GABAergic Modulation in Movement Related Oscillatory Activity: A Review of the Effect Pharmacologically and with Aging

Groth, Christopher L.; Singh, Anneliese A.; Zhang, Qiang; Berman, Brian D.; Narayanan, Nandakumar S.

doi:10.5334/tohm.655

Cited by 5 publications

(6 citation statements)

References 97 publications

(230 reference statements)

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“… 49 It is established that intrinsic inhibitory GABAergic modulation via interneurons is essential for controlling movement in the healthy brain. 50 Administering a GABA A agonist to healthy participants increased MEG beta power in the motor cortex. 49 Another study found that GABA A - and gap junction-blockers reduced beta oscillation amplitude.…”

Section: Discussionmentioning

confidence: 99%

The cortical neurophysiological signature of amyotrophic lateral sclerosis

Trubshaw,

Gohil,

Yoganathan

et al. 2024

Brain Communications

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The progressive loss of motor function characteristic of amyotrophic lateral sclerosis is associated with widespread cortical pathology extending beyond primary motor regions. Increasing muscle weakness reflects a dynamic, variably compensated brain network disorder. In the quest for biomarkers to accelerate therapeutic assessment, the high temporal resolution of magnetoencephalography is uniquely able to non-invasively capture micro-magnetic fields generated by neuronal activity across the entire cortex simultaneously. This study examined task-free magnetoencephalography to characterise the cortical oscillatory signature of amyotrophic lateral sclerosis for potential as a pharmacodynamic biomarker. Eight-ten minutes of magnetoencephalography in the task-free, eyes-open state was recorded in amyotrophic lateral sclerosis (n=36) and healthy age-matched controls (n=51), followed by a structural MRI scan for co-registration. Extracted magnetoencephalography metrics from the delta, theta, alpha, beta, low-gamma, high-gamma frequency bands included oscillatory power (regional activity), 1/f exponent (complexity) and amplitude envelope correlation (connectivity). Groups were compared using a permutations-based general linear model with correction for multiple comparisons and confounders. To test whether the extracted metrics could predict disease severity, a Random Forest Regression model was trained and evaluated using nested Leave-One-Out Cross-Validation. Amyotrophic lateral sclerosis was characterised by reduced sensorimotor beta band and increased high-gamma band power. Within the premotor cortex, increased disability was associated with a reduced 1/f exponent. Increased disability was more widely associated with increased global connectivity in the delta, theta, and high-gamma bands. Intra-hemispherically, increased disability scores were particularly associated with increases in temporal connectivity and inter-hemispherically with increases in frontal and occipital connectivity. The Random Forest model achieved a coefficient of determination (R2) of 0.24. The combined reduction in cortical sensorimotor beta and rise in gamma power is compatible with the established hypothesis of loss of inhibitory, GABAergic interneuronal circuits in pathogenesis. A lower 1/f exponent potentially reflects a more excitable cortex and a pathology unique to amyotrophic lateral sclerosis when considered with the findings published in other neurodegenerative disorders. Power and complexity changes corroborate with the results from paired-pulse transcranial magnetic stimulation. Increased magnetoencephalography connectivity in worsening disability is thought to represent compensatory responses to a failing motor system. Restoration of cortical beta and gamma band power has significant potential to be tested in an experimental medicine setting. Magnetoencephalography-based measures have potential as sensitive outcome measures of therapeutic benefit in drug trials and may have wider diagnostic value with further study, including as predictive markers in asymptomatic carriers of disease-causing genetic variants.

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Section: Discussionmentioning

confidence: 99%

The cortical neurophysiological signature of amyotrophic lateral sclerosis

Trubshaw,

Gohil,

Yoganathan

et al. 2024

Brain Communications

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“…Excitability can be modulated by change in the Gamma-aminobutyric acid (GABA) / glutamate balance in the brain (25). It is also known that the GABA concentration modulates the beta frequencies and power in the sensorimotor areas of the brain (26, 27). Furthermore it has been shown that the pre-execution part of a movement (ERD) and the reaffirmation of limb position after a movement (ERS) reacts differently to drugs modulating the GABA receptor (28) this would perhaps suggest that our finding are modulated by more than just GABA.…”

Section: Discussionmentioning

confidence: 99%

“…In this study we investigate the neural oscillations occurring in the beta band (13)(14)(15)(16)(17)(18)(19)(20)(21)(22)(23)(24)(25)(26)(27)(28)(29)(30) of the sensorimotor cortex in both active and passive movement tasks, using magnetoencephalography (MEG). This enables us to investigate whether ALS impacts only the movement output or also leads to changes in processing of input to the sensorimotor cortex.…”

