tDCS-induced alterations in GABA concentration within primary motor cortex predict motor learning and motor memory: a 7 T magnetic resonance spectroscopy study

Abstract

Transcranial direct current stimulation (tDCS) is a non-invasive brain stimulation technique that alters cortical excitability in a polarity specific manner and has been shown to influence learning and memory. tDCS may have both on-line and after-effects on learning and memory, and the latter are thought to be based upon tDCS-induced alterations in neurochemistry and synaptic function. We used ultra-high-field (7 T) magnetic resonance spectroscopy (MRS), together with a robotic force adaptation and de-adaptation task, to investigate whether tDCS-induced alterations in GABA and Glutamate within motor cortex predict motor learning and memory. Note that adaptation to a robot-induced force field has long been considered to be a form of model-based learning that is closely associated with the computation and 'supervised' learning of internal 'forward' models within the cerebellum. Importantly, previous studies have shown that on-line tDCS to the cerebellum, but not to motor cortex, enhances model-based motor learning. Here we demonstrate that anodal tDCS delivered to the hand area of the left primary motor cortex induces a significant reduction in GABA concentration. This effect was specific to GABA, localised to the left motor cortex, and was polarity specific insofar as it was not observed following either cathodal or sham stimulation. Importantly, we show that the magnitude of tDCS-induced alterations in GABA concentration within motor cortex predicts individual differences in both motor learning and motor memory on the robotic force adaptation and de-adaptation task.

Keywords: Biological Sciences; Cognitive Sciences; Force adaptation; GABA; Magnetic resonance spectroscopy; Motor learning; Neuroscience; Psychological; tDCS.

Fig. 1

A graphical representation of the procedure.

Fig. 2

a. A graphical representation of the display used within the force adaptation task (left) and an illustration of the measurement of the perpendicular error from a straight line. b. Example trajectory of the first bin and the last bin (bin size = 8 trials, blue: force trials; red: catch trials). Note that, whereas force trials decrease in error with practice, errors during catch trials increase. c. Binned results of the force adaptation task of the adaptation phase (top: force trials; bottom: catch trials) and the de-adaptation phase for each group (solid line: force field; dashed line: null field). Groups 1, 2, and 3 each subsequently went on to receive anodal, cathodal, or sham tDCS in the following MRS session.

Fig. 3

a. Left M1 GABA changes induced by anodal, cathodal, and sham tDCS. The box limits indicate the 25th and 75th percentiles, and the line inside the box shows the median. The whiskers indicate the range of the data within 1.5 times of the box width. b & c. Illustrate the relationship between MRS-GABA concentration change ratios induced by anodal tDCS and the movement error measured in the adaptation (b) and the de-adaptation phase (c) of the robot force adaptation task.