Human motor cortical gamma activity relates to GABAergic signalling and to behaviour

Abstract

Gamma activity (γ, >30 Hz) is universally demonstrated across brain regions and species. However, the physiological basis and functional role of γ sub-bands (slow-γ, mid-γ, fast-γ) have been predominantly studied in rodent hippocampus; γ activity in the human neocortex is much less well understood. Here we combined neuroimaging and non-invasive brain stimulation to examine the properties of γ activity sub-bands in the primary motor cortex (M1), and their relationship to both local GABAergic activity and to motor learning. In 33 healthy individuals, we quantified movement-related γ activity in M1 using magnetoencephalography, assessed GABAergic signaling using transcranial magnetic stimulation (TMS), and estimated motor learning via a serial reaction time task. We characterised two distinct γ sub-bands (slow-γ, mid-γ) which show movement-related increase in activity during unilateral index finger movements and are characterised by distinct temporal-spectral-spatial profiles. Bayesian correlation analysis revealed strong evidence for a positive relationship between slow-γ (~30-60Hz) peak frequency and endogenous GABA signalling during movement preparation (as assessed using the TMS-metric short interval intracortical inhibition). There was also moderate evidence for a relationship between power of the movement-related mid-γ activity (60-90Hz) and motor learning. These relationships were neurochemically- and frequency-specific. These data provide new insights into the neurophysiological basis and functional roles of γ activity in human M1 and allow the development of a new theoretical framework for γ activity in the human neocortex.

Temporal Signature of Task‐Specificity in Isolated Focal Laryngeal Dystonia

“…12,13,[60][61][62][63][64][65] Furthermore, using GABAergic neuroreceptor mapping, loss of inhibition has been demonstrated in these prefrontal and parietal regions across different forms of dystonia. [66][67][68][69] As gamma oscillations depend on synaptic inhibition driven by GABAergic interneurons, 44,45 our finding of aberrant gamma synchronization in regions previously reported to have loss of inhibition points to important consequences of altered prefrontal-parietal neural dynamics on the execution of motor programs in patients with dystonia.…”

“…Gamma oscillations are generated by fast‐spiking inhibitory interneurons 43‐45 and contribute to balancing basal ganglia‐thalamo‐cortical excitation 46,47 . These oscillations play an important role in temporal encoding, sensory processes in terms of binding features into a coherent percept, storage and recall of information, and feedback processing, including those during movement execution 48‐53 .…”

An integrated measure of GABA to characterize post-stroke plasticity

“…Driving gamma frequency oscillations using transcranial Alternate Current Stimulation (tACS) significantly decreases local resting GABA A inhibition, which is closely related with performance in a motor learning task ( Nowak et al, 2017 ). Interestingly, the peak frequency of slow gamma sub-band (∼30-60 Hz) seems to be positively related with endogenous GABA signaling during movement preparation whereases the power of the mid gamma sub-band (60–90 Hz) predicted performance in a subsequent motor task ( Zich et al, 2021 ). Some MRS- and PET-MEG studies showed a positive correlation between gamma oscillation frequency and both resting GABA concentration and GABA A receptor density in the visual cortex.…”