Section: Introductionmentioning

confidence: 99%

Movement-related beta modulation in amyotrophic lateral sclerosis depends on muscle strength: A magnetoencephalography study

Stærmose

Andersen

Dalal

et al. 2022

Preprint

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Background: Movement related cortical beta (13-30 Hz) modulation is fundamental in the preparation and execution of movement. This oscillatory modulation is altered in amyotrophic lateral sclerosis (ALS) during active movement, with reports of both decreased and increased beta band power. These beta band changes have never been examined in a proprioceptive paradigm in ALS. Methods: Using magnetoencephalography (MEG) we examined 11 ALS patients and 12 healthy participants. We recorded beta band activity during a session of active movement of the dominant hand index finger, using a visual cue. We also recorded activity during a passive movement of the same finger using a MEG compatible pneumatically activated device. All ALS patients underwent a clinical examination including an estimation of the muscle strength of the arm used for the experiment. Results: Using an analysis of variance (ANOVA), we find that movement related beta band power is modified by ALS and the amplitude of beta power is decreased, both for the active and passive movements. We also find that the beta band power modulation depends on the muscle strength of the arm used, with movement related power amplitude being decrease in patients with arm weakness. This was observed for both active and passive movement. Conclusion: ALS patients show decreased movement related beta band amplitude compared to the healthy control group. The decrease seems to depend on disease severity. These results show that ALS affects the motor outputs and sensory inputs of the sensorimotor cortex and that the modulation differs depending on disease severity. Severity dependent modulation of beta power could be related to disturbance in excitatory/inhibitory intracortical circuitry.

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“…In MDD patients, we particularly focused on the retardation factor scores, and we found that the retardation scores were inversely correlated with PMBR (r = -0.365, p = 0.002). Moreover, given that healthy aging has an impact on beta oscillations [30][31][32][33][34][35][36][37][38][39], the correlations remained signi cant (r = -0.374, p = 0.006, FDR corrected) after controlling sex, age and education (Fig. 5A).…”

Section: Association Between Pmbr and Clinical Assessmentsmentioning

confidence: 99%

“…Research in healthy individuals demonstrated that the decrease of PMBR leads to a slower movement state [28], consistent with reduced movement-related beta activity in Parkinson's disease (PD) [29]. Many physiological or pathological factors in uence beta oscillations, such as healthy ageing [30][31][32][33][34][35][36][37][38][39]. Previous studies found that poor motor performance in healthy older adults is related to changes in beta oscillations.…”

Section: Introductionmentioning

confidence: 95%

Attenuated post-movement beta rebound reflects psychomotor alterations in major depressive disorder during a simple visuomotor task: a MEG study

Xia

Dai³

et al. 2022

Preprint

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Background Psychomotor alterations are a common symptom in patients with major depressive disorder (MDD). The primary motor cortex (M1) plays a vital role in the mechanism of psychomotor alterations. Post-movement beta rebound (PMBR) in the sensorimotor cortex is abnormal in patients with motor abnormalities. However, the changes in M1 beta rebound in patients with MDD remain unclear. This study aimed to primarily explore the relationship between psychomotor alterations and PMBR in MDD. Methods 132 subjects were enrolled in the study, comprising 65 healthy controls (HCs) and 67 MDD patients. All participants performed a simple right-hand visuomotor task during MEG scanning. PMBR was measured in the left M1 at the source reconstruction level with the time-frequency analysis method. Retardation factor scores and neurocognitive test performance, including the Digit Symbol Substitution Test (DSST), the Making Test Part A (TMT-A), and the Verbal Fluency Test (VFT), were used to measure psychomotor functions. Pearson correlation analyses were used to assess relationships between PMBR and psychomotor alterations in MDD. Results The MDD group showed worse neurocognitive performance than the HC group in all three neurocognitive tests. The PMBR was diminished in patients with MDD compared to HCs. In a group of MDD patients, the reduced PMBR was negatively correlated with retardation factor scores. Further, there was a positive correlation between the PMBR and DSST scores. PMBR is negatively associated with the TMT-A scores. Conclusion Our findings suggested that the attenuated PMBR in M1 could illustrate the psychomotor disturbance in MDD, possibly contributing to clinical psychomotor symptoms and deficits of cognitive functions.

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GABAergic Modulation in Movement Related Oscillatory Activity: A Review of the Effect Pharmacologically and with Aging

Cited by 5 publications

References 97 publications

The cortical neurophysiological signature of amyotrophic lateral sclerosis

The cortical neurophysiological signature of amyotrophic lateral sclerosis

Movement-related beta modulation in amyotrophic lateral sclerosis depends on muscle strength: A magnetoencephalography study

Attenuated post-movement beta rebound reflects psychomotor alterations in major depressive disorder during a simple visuomotor task: a MEG study

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