Stochastic resonance effects reveal the neural mechanisms of transcranial magnetic stimulation

Abstract

Transcranial magnetic stimulation (TMS) is a popular method for studying causal relationships between neural activity and behavior. However, its mode of action remains controversial, and so far there is no framework to explain its wide range of facilitatory and inhibitory behavioral effects. While some theoretical accounts suggest that TMS suppresses neuronal processing, other competing accounts propose that the effects of TMS result from the addition of noise to neuronal processing. Here we exploited the stochastic resonance phenomenon to distinguish these theoretical accounts and determine how TMS affects neuronal processing. Specifically, we showed that online TMS can induce stochastic resonance in the human brain. At low intensity, TMS facilitated the detection of weak motion signals, but with higher TMS intensities and stronger motion signals, we found only impairment in detection. These findings suggest that TMS acts by adding noise to neuronal processing, at least in an online TMS protocol. Importantly, such stochastic resonance effects may also explain why TMS parameters that under normal circumstances impair behavior can induce behavioral facilitations when the stimulated area is in an adapted or suppressed state.

Figure 1.

Stochastic resonance. Top, When the signal (picture of a flag) is weak, it is difficult to recognize the image, as only pixels at the edges of the differently colored regions pass the threshold. Bottom, Adding high levels of noise to the image drowns out the signal, and recognition remains difficult. Middle, Recognition can be best when an optimal amount of noise is added. This is because the noise pushes some signal pixels above the threshold.

Figure 2.

A, On each trial, participants were instructed to discriminate the direction of motion of a random dot stimulus where a proportion of dots moved either left or right (black arrows), while the direction of remaining dots was random (gray arrows). We tested two levels of coherence affording 60% and 85% correct (left and right panels), respectively. TMS was delivered simultaneously with stimulus onset at one of three intensities or not at all. B, Percentage correct discrimination plotted for the two coherence levels and the four levels of TMS intensity. The asterisks above a bar indicate that performance in this condition was significantly (two-tailed t test p < 0.05) different from trials without TMS (black bars).