Spatiotemporal network dynamics and structural correlates in the human cerebral cortex in vitro

Highlights

• Human cortical slices express spontaneous slow rhythmic activity in vitro.
• Deep layers lead the initiation of spontaneous slow rhythmic activity in human cortical slices.
• Wave propagation speed and excitability in human tissue are higher than in other species.
• Progressive GABAergic blockade results in higher firing rates, network recruitment and propagation, and infraslow rhythmicity
• Emergent activity in human cortical slices provides a model for investigating cortical mechanisms and neuromodulation.

Abstract

Elucidating human cerebral cortex function is essential for understanding the physiological basis of both healthy and pathological brain states. We obtained extracellular local field potential recordings from slices of neocortical tissue from refractory epilepsy patients. Multi-electrode recordings were combined with histological information, providing a two-dimensional spatiotemporal characterization of human cortical dynamics in control conditions and following modulation of the excitation/inhibition balