0079-17.2017.
Baron, J.-C., Yamauchi, H., Fujioka, M., Endres, M., Selective neuronal loss in ischemic stroke and cerebrovascular disease. J. Cereb. Blood Flow Metab. 34:1 (2014), 2–18.
Bednařík, P., Tkáč, I., Giove, F., DiNuzzo, M., Deelchand, D.K., Emir, U.E., Eberly, L.E., Mangia, S., Neurochemical and BOLD responses during neuronal activation measured in the human visual cortex at 7 Tesla. J. Cereb. Blood Flow Metab. 35:4 (2015), 601–610.
Belardinelli, P., Biabani, M., Blumberger, D.M., Bortoletto, M., Casarotto, S., David, O., Desideri, D., Etkin, A., Ferrarelli, F., Fitzgerald, P.B., Fornito, A., Gordon, P.C., Gosseries, O., Harquel, S., Julkunen, P., Keller, C.J., Kimiskidis, V.K., Lioumis, P., Miniussi, C., Rosanova, M., Rossi, S., Sarasso, S., Wu, W., Zrenner, C., Daskalakis, Z.J., Rogasch, N.C., Massimini, M., Ziemann, U., Ilmoniemi, R.J., Reproducibility in TMS–EEG studies: A call for data sharing, standard procedures and effective experimental control. Brain Stimulation: Basic, Translational, and Clinical Research in Neuromodulation 12:3 (2019), 787–790.
Belelli, D., Harrison, N.L., Maguire, J., Macdonald, R.L., Walker, M.C., Cope, D.W., Extrasynaptic GABAA receptors: form, pharmacology, and function. J. Neurosci. 29:41 (2009), 12757–12763.
Bernhardt, J., Hayward, K.S., Kwakkel, G., Ward, N.S., Wolf, S.L., Borschmann, K., Krakauer, J.W., Boyd, L.A., Carmichael, S.T., Corbett, D., Cramer, S.C., Agreed definitions and a shared vision for new standards in stroke recovery research: the stroke recovery and rehabilitation roundtable taskforce. Int. J. Stroke 12:5 (2017), 444–450.
Bhattacharyya, P.K., Phillips, M.D., Stone, L.A., Lowe, M.J., Activation volume vs BOLD signal change as measures of fMRI activation–Its impact on GABA–fMRI activation correlation. Magn. Reson. Imaging 42 (2017), 123–129.
Blicher, J.U., Near, J., Næss-Schmidt, E., Stagg, C.J., Johansen-Berg, H., Nielsen, J.F., Østergaard, L., Ho, Y.C.L., GABA levels are decreased after stroke and GABA changes during rehabilitation correlate with motor improvement. Neurorehabil. Neural Repair 29:3 (2015), 278–286, 10.1177/1545968314543652.
Brickley, S.G., Revilla, V., Cull-Candy, S.G., Wisden, W., Farrant, M., Adaptive regulation of neuronal excitability by a voltage-independent potassium conductance. Nature 409:6816 (2001), 88–92.
Brix, G., Nekolla, E.A., Nosske, D., Griebel, J., Risks and safety aspects related to PET/MR examinations. Eur. J. Nucl. Med. Mol. Imaging 36:S1 (2009), 131–138.
Brown, C.E., Li, P., Boyd, J.D., Delaney, K.R., Murphy, T.H., Extensive turnover of dendritic spines and vascular remodeling in cortical tissues recovering from stroke. J. Neurosci. 27:15 (2007), 4101–4109.
Bütefisch, C.M., Netz, J., Wessling, M., Seitz, R.J., Hömberg, V., Remote changes in cortical excitability after stroke. Brain 126:2 (2003), 470–481.
Caporale, N., Dan, Y., Spike timing-dependent plasticity: a Hebbian learning rule. Annu. Rev. Neurosci. 31:1 (2008), 25–46.
Carmichael, S.T., Cellular and molecular mechanisms of neural repair after stroke: making waves. Annals of Neurology: Official Journal of the American Neurological Association and the Child Neurology Society 59:5 (2006), 735–742.
Carmichael, S.T., Wei, L., Rovainen, C.M., Woolsey, T.A., New patterns of intracortical projections after focal cortical stroke. Neurobiol. Dis. 8:5 (2001), 910–922.
Carmichael, S.T., Tatsukawa, K., Katsman, D., Tsuyuguchi, N., Kornblum, H.I., Evolution of diaschisis in a focal stroke model. Stroke 35:3 (2004), 758–763.
Cash, R.F.H., Ziemann, U., Murray, K., Thickbroom, G.W., Late cortical disinhibition in human motor cortex: a triple-pulse transcranial magnetic stimulation study. J. Neurophysiol. 103:1 (2010), 511–518.
Chellappa, S.L., Gaggioni, G., Ly, J.Q.M., Papachilleos, S., Borsu, C., Brzozowski, A., Rosanova, M., Sarasso, S., Luxen, A., Middleton, B., Archer, S.N., Dijk, D.J., Massimini, M., Maquet, P., Phillips, C., Moran, R.J., Vandewalle, G., Circadian dynamics in measures of cortical excitation and inhibition balance. Sci. Rep. 6:May (2016), 1–13, 10.1038/srep33661.
