Amplifying post-stimulation oscillatory dynamics by engaging synaptic plasticity with periodic stimulation: a modelling study

Periodic brain stimulation (PBS) techniques, either intracranial or non-invasive, electrical or magnetic, represent promising neuromodulatory tools for the treatment of neurological and neuropsychiatric disorders. Through the modulation of endogenous oscillations, PBS may engage synaptic plasticity, hopefully leading to persistent lasting effects. However, stabilizing such effects represents an important challenge: the interaction between induced electromagnetic fields and neural circuits may yield highly variable responses due to heterogeneous neuronal and synaptic biophysical properties, limiting PBS clinical potential. In this study, we explored the conditions on which PBS leads to amplified post-stimulation oscillatory power, persisting once stimulation has been turned off. We specifically examined the effects of heterogeneity in neuron time scales on post-stimulation dynamics in a population of balanced leaky-integrated and fire (LIF) neurons that exhibit synchronous-irregular spiking activity. Our analysis reveals that such heterogeneity enables PBS to engage synaptic plasticity, amplifying post-stimulation power. Our results show that such post-stimulation aftereffects result from selective frequency- and cell-type-specific synaptic modifications. We evaluated the relative importance of stimulation-induced plasticity amongst and between excitatory and inhibitory populations. Our results indicate that heterogeneity in neurons time scales and synaptic plasticity are both essential for stimulation to support post-stimulation aftereffects, notably to amplify the power of endogenous rhythms.