Altered Bidirectional Plasticity and Reduced Implicit Motor Learning in Concussed Athletes
Abstract
Persistent motor/cognitive alterations and increased prevalence of Alzheimer's disease are known consequences of recurrent sports concussions, the most prevalent cause of mild traumatic brain injury (TBI) among youth. Animal models of TBI demonstrated that impaired learning was related to persistent synaptic plasticity suppression in the form of long-term potentiation (LTP) and depression (LTD). In humans, single and repeated concussive injuries lead to lifelong and cumulative enhancements of gamma-aminobutyric acid (GABA)-mediated inhibition, which is known to suppress LTP/LTD plasticity. To test the hypothesis that increased GABAergic inhibition after repeated concussions suppresses LTP/LTD and contributes to learning impairments, we used a paired associative stimulation (PAS) protocol to induce LTP/LTD-like effects in primary motor cortex (M1) jointly with an implicit motor learning task (serial reaction time task, SRTT). Our results indicate that repeated concussions induced persistent elevations of GABA(B)-mediated intracortical inhibition in M1, which was associated with suppressed PAS-induced LTP/LTD-like synaptic plasticity. This synaptic plasticity suppression was related to reduced implicit motor learning on the SRTT task relative to normal LTP/LTD-like synaptic plasticity in unconcussed teammates. These findings identify GABA neurotransmission alterations after repeated concussions and suggest that impaired learning after multiple concussions could at least partly…
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The short-lived cTBS response in this study contradicts the previous finding of persistent motor cortex LTD- and LTP-like deficits in the chronic phase following sport concussion.
“The inability of the injured brain to respond to cTBS appears short-lived, however, which is in contradiction with the previous study by De Beaumont and collaborators (2012) who showed persistent motor cortex LTD- and LTP-like deficits in the chronic phase following sport concussion.”
From Theta burst stimulation to characterize changes in brain plasticity following mild traumatic brain injury: A proof-of-principle study (2015) · cites this paper as De Beaumont et al., 2012
Chronic alterations in synaptic plasticity, possibly reflecting faulty LTP- and LTD-like mechanisms, were found after multiple concussions and were associated with intracortical inhibition abnormalities.
“Moreover, chronic alterations in synaptic plasticity, possibly reflecting faulty long term potentiation (LTP) – and long term depression (LTD) - like mechanisms were found after multiple concussions, and were associated with intracortical inhibition abnormalities (De Beaumont et al., 2012).”
From Theta burst stimulation to characterize changes in brain plasticity following mild traumatic brain injury: A proof-of-principle study (2015) · cites this paper as De Beaumont et al., 2012
De Beaumont et al. (2012) reported that increased silent period durations in concussed athletes, presumably reflecting faulty GABAB transmission, were negatively correlated with the level of synaptic plasticity induced with paired associative stimulation.
“De Beaumont et al. (2012) reported that increased silent period durations in concussed athletes, presumably reflecting faulty GABAB transmission, were negatively correlated with the level of synaptic plasticity induced with paired associative stimulation.”
From Theta burst stimulation to characterize changes in brain plasticity following mild traumatic brain injury: A proof-of-principle study (2015) · cites this paper as De Beaumont et al., 2012
mTBI influences LTD-like mechanisms.
“Second, previous assessment of neuroplasticity was limited to an intervention thought to induce long-term potentiation (LTP)-like effects, whereas previous work from our group (Opie et al. 2019) and others (De Beaumont et al. 2012) suggests mTBI also influences long-term-depression (LTD)-like mechanisms.”
From Mild traumatic brain injury alters function in the dorsolateral prefrontal cortex: a TMS-EEG study (2025) · cites this paper as De Beaumont et al. 2012
Previous assessment of neuroplasticity after mTBI was limited to an intervention thought to induce LTP-like effects.
“Second, previous assessment of neuroplasticity was limited to an intervention thought to induce long-term potentiation (LTP)-like effects, whereas previous work from our group (Opie et al. 2019) and others (De Beaumont et al. 2012) suggests mTBI also influences long-term-depression (LTD)-like mechanisms.”
From Mild traumatic brain injury alters function in the dorsolateral prefrontal cortex: a TMS-EEG study (2025) · cites this paper as De Beaumont et al. 2012
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Modifying motor learning through gating and homeostatic metaplasticity
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Mechanisms Underlying the Rules for Associative Plasticity at Adult Human Neocortical Synapses
Verhoog, M. B., Goriounova, N. A., Obermayer, J., Stroeder, J., Hjorth, J. J. J., Testa-Silva, G., Baayen, J. C., de Kock, C. P. J., Meredith, R. M., & Mansvelder, H. D. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.3158-13.2013 · Cited by 127 · see citing works
Tremblay, S., Vernet, M., Bashir, S., Pascual-Leone, A., & Théoret, H. (2015) · Restorative Neurology and Neuroscience · doi:10.3233/rnn-140459 · Cited by 14 · see citing works
Self-citationMild traumatic brain injury alters function in the dorsolateral prefrontal cortex: a TMS-EEG study
Moore, E., Webb, E., Sasaki, R., Rogasch, N. C., Foo, N., Semmler, J. G., & Opie, G. M. (2025) · doi:10.1101/2025.05.22.655676 · Cited by 3 · see citing works
“…previous assessment of neuroplasticity was limited to an intervention thought to induce long-term potentiation (LTP)-like effects, whereas previous work from our group (Opie et al. 2019) and others (De Beaumont et al. 2012) suggests mTBI also influences long-term-depression (LTD)-like mechanisms.”
Influential
- Authors
- De Beaumont, L., Tremblay, S., Poirier, J., Lassonde, M., & Theoret, H.
- Affiliations
- Université de Montréal (CA)
- Douglas Mental Health University Institute (CA)
- Centre Hospitalier Universitaire Sainte-Justine (CA)
- Venue
- Cerebral Cortex
- Publisher
- Oxford University Press (OUP)
- Published
- 2011-05-13
- Volume
- 22
- Issue
- 1
- Pages
- 112-121
- ISSN
- 1047-3211 (ISSN-L)
- 1460-2199
- OpenAlex
- W2104674917
- Cited by
- 133
- References
- 4
- Citations by year
- 2026: 2 · 2025: 5 · 2024: 9 · 2023: 7 · 2022: 5 · 2021: 4 · 2020: 9 · 2019: 13 · 2018: 10 · 2017: 11 · 2016: 13 · 2015: 16 · 2014: 9 · 2013: 8 · 2012: 12
- FWCI
- 6.95
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Cerebral Cortex (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Canadian Institutes of Health Research
- Topics
- Health Sciences › Medicine › Epidemiology › Traumatic Brain Injury Research
- Life Sciences › Neuroscience › Neurology › Transcranial Magnetic Stimulation Studies
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- sports-related concussion, mild traumatic brain injury, repeated concussions, synaptic plasticity, long-term potentiation, long-term depression, GABAergic inhibition, GABAB receptors, intracortical inhibition, primary motor cortex, implicit motor learning, serial reaction time task, paired associative stimulation, athletes
- MeSH terms
- Adult, Analysis of Variance, Athletic Injuries, Brain Concussion, Electric Stimulation, Electromyography, Football, Humans, Learning Disabilities, Male, Methionine, Motor Activity, Motor Cortex, Neural Inhibition, Neuronal Plasticity, Neuropsychological Tests, Psychomotor Performance, Reaction Time, Severity of Illness Index, Statistics as Topic, Valine, Evoked Potentials, Motor, Brain-Derived Neurotrophic Factor, Polymorphism, Single Nucleotide, Transcranial Magnetic Stimulation, Young Adult
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