Chen, X.i., Fan, X., Hu, Y., Zuo, C., Whitfield-Gabrieli, S., Holt, D., Gong, Q., Yang, Y., Pizzagalli, D.A., Du, F., Ongur, D., Regional GABA concentrations modulate inter-network resting-state functional connectivity. Cereb. Cortex 29:4 (2019), 1607–1618.
Chen, Z., Silva, A.C., Yang, J., Shen, J., Elevated endogenous GABA level correlates with decreased fMRI signals in the rat brain during acute inhibition of GABA transaminase. J. Neurosci. Res. 79:3 (2005), 383–391.
Chen, Q.M., Yao, F.R., Sun, H.W., Chen, Z.G., Ke, J., Liao, J., Cai, X.Y., Yu, L.Q., Wu, Z.Y., Wang, Z., Pan, X., Liu, H.Y., Li, L., Zhang, Q.Q., Ling, W.H., Fang, Q., Combining inhibitory and facilitatory repetitive transcranial magnetic stimulation (rTMS) treatment improves motor function by modulating GABA in acute ischemic stroke patients. Restor. Neurol. Neurosci. 39:6 (2021), 419–434, 10.3233/RNN-211195.
Cirillo, J., Mooney, R.A., Ackerley, S.J., Alan Barber, P., Borges, V.M., Clarkson, A.N., Mangold, C., Ren, A., Smith, M.C., Stinear, C.M., Byblow, W.D., Neurochemical balance and inhibition at the subacute stage after stroke. J. Neurophysiol. 123:5 (2020), 1775–1790, 10.1152/jn.00561.2019.
Conde, V., Tomasevic, L., Akopian, I., Stanek, K., Saturnino, G.B., Thielscher, A., Bergmann, T.O., Siebner, H.R., The non-transcranial TMS-evoked potential is an inherent source of ambiguity in TMS-EEG studies. Neuroimage 185 (2019), 300–312.
Connelly, W.M., Fyson, S.J., Errington, A.C., McCafferty, C.P., Cope, D.W., Di Giovanni, G., Crunelli, V., GABAB receptors regulate extrasynaptic GABAA receptors. J. Neurosci. 33:9 (2013), 3780–3785.
Constans, C., Ahnine, H., Santin, M., Lehericy, S., Tanter, M., Pouget, P., Aubry, J.F., Non-invasive ultrasonic modulation of visual evoked response by GABA delivery through the blood brain barrier. J. Control. Release 318:May 2019 (2020), 223–231, 10.1016/j.jconrel.2019.12.006.
Cousijn, H., Haegens, S., Wallis, G., Near, J., Stokes, M.G., Harrison, P.J., Nobre, A.C., Resting GABA and glutamate concentrations do not predict visual gamma frequency or amplitude. Resting GABA and glutamate concentrations do not predict visual gamma frequency or amplitude. 111:25 (2014), 9301–9306.
Cramer, S.C., Chopp, M., Recovery recapitulates ontogeny. Trends Neurosci. 23:6 (2000), 265–271.
Cramer, S.C., Sur, M., Dobkin, B.H., O'Brien, C., Sanger, T.D., Trojanowski, J.Q., Rumsey, J.M., Hicks, R., Cameron, J., Chen, D., Chen, W.G., Cohen, L.G., deCharms, C., Duffy, C.J., Eden, G.F., Fetz, E.E., Filart, R., Freund, M., Grant, S.J., Haber, S., Kalivas, P.W., Kolb, B., Kramer, A.F., Lynch, M., Mayberg, H.S., McQuillen, P.S., Nitkin, R., Pascual-Leone, A., Reuter-Lorenz, P., Schiff, N., Sharma, A., Shekim, L., Stryker, M., Sullivan, E.V., Vinogradov, S., Harnessing neuroplasticity for clinical applications. Brain 134:6 (2011), 1591–1609.
Cuypers, K., Hehl, M., van Aalst, J., Chalavi, S., Mikkelsen, M., Van Laere, K., Dupont, P., Mantini, D., Swinnen, S.P., Age-related GABAergic differences in the primary sensorimotor cortex: A multimodal approach combining PET, MRS and TMS. Neuroimage, 226(October 2020), 2021, 117536, 10.1016/j.neuroimage.2020.117536.
Darmani, G., Ziemann, U., Pharmacophysiology of TMS-evoked EEG potentials: A mini-review. Brain Stimul. 12:3 (2019), 829–831, 10.1016/j.brs.2019.02.021.
Darmani, G., Zipser, C.M., Böhmer, G.M., Deschet, K., Müller-Dahlhaus, F., Belardinelli, P., Schwab, M., Ziemann, U., Effects of the selective α5-GABAAR antagonist S44819 on excitability in the human brain: a TMS–EMG and TMS–EEG phase I study. J. Neurosci. 36:49 (2016), 12312–12320.
Desai, N.S., Homeostatic plasticity in the CNS: synaptic and intrinsic forms. Journal of Physiology-Paris 97:4–6 (2003), 391–402.
Doyle, K.P., Simon, R.P., Stenzel-Poore, M.P., Mechanisms of ischemic brain damage. Neuropharmacology 55:3 (2008), 310–318.
Dromerick, A.W., Geed, S., Barth, J., Brady, K., Giannetti, M.L., Mitchell, A., Edwardson, M.A., Tan, M.T., Zhou, Y., Newport, E.L., Edwards, D.F., Critical Period After Stroke Study (CPASS): A phase II clinical trial testing an optimal time for motor recovery after stroke in humans. PNAS, 118(39), 2021.
