Direct cortical stimulation induces short-term plasticity of neural oscillations in humans.

Patterned brain stimulation is commonly employed as a tool for eliciting plasticity in brain circuits and treating neuropsychiatric disorders. Although widely used in clinical settings, there remains a limited understanding of how stimulation-induced plasticity influences neural oscillations and their interplay with the underlying baseline functional architecture. To address this question, we applied 15 minutes of 10Hz focal electrical simulation, a pattern identical to 'excitatory' repetitive transcranial magnetic stimulation (rTMS), to 14 medically-intractable epilepsy patients undergoing intracranial electroencephalographic (iEEG). We quantified the spectral features of the cortico-cortical evoked potential (CCEPs) in these patients before and after stimulation. We hypothesized that for a given region the temporal and spectral components of the CCEP predicted the location and degree of stimulation-induced plasticity. Across patients, low frequency power (alpha and beta) showed the broadest change, while the magnitude of change was stronger in high frequencies (beta and gamma). Next we demonstrated that regions with stronger baseline evoked spectral responses were more likely to undergo plasticity after stimulation. These findings were specific to a given frequency in a specific temporal window. Post-stimulation power changes were driven by the interaction between direction of change in baseline power and temporal window of change. Finally, regions exhibiting early increases and late decreases in evoked baseline power exhibited power changes after stimulation and were independent of stimulation location. Together, these findings that time-frequency baseline features predict post-stimulation plasticity effects demonstrate properties akin to Hebbian learning in humans and extend this theory to the temporal and spectral window of interest. These findings can help improve our understanding of human brain plasticity and lead to more effective brain stimulation techniques.