Stimulating the brain with high frequency electrical noise can supersede the beneficial effects observed from transcranial direct current stimulation, either anodal or cathodal (as well as those observed from sham stimulation), in perceptual learning, as newly reported by Fertonani, Pirully & Miniussi in the Journal of Neuroscience. The authors suggest that transcranial random noise stimulation may work by preventing those neurophysiological homeostatic mechanisms that govern ion channel conductance from rebalancing the changes induced by prolonged practice on this perceptual learning task.
Over several experiments, a total of 99 subjects underwent transcranical random noise stimulation, consisting of an AC current of 1.5 mA intensity at random frequencies between 0.1 to 100 Hz (for low-frequency stimulation) or 100-640 Hz (for high frequency stimulation). Direct current stimuliation was similarly provided at 1.5mA. (In case you wanted to replicate this experiment at home, the company that sells the device used in this study has made it clear they’re perfectly fine with selling you one for your own personal use ["Unser Service für Sie persönliche Beratung"] – not that I’m recommending that!) At any rate, no artifactual visual perceptions were induced by these stimulations, and all women were tested during their follicular menstrual phase (at which point their cortical excitability is most similar to that of men). Stimulation was provided for approximately 4 minutes over the occipital lobe (or vertex, for control stimulation conditions) during each block of a visual orientation discrimination task. Subjects simply had to say whether a given stimulus was tilted clockwise or counterclockwise relative to a preceding reference stimulus.
Over the course of five successive blocks of this task, subjects undergoing high frequency random electrical stimulation performed consistently better than subjects undergoing any other kind of stimulation, including low frequency random stimulation, cathodal or anodal direct current, control stimulation to the vertex, or sham stimulation. The rate of change in performance was also increased in high frequency random stimulation relative to anodal direct current, which yielded no apparent learning effect – even though anodal direct current is typically thought to enhance neural activity and is in other domains helpful to performance. The authors even replicated these advantages of high frequency random stimulation (just relative to sham stimulation) in a second experiment.
And in case you think these effects are driven by demand characteristics, note that participants failed to correctly guess whether they received actual stimulation or placebo (sham) stimulation – indicating these effects are unlikely to be driven by any explicit perception arising from electrical stimulation. Moreover, anodal and cathodal direct current stimulation was associated with an increased report of itchiness, irritation and burning than the other conditions. In no case did reported sensations during stimulation correlate with performance (absolute R values <.1), and random noise stimulation was never differentiable from sham stimulation, neither in terms of explicit report nor subject ratings of various subjective experiences like itching, burning, irritation, pain, heat, or "iron taste".
So, how on earth is this happening? Fertonani et al suggest that repeated random stimulation at a high frequency can actually support temporal summation of neural activity, whereas anodal direct current will induce a facilitation that is followed by homeostatic re-regulation of the ion channel conductances and thus ultimately reduce neuronal excitability. I think the authors are reasonably careful to acknowledge that this particular scenario may be highly dependent on a number of factors, including the exact placement of reference electrodes, the exact stimulation parameters used, as well as possibly more interesting things like the cytoarchitectural features of the areas undergoing stimulation.
Nonetheless, Fertonani can't resist some speculations about another possible explanation for these effects: stochastic resonance. Stochastic resonance refers to the (apparently) paradoxical phenomenon by which the signal to noise ratio in a thresholded system can sometimes be enhanced following the addition of broadband noise, which may provide additional excitation that allows nascent signals to reach a criterial threshold for experiencing positive feedback. Originally, stochastic resonance was proposed as an explanation for the presence of ice ages throughout geological history, and has subsequently been (hypothesized to explain some neuropsychiatric phenomena; indeed, it has been observed in hippocampus, and a number of sensory regions). Fertonani et al carefully suggest that random noise stimulation could have beneficial effects by pushing the neuronal population “over the threshold” required for some form of positive feedback (perhaps due to recurrent activation or perhaps thalamocortical in nature) or by preferentially recruiting additional subthreshold neurons to participate in such neuronal population coding.
This of course is not mutually exclusive with the idea that random noise stimulation eliminated homeostatic mechanisms for regulating ion channel conductances, but I do tend to prefer the stochastic resonance interpretation. It’s unclear to me why anodal direction current stimulation should ever benefit performance if these homeostatic mechanisms are so perniciously counterbalancing any changes that are being induced, unless such homeostatic mechanisms are simply more operative in visual cortex than over other regions.
An alternative explanation, unmentioned by Fertonani et al., is that their transcranial random noise stimulation effectively acted as a biological version of the simulated annealing process sometimes used to improve learning in artificial neural networks. In simulated annealing, the injection of random noise during learning can bump the system out of local minima in the energy landscape and promote better long-term performance. Although orientation discrimination is presumably a well-learned skill in the adults used in this experiment, there may be task-specific associative learning that is occurring over the course of the experiment, and such learning could conceivably be enhanced through this kind of annealing process.
At the same time, there are new reports that random noise stimulation is not effective in improving performance in tasks relying crucially on more anterior cortical regions – including everyone’s favorite area, the DLPFC, in everyone’s favorite task, the n-back. It is difficult to integrate these failures with a weight-based interpretation of short-term synaptic facilitation demonstrated by Itskov et al to be important for stabilizing attractor states in the prefrontal cortex. Indeed, random noise stimulation may decrease motor-related BOLD responses even as it increases corticospinal excitability. These confusing and sometimes conflicting results pose a significant challenge to any explanation of random noise stimulation invoking stochastically resonant, or annealing-sensitive, neurobiological mechanisms.