Feigin, V.L., Forouzanfar, M.H., Krishnamurthi, R., Mensah, G.A., Connor, M., Bennett, D.A., Moran, A.E., Sacco, R.L., Anderson, L., Truelsen, T., Global and regional burden of stroke during 1990–2010: findings from the Global Burden of Disease Study 2010. Lancet 383:9913 (2014), 245–255.
Feigin, V.L., Vos, T., Alahdab, F., Amit, A.M.L., Bärnighausen, T.W., Beghi, E., Beheshti, M., Chavan, P.P., Criqui, M.H., Desai, R., Dhamminda Dharmaratne, S., Dorsey, E.R., Wilder Eagan, A., Elgendy, I.Y., Filip, I., Giampaoli, S., Giussani, G., Hafezi-Nejad, N., Hole, M.K., Ikeda, T., Owens Johnson, C., Kalani, R., Khatab, K., Khubchandani, J., Kim, D., Koroshetz, W.J., Krishnamoorthy, V., Krishnamurthi, R.V., Liu, X., Lo, W.D., Logroscino, G., Mensah, G.A., Miller, T.R., Mohammed, S., Mokdad, A.H., Moradi-Lakeh, M., Morrison, S.D., Shivamurthy, V.K.N., Naghavi, M., Nichols, E., Norrving, B.o., Odell, C.M., Pupillo, E., Radfar, A., Roth, G.A., Shafieesabet, A., Sheikh, A., Sheikhbahaei, S., Shin, J.I., Singh, J.A., Steiner, T.J., Stovner, L.J., Wallin, M.T., Weiss, J., Wu, C., Zunt, J.R., Adelson, J.D., Murray, C.J.L., Burden of neurological disorders across the US from 1990–2017: a global burden of disease study. JAMA Neurol., 78(2), 2021, 165.
Fisicaro, F., Lanza, G., Grasso, A.A., Pennisi, G., Bella, R., Paulus, W., Pennisi, M., Repetitive transcranial magnetic stimulation in stroke rehabilitation: review of the current evidence and pitfalls. Ther. Adv. Neurol. Disord., 12, 2019.
Floyer-Lea, A., Wylezinska, M., Kincses, T., Matthews, P.M., Rapid modulation of GABA concentration in human sensorimotor cortex during motor learning. J. Neurophysiol. 95:3 (2006), 1639–1644.
Friston, K.J., Harrison, L., Penny, W., Dynamic causal modelling. Neuroimage 19:4 (2003), 1273–1302.
Gainey, M.A., Hurvitz-Wolff, J.R., Lambo, M.E., Turrigiano, G.G., Synaptic scaling requires the GluR2 subunit of the AMPA receptor. J. Neurosci. 29:20 (2009), 6479–6489.
Galanis, C., Vlachos, A., Hebbian and Homeostatic Synaptic Plasticity—Do Alterations of One Reflect Enhancement of the Other?. Front. Cell. Neurosci. 14:March (2020), 1–8, 10.3389/fncel.2020.00050.
Gawne, T.J., Overbeek, G.J., Killen, J.F., Reid, M.A., Ellis, C.A., Lahti, A.C., Kraguljac, N.V., Denney, T.S., OPEN A multimodal magnetoencephalography 7 T fMRI and 7 T proton MR spectroscopy study in fi rst episode psychosis. NPJ Schizophr. 6(1), 23 (2020), 1–9, 10.1038/s41537-020-00113-4.
Głodzik-Sobańska, L., Słowik, A., Kozub, J., Sobiecka, B., Urbanik, A., Szczudlik, A., GABA in ischemic stroke: proton magnetic resonance study. Med. Sci. Monit., 10(Supplement 3), 2004.
Grefkes, C., Fink, G.R., Recovery from stroke: current concepts and future perspectives. Neurological Research and Practice, 2(1), 2020, 10.1186/s42466-020-00060-6.
Grigoras, I.-F., Stagg, C.J., Recent advances in the role of excitation–inhibition balance in motor recovery post-stroke. Faculty Reviews, 10(58), 2021, 10.12703/r/10-58.
Hagemann, G., Redecker, C., Neumann-Haefelin, T., Freund, H., Witte, O.W., Increased long-term potentiation in the surround of experimentally induced focal cortical infarction. Annals of Neurology: Official Journal of the American Neurological Association and the Child Neurology Society 44:2 (1998), 255–258.
Hall, S.D., Yamawaki, N., Fisher, A.E., Clauss, R.P., Woodhall, G.L., Stanford, I.M., GABA (A) alpha-1 subunit mediated desynchronization of elevated low frequency oscillations alleviates specific dysfunction in stroke–a case report. Clin. Neurophysiol. 121:4 (2010), 549–555.
Hartman, K.N., Pal, S.K., Burrone, J., Murthy, V.N., Activity-dependent regulation of inhibitory synaptic transmission in hippocampal neurons. Nat. Neurosci. 9:5 (2006), 642–649.
Hattiangady, B., Rao, M.S., Shetty, G.A., Shetty, A.K., Brain-derived neurotrophic factor, phosphorylated cyclic AMP response element binding protein and neuropeptide Y decline as early as middle age in the dentate gyrus and CA1 and CA3 subfields of the hippocampus. Exp. Neurol. 195:2 (2005), 353–371.
