Transcranial direct and alternating current stimulation produce distinct long-lasting changes in macaque V1 stimulus-induced gamma

Abstract

Transcranial direct or alternating current stimulation (tDCS or tACS) are used for the treatment of several cognitive disorders, many of which are due to imbalances in excitatory-inhibitory (E-I) interactions, but how stimulation affects the underlying cortical network remains an open question. In the primary visual cortex (V1), E-I interactions due to presentation of large gratings induce slow (20 Hz-35 Hz) and fast gamma (40 Hz-70 Hz) oscillations, which weaken with ageing and neurodegeneration and have been associated with different subtypes of interneurons. However, the effect of tDCS/tACS on stimulus-induced gamma is unknown. To investigate the impact of sustained stimulation on cortical E-I networks, we applied tDCS and tACS to two alert non-human primates while presenting full-screen gratings. We analyzed local field potentials before, during, and post-stimulation, focusing on gamma power and field-field coherency (FFC) as a measure of phase consistency. We found that tDCS significantly increased post-stimulation slow and fast gamma power, as well as FFC (60 Hz-100 Hz), with this effect lasting for approximately 1.5 hours. In contrast, tACS at 20 Hz consistently reduced slow gamma power, along with FFC (40 Hz-60 Hz). Our experimental observations were replicated in a physiologically realistic computational model of gamma generation by introducing targeted modifications to the synaptic weights within the simulated E-I network. Because long-lasting changes in local power and coherency strongly influence and modify cortical network, our findings reiterate the therapeutic and experimental potential of transcranial electrical stimulation to induce sustained modulation of cortical networks. SIGNIFICANCE STATEMENTNon-invasive transcranial current stimulation is used as a treatment for neural disorders, but how it modifies cortical dynamics to produce lasting changes is still debated. We recorded stimulus-induced gamma oscillations in macaque visual cortex as a readout of network interaction to study the effect of cortical stimulation. After stimulation over clinically relevant durations ([~]20 minutes), direct and alternating current increased and suppressed gamma power and connectivity, respectively, and this effect persisted for more than an hour. We also found that modifying the synaptic weights informed by earlier research in a realistic gamma-generating model could replicate our experimental results. Our results establish gamma rhythm as a useful indicator to study the effect of neurostimulation on neural circuitry.