GABA Modulates Frequency-Dependent Plasticity in Humans.

Caroline A. Lea-Carnall,Stephen R. Williams,Marcelo A. Montemurro,Wael El-Deredy,Laura M. Parkes,Nelson J. Trujillo-Barreto,Faezeh Sanaei-Nezhad

doi:10.1016/j.isci.2020.101657

Caroline A. Lea-Carnall, Stephen R. Williams + Show 5 more

Open Access

https://doi.org/10.1016/j.isci.2020.101657

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Abstract

SummaryFrequency-dependent reorganization of the primary somatosensory cortex, together with perceptual changes, arises following repetitive sensory stimulation. Here, we investigate the role of GABA in this process. We co-stimulated two finger tips and measured GABA and Glx using magnetic resonance (MR) spectroscopy at the beginning and end of the stimulation. Participants performed a perceptual learning task before and after stimulation. There were 2 sessions with stimulation frequency either at or above the resonance frequency of the primary somatosensory cortex (23 and 39 Hz, respectively). Perceptual learning occurred following above resonance stimulation only, while GABA reduced during this condition. Lower levels of early GABA were associated with greater perceptual learning. One possible mechanism underlying this finding is that cortical disinhibition “unmasks” lateral connections within the cortex to permit adaptation to the sensory environment. These results provide evidence in humans for a frequency-dependent inhibitory mechanism underlying learning and suggest a mechanism-based approach for optimizing neurostimulation frequency.

Highlights

Plasticity is the process of altering synaptic efficacy via long-term potentiation (LTP) or long-term depression (LTD) which result in strengthening or weakening of the synapses, respectively (Malenka and Bear, 2004)
Perceptual learning occurred following above resonance stimulation only, while gamma-aminobutyric acid (GABA) reduced during this condition
Lower levels of early GABA were associated with greater perceptual learning

Summary

Introduction

Plasticity is the process of altering synaptic efficacy via long-term potentiation (LTP) or long-term depression (LTD) which result in strengthening or weakening of the synapses, respectively (Malenka and Bear, 2004). It has been shown that high-frequency tactile stimulation (20 Hz) delivered to the tip of the index finger improved 2-point tactile discrimination while low-frequency stimulation (1 Hz) impaired performance which was attributed to LTP-like changes in the primary somatosensory cortex (SI) (Ragert et al, 2008) It was noted in our recent work that 20 Hz is close to the stimulation frequency that evokes the maximum neural response of the somatosensory cortex, the resonance frequency (Snyder, 1992; Tobimatsu et al, 1999), and that the impaired performance at 1 Hz applied to higher off-resonance frequencies (39 Hz) using tactile stimulation applied to two digits rather than one (Lea-Carnall et al, 2017), this is likely via different mechanisms.

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