Hebb, D.O., Organization of behavior. new york: Wiley. J. Clin. Psychol. 6:3 (1949), 307–335.
Hebb, D.O., The first stage of perception: growth of the assembly. The Organization of Behavior 4 (1949), 60–78.
Hensch, T.K., Critical period plasticity in local cortical circuits. Nat. Rev. Neurosci. 6:11 (2005), 877–888.
Hess, G., Aizenman, C.D., Donoghue, J.P., Conditions for the induction of long-term potentiation in layer II/III horizontal connections of the rat motor cortex. J. Neurophysiol. 75:5 (1996), 1765–1778.
Hiu, T., Farzampour, Z., Paz, J.T., Wang, E.H.J., Badgely, C., Olson, A., Micheva, K.D., Wang, G., Lemmens, R., Tran, K.V., Nishiyama, Y., Liang, X., Hamilton, S.A., O'Rourke, N., Smith, S.J., Huguenard, J.R., Bliss, T.M., Steinberg, G.K., Enhanced phasic GABA inhibition during the repair phase of stroke: a novel therapeutic target. Brain 139:2 (2016), 468–480.
Hordacre, B., McCambridge, A.B., Ridding, M.C., Bradnam, L.V., Can Transcranial Direct Current Stimulation Enhance Poststroke Motor Recovery?. Neurology 97:4 (2021), 170–180, 10.1212/wnl.0000000000012187.
Hu, H., Gan, J., Jonas, P., Fast-spiking, parvalbumin+ GABAergic interneurons: From cellular design to microcircuit function. Science, 345(6196), 2014, 10.1126/science.1255263.
Hubbard, I.J., Parsons, M.W., Neilson, C., Carey, L.M., Task-specific training: evidence for and translation to clinical practice. Occup. Ther. Int. 16:3–4 (2009), 175–189.
Hummel, F.C., Steven, B., Hoppe, J., Heise, K., Thomalla, G., Cohen, L.G., Gerloff, C., Deficient intracortical inhibition (SICI) during movement preparation after chronic stroke. Neurology 72:20 (2009), 1766–1772.
Hynynen, K., McDannold, N., Sheikov, N.A., Jolesz, F.A., Vykhodtseva, N., Local and reversible blood–brain barrier disruption by noninvasive focused ultrasound at frequencies suitable for trans-skull sonications. Neuroimage 24:1 (2005), 12–20.
Ilmoniemi, R.J., Virtanen, J., Ruohonen, J., Karhu, J., Aronen, H.J., Näätänen, R., Katila, T., Neuronal responses to magnetic stimulation reveal cortical reactivity and connectivity. Neuroreport 8:16 (1997), 3537–3540.
Jensen, O., Goel, P., Kopell, N., Pohja, M., Hari, R., Ermentrout, B., On the human sensorimotor-cortex beta rhythm: sources and modeling. Neuroimage 26:2 (2005), 347–355.
Johnstone, A., Grigoras, I., Petitet, P., Capitão, L.P., Stagg, C.J., A single, clinically relevant dose of the GABA B agonist baclofen impairs visuomotor learning. J. Physiol. 599:1 (2021), 307–322.
Johnstone, A., Brander, F., Kelly, K., Bestmann, S., Ward, N., Differences in outcomes following an intensive upper-limb rehabilitation program for patients with common central nervous system-acting drug prescriptions. Int. J. Stroke 17:3 (2022), 269–281, 10.1177/17474930211006287.
Jung, J., Williams, S.R., Sanaei Nezhad, F., Lambon Ralph, M.A., GABA concentrations in the anterior temporal lobe predict human semantic processing. Sci. Rep., 7(1), 2017, 15748.
Kang, N., Summers, J.J., Cauraugh, J.H., Transcranial direct current stimulation facilitates motor learning post-stroke: a systematic review and meta-analysis. J. Neurol. Neurosurg. Psychiatry 87:4 (2016), 345–355.
Kassenbrock, A., Vasdev, N., Liang, H., S., Selected PET radioligands for ion channel linked neuroreceptor imaging: focus on GABA, NMDA and nACh receptors. Curr. Top. Med. Chem. 16:16 (2016), 1830–1842.
Kiemes, A., Davies, C., Kempton, M. J., Lukow, P. B., Bennallick, C., Stone, J. M., & Modinos, G. (2021). GABA, Glutamate and Neural Activity: A Systematic Review With Meta-Analysis of Multimodal 1H-MRS-fMRI Studies. In Frontiers in Psychiatry (Vol. 12, Issue March). https://doi.org/10.3389/fpsyt.2021.644315.
Kilman, V., Van Rossum, M.C.W., Turrigiano, G.G., Activity deprivation reduces miniature IPSC amplitude by decreasing the number of postsynaptic GABAA receptors clustered at neocortical synapses. J. Neurosci. 22:4 (2002), 1328–1337.
Kim, Y.K., Yang, E.J., Cho, K., Lim, J.Y., Paik, N.-J., Functional recovery after ischemic stroke is associated with reduced GABAergic inhibition in the cerebral cortex: a GABA PET study. Neurorehabil. Neural Repair 28:6 (2014), 576–583.
Krakauer, J.W., Carmichael, S.T., Broken movement: the neurobiology of motor recovery after stroke. 2022, MIT Press.
Kuhlman, S.J., Olivas, N.D., Tring, E., Ikrar, T., Xu, X., Trachtenberg, J.T., A disinhibitory microcircuit initiates critical-period plasticity in the visual cortex. Nature 501:7468 (2013), 543–546.
Kumar, A., Kitago, T., Pharmacological Enhancement of Stroke Recovery. Curr. Neurol. Neurosci. Rep., 19(7), 2019, 10.1007/s11910-019-0959-2.
Kuśmierz, Ł., Isomura, T., Toyoizumi, T., Learning with three factors: modulating Hebbian plasticity with errors. Curr. Opin. Neurobiol. 46 (2017), 170–177, 10.1016/j.conb.2017.08.020.
Lawrence, E.S., Coshall, C., Dundas, R., Stewart, J., Rudd, A.G., Howard, R., Wolfe, C.D.A., Estimates of the prevalence of acute stroke impairments and disability in a multiethnic population. Stroke 32:6 (2001), 1279–1284.
Lea-carnall, C.A., El-deredy, W., Williams, S.R., Stagg, C.J., Trujillo-barreto, N.J., From synaptic activity to human in vivo quantification of neurotransmitter dynamics: a neural modelling approach. BioRxiv, 2021, 1–33.
Lemke, C., Hess, A., Clare, S., Bachtiar, V., Stagg, C., Jezzard, P., Emir, U., Two-voxel spectroscopy with dynamic B0 shimming and flip angle adjustment at 7 T in the human motor cortex. NMR Biomed. 28:7 (2015), 852–860.
Lindsay, M.P., Norrving, B., Sacco, R.L., Brainin, M., Hacke, W., Martins, S., Pandian, J., Feigin, V., World Stroke Organization (WSO): Global Stroke Fact Sheet 2019. Int. J. Stroke 14:8 (2019), 806–817, 10.1177/1747493019881353.
Magee, J.C., Grienberger, C., Synaptic Plasticity Forms and Functions. Annu. Rev. Neurosci. 43 (2020), 95–117, 10.1146/annurev-neuro-090919-022842.
Martin, D.L., Rimvall, K., Regulation of γ-aminobutyric acid synthesis in the brain. J. Neurochem. 60:2 (1993), 395–407.
Marty, B., Larrat, B., Van Landeghem, M., Robic, C., Robert, P., Port, M., Le Bihan, D., Pernot, M., Tanter, M., Lethimonnier, F., Mériaux, S., Dynamic study of blood–brain barrier closure after its disruption using ultrasound: a quantitative analysis. J. Cereb. Blood Flow Metab. 32:10 (2012), 1948–1958.
Matuszewski, J., Kossowski, B., Bola, Ł., Banaszkiewicz, A., Paplińska, M., Gyger, L., Kherif, F., Szwed, M., Frackowiak, R.S., Jednoróg, K., Draganski, B., Marchewka, A., Brain plasticity dynamics during tactile Braille learning in sighted subjects: Multi-contrast MRI approach. Neuroimage, 227, 2021, 117613.
McDonnell, M.N., Orekhov, Y., Ziemann, U., The role of GABAB receptors in intracortical inhibition in the human motor cortex. Exp. Brain Res. 173:1 (2006), 86–93.
McDonnell, M.N., Stinear, C.M., TMS measures of motor cortex function after stroke: a meta-analysis. Brain Stimul. 10:4 (2017), 721–734.
Mehrholz, J., Hädrich, A., Platz, T., Kugler, J., & Pohl, M. (2012). Electromechanical and robot‐assisted arm training for improving generic activities of daily living, arm function, and arm muscle strength after stroke. Cochrane Database of Systematic Reviews, 6.
Mehrholz, J., Thomas, S., Elsner, B., Treadmill training and body weight support for walking after stroke. Cochrane Database Syst. Rev., 8, 2017.
Mehrholz, J., Thomas, S., Kugler, J., Pohl, M., Elsner, B., Electromechanical-assisted training for walking after stroke. Cochrane Database Syst. Rev., 10, 2020.
Meng, Y., Hynynen, K., Lipsman, N., Applications of focused ultrasound in the brain: from thermoablation to drug delivery. Nat. Rev. Neurol. 17:1 (2021), 7–22, 10.1038/s41582-020-00418-z.
Michalettos, G., Ruscher, K., Crosstalk Between GABAergic Neurotransmission and Inflammatory Cascades in the Post-ischemic Brain: Relevance for Stroke Recovery. Front. Cell. Neurosci. 16:March (2022), 1–16, 10.3389/fncel.2022.807911.
Mooney, R.A., Cirillo, J., Byblow, W.D., GABA and primary motor cortex inhibition in young and older adults: a multimodal reliability study. J. Neurophysiol. 118:1 (2017), 425–433.
Mooney, R.A., Ackerley, S.J., Rajeswaran, D.K., Cirillo, J., Barber, P.A., Stinear, C.M., Byblow, W.D., The influence of primary motor cortex inhibition on upper limb impairment and function in chronic stroke: a multimodal study. Neurorehabil. Neural Repair 33:2 (2019), 130–140.
Moran, R.J., Symmonds, M., Stephan, K.E., Friston, K.J., Dolan, R.J., An in vivo assay of synaptic function mediating human cognition. Curr. Biol. 21:15 (2011), 1320–1325, 10.1016/j.cub.2011.06.053.
Moran, R.J., Pinotsis, D.A., Friston, K.J., Neural masses and fields in dynamic causal modeling. Front. Comput. Neurosci., 7, 2013, 57.
Murphy, T.H., Corbett, D., Plasticity during stroke recovery: From synapse to behaviour. Nat. Rev. Neurosci. 10:12 (2009), 861–872, 10.1038/nrn2735.
Muthukumaraswamy, S.D., Carhart-Harris, R.L., Moran, R.J., Brookes, M.J., Williams, T.M., Errtizoe, D., Sessa, B., Papadopoulos, A., Bolstridge, M., Singh, K.D., Feilding, A., Friston, K.J., Nutt, D.J., Broadband cortical desynchronization underlies the human psychedelic state. J. Neurosci. 33:38 (2013), 15171–15183, 10.1523/JNEUROSCI.2063-13.2013.
Muthukumaraswamy, S.D., Shaw, A.D., Jackson, L.E., Hall, J., Moran, R., Saxena, N., Evidence that subanesthetic doses of ketamine cause sustained disruptions of NMDA and AMPA-mediated frontoparietal connectivity in humans. J. Neurosci. 35:33 (2015), 11694–11706.
Nelson, S.B., Turrigiano, G.G., Strength through diversity. Neuron 60:3 (2008), 477–482.
Nievelstein, R.A.J., Quarles van Ufford, H.M.E., Kwee, T.C., Bierings, M.B., Ludwig, I., Beek, F.J.A., de Klerk, J.M.H., Mali, W.P.T.M., de Bruin, P.W., Geleijns, J., Radiation exposure and mortality risk from CT and PET imaging of patients with malignant lymphoma. Eur. Radiol. 22:9 (2012), 1946–1954.
Nishibe, M., Urban, E.T.R. III, Barbay, S., Nudo, R.J., Rehabilitative training promotes rapid motor recovery but delayed motor map reorganization in a rat cortical ischemic infarct model. Neurorehabil. Neural Repair 29:5 (2015), 472–482.
Nowak, M., Hinson, E., Van Ede, F., Pogosyan, A., Guerra, A., Quinn, A., Brown, P., Stagg, C.J., Driving human motor cortical oscillations leads to behaviorally relevant changes in local GABAA inhibition: a tACS-TMS study. J. Neurosci. 37:17 (2017), 4481–4492.
Oh, M.-K., Yoon, K.J., Lee, Y.-T., Chae, S.W., Choi, H.Y., Shin, H.S., Park, Y.H., Chun, S.-W., Park, Y.S., Effect of zolpidem on functional recovery in a rat model of ischemic stroke. J. Int. Med. Res. 46:1 (2018), 249–257.
Paille, V., Fino, E., Du, K., Morera-Herreras, T., Perez, S., Kotaleski, J.H., Venance, L., GABAergic circuits control spike-timing-dependent plasticity. J. Neurosci. 33:22 (2013), 9353–9363, 10.1523/JNEUROSCI.5796-12.2013.
Plautz, E.J., Barbay, S., Frost, S.B., Friel, K.M., Dancause, N., Zoubina, E.V., Stowe, A.M., Quaney, B.M., Nudo, R.J., Post-infarct cortical plasticity and behavioral recovery using concurrent cortical stimulation and rehabilitative training: a feasibility study in primates. Neurol. Res. 25:8 (2003), 801–810.
Pradhan, S., Bonekamp, S., Gillen, J.S., Rowland, L.M., Wijtenburg, S.A., Edden, R.A.E., Barker, P.B., Comparison of single voxel brain MRS AT 3 T and 7 T using 32-channel head coils. Magn. Reson. Imaging 33:8 (2015), 1013–1018.
Premoli, I., Castellanos, N., Rivolta, D., Belardinelli, P., Bajo, R., Zipser, C., Espenhahn, S., Heidegger, T., Müller-Dahlhaus, F., Ziemann, U., TMS-EEG signatures of GABAergic neurotransmission in the human cortex. J. Neurosci. 34:16 (2014), 5603–5612.
Premoli, I., Bergmann, T.O., Fecchio, M., Rosanova, M., Biondi, A., Belardinelli, P., Ziemann, U., The impact of GABAergic drugs on TMS-induced brain oscillations in human motor cortex. Neuroimage 163 (2017), 1–12.
Redecker, C., Wang, W., Fritschy, J.M., Witte, O.W., Widespread and long-lasting alterations in GABAA-receptor subtypes after focal cortical infarcts in rats: Mediation by NMDA-dependent processes. J. Cereb. Blood Flow Metab. 22:12 (2002), 1463–1475, 10.1097/01.WCB.0000034149.72481.BD.
Richter, G., Liao, V.W.Y., Ahring, P.K., Chebib, M., The Z-Drugs Zolpidem, Zaleplon, and Eszopiclone Have Varying Actions on Human GABAA Receptors Containing γ1, γ2, and γ3 Subunits. Front. Neurosci., 14, 2020, 10.3389/fnins.2020.599812.
Rochester, N., Holland, J., Haibt, L., Duda, W., Tests on a cell assembly theory of the action of the brain, using a large digital computer. IRE Trans. Inf. Theory 2:3 (1956), 80–93.
Russo, S., Sarasso, S., Puglisi, G.E., Dal Palù, D., Pigorini, A., Casarotto, S., D'Ambrosio, S., Astolfi, A., Massimini, M., Rosanova, M., Fecchio, M., TAAC-TMS Adaptable Auditory Control: A universal tool to mask TMS clicks. J. Neurosci. Methods, 370, 2022.
Schambra, H.M., Ogden, R.T., Martínez-Hernández, I.E., Lin, X., Chang, Y.B., Rahman, A., Edwards, D.J., Krakauer, J.W., The reliability of repeated TMS measures in older adults and in patients with subacute and chronic stroke. Front. Cell. Neurosci., 9, 2015, 335.
Schiene, K., Bruehl, C., Zilles, K., Qu, M., Hagemann, G., Kraemer, M., Witte, O.W., Neuronal hyperexcitability and reduction of GABAA-receptor expression in the surround of cerebral photothrombosis. J. Cereb. Blood Flow Metab. 16:5 (1996), 906–914.
Sedova, P., Brown, R.D., Zvolsky, M., Belaskova, S., Volna, M., Baluchova, J., Bednarik, J., Mikulik, R., Incidence of stroke and ischemic stroke subtypes: a community-based study in Brno. Czech Republic. Cerebrovascular Diseases 50:1 (2021), 54–61.
Sejnowski, T.J., Statistical constraints on synaptic plasticity. J. Theor. Biol. 69:2 (1977), 385–389.
Sigel, E., Mapping of the benzodiazepine recognition site on GABA-A receptors. Curr. Top. Med. Chem. 2:8 (2002), 833–839.
Smania, N., Gandolfi, M., Paolucci, S., Iosa, M., Ianes, P., Recchia, S., Giovanzana, C., Molteni, F., Avesani, R., Di Paolo, P., Zaccala, M., Agostini, M., Tassorelli, C., Fiaschi, A., Primon, D., Ceravolo, M.G., Farina, S., Reduced-intensity modified constraint-induced movement therapy versus conventional therapy for upper extremity rehabilitation after stroke: a multicenter trial. Neurorehabil. Neural Repair 26:9 (2012), 1035–1045.
Song, S., Miller, K.D., Abbott, L.F., Competitive Hebbian learning through spike-timing-dependent synaptic plasticity. Nat. Neurosci. 3:9 (2000), 919–926.
Sparta, D.R., Hovelsø, N., Mason, A.O., Kantak, P.A., Ung, R.L., Decot, H.K., Stuber, G.D., Activation of prefrontal cortical parvalbumin interneurons facilitates extinction of reward-seeking behavior. J. Neurosci. 34:10 (2014), 3699–3705.
Stagg, C.J., Wylezinska, M., Matthews, P.M., Johansen-Berg, H., Jezzard, P., Rothwell, J.C., Bestmann, S., Neurochemical effects of theta burst stimulation as assessed by magnetic resonance spectroscopy. J. Neurophysiol. 101:6 (2009), 2872–2877.
Stagg, C.J., Bachtiar, V., Johansen-Berg, H., The role of GABA in human motor learning. Curr. Biol. 21:6 (2011), 480–484, 10.1016/j.cub.2011.01.069.
Stagg, C.J., Bachtiar, V., Johansen-Berg, H., What are we measuring with GABA Magnetic Resonance Spectroscopy?. Commun. Integr. Biol. 4:5 (2011), 573–575, 10.4161/cib.16213.
Stagg, C.J., Bestmann, S., Constantinescu, A.O., Moreno Moreno, L., Allman, C., Mekle, R., Woolrich, M., Near, J., Johansen-Berg, H., Rothwell, J.C., Relationship between physiological measures of excitability and levels of glutamate and GABA in the human motor cortex. J. Physiol. 589:23 (2011), 5845–5855, 10.1113/jphysiol.2011.216978.
Stagg, C., Rothman, D., Magnetic resonance spectroscopy: tools for neuroscience research and emerging clinical applications. 2013, Academic Press.
Stinear, C.M., Lang, C.E., Zeiler, S., Byblow, W.D., Advances and challenges in stroke rehabilitation. The Lancet Neurology 19:4 (2020), 348–360.
Stroemer, R.P., Kent, T.A., Hulsebosch, C.E., Neocortical neural sprouting, synaptogenesis, and behavioral recovery after neocortical infarction in rats. Stroke 26:11 (1995), 2135–2144.
Sumner, P., Edden, R.A.E., Bompas, A., Evans, C.J., Singh, K.D., More GABA, less distraction: a neurochemical predictor of motor decision speed. Nat. Neurosci. 13:7 (2010), 825–827.
Swayne, O.B.C., Rothwell, J.C., Ward, N.S., Greenwood, R.J., Stages of motor output reorganization after hemispheric stroke suggested by longitudinal studies of cortical physiology. Cereb. Cortex 18:8 (2008), 1909–1922, 10.1093/cercor/bhm218.
Talelli, P., Greenwood, R.J., Rothwell, J.C., Arm function after stroke: neurophysiological correlates and recovery mechanisms assessed by transcranial magnetic stimulation. Clin. Neurophysiol. 117:8 (2006), 1641–1659.
Teasell, R., Salbach, N.M., Foley, N., Mountain, A., Cameron, J.I., Jong, A.d., Acerra, N.E., Bastasi, D., Carter, S.L., Fung, J., Halabi, M.-L., Iruthayarajah, J., Harris, J., Kim, E., Noland, A., Pooyania, S., Rochette, A., Stack, B.D., Symcox, E., Timpson, D., Varghese, S., Verrilli, S., Gubitz, G., Casaubon, L.K., Dowlatshahi, D., Lindsay, M.P., Canadian Stroke Best Practice Recommendations: Rehabilitation, Recovery, and Community Participation following Stroke. Part One: Rehabilitation and Recovery Following Stroke; 6th Edition Update 2019. Int. J. Stroke 15:7 (2020), 763–788.
Thieme, H., Mehrholz, J., Pohl, M., Behrens, J., Dohle, C., Mirror therapy for improving motor function after stroke. Cochrane Database Syst. Rev., 3, 2012.
Todd, N., Zhang, Y., Power, C., Becerra, L., Borsook, D., Livingstone, M., McDannold, N., Modulation of brain function by targeted delivery of GABA through the disrupted blood-brain barrier. Neuroimage 189:September 2018 (2019), 267–275, 10.1016/j.neuroimage.2019.01.037.
Topolnik, L., Tamboli, S., The role of inhibitory circuits in hippocampal memory processing. Nat. Rev. Neurosci. 23:8 (2022), 476–492, 10.1038/s41583-022-00599-0.
Tremblay, S., Rogasch, N.C., Premoli, I., Blumberger, D.M., Casarotto, S., Chen, R., Di Lazzaro, V., Farzan, F., Ferrarelli, F., Fitzgerald, P.B., Hui, J., Ilmoniemi, R.J., Kimiskidis, V.K., Kugiumtzis, D., Lioumis, P., Pascual-Leone, A., Pellicciari, M.C., Rajji, T., Thut, G., Daskalakis, Z.J., Clinical utility and prospective of TMS–EEG. Clin. Neurophysiol. 130:5 (2019), 802–844, 10.1016/j.clinph.2019.01.001.
Turrigiano, G.G., The self-tuning neuron: synaptic scaling of excitatory synapses. Cell 135:3 (2008), 422–435.
Turrigiano, G., Too many cooks? Intrinsic and synaptic homeostatic mechanisms in cortical circuit refinement. Annu. Rev. Neurosci. 34 (2011), 89–103.
Turrigiano, G., Abbott, L.F., Marder, E., Activity-dependent changes in the intrinsic properties of cultured neurons. Science 264:5161 (1994), 974–977.
Turrigiano, G.G., Leslie, K.R., Desai, N.S., Rutherford, L.C., Nelson, S.B., Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature 391:6670 (1998), 892–896.
Turrigiano, G.G., Nelson, S.B., Homeostatic plasticity in the developing nervous system. Nat. Rev. Neurosci. 5:2 (2004), 97–107.
Wafford, K.A., Ebert, B., Gaboxadol - A new awakening in sleep. Curr. Opin. Pharmacol., 6(1 SPEC. ISS.), 30–36, 2006, 10.1016/j.coph.2005.10.004.
Wang, J.B., Aryal, M., Zhong, Q., Vyas, D.B., Airan, R.D., Noninvasive Ultrasonic Drug Uncaging Maps Whole-Brain Functional Networks. Neuron 100:3 (2018), 728–738.e7, 10.1016/j.neuron.2018.10.042.
Wang, X., Jin, Y., Hao, K., Synergies between synaptic and intrinsic plasticity in echo state networks. Neurocomputing 432 (2021), 32–43.
Ward, N.S., Brander, F., Kelly, K., Intensive upper limb neurorehabilitation in chronic stroke: outcomes from the Queen Square programme. J. Neurol. Neurosurg. Psychiatry 90:5 (2019), 498–506.
Winship, I.R., Murphy, T.H., In vivo calcium imaging reveals functional rewiring of single somatosensory neurons after stroke. J. Neurosci. 28:26 (2008), 6592–6606.
Winship, I.R., Murphy, T.H., Remapping the somatosensory cortex after stroke: insight from imaging the synapse to network. Neuroscientist 15:5 (2009), 507–524.
Wolf, S.L., Thompson, P.A., Winstein, C.J., Miller, J.P., Blanton, S.R., Nichols-Larsen, D.S., Morris, D.M., Uswatte, G., Taub, E., Light, K.E., The EXCITE stroke trial: comparing early and delayed constraint-induced movement therapy. Stroke 41:10 (2010), 2309–2315.
Wolff, S.B.E., Gründemann, J., Tovote, P., Krabbe, S., Jacobson, G.A., Müller, C., Herry, C., Ehrlich, I., Friedrich, R.W., Letzkus, J.J., Amygdala interneuron subtypes control fear learning through disinhibition. Nature 509:7501 (2014), 453–458.
Wu, B., Warnock, G., Zaiss, M., Lin, C., Chen, M., Zhou, Z., Mu, L., Nanz, D., Tuura, R., Delso, G., An overview of CEST MRI for non-MR physicists. EJNMMI Physics 3:1 (2016), 1–21.
Zich, C., Nowak, M., Hinson, E.L., Quinn, A.J., Woolrich, M.W., Stagg, C.J., Human motor cortical gamma activity relates to GABAergic signalling and to behaviour. BioRxiv, 2021, 2006–2021.
Ziemann, U., Muellbacher, W., Hallett, M., Cohen, L.G., Modulation of practice-dependent plasticity in human motor cortex. Brain 124:6 (2001), 1171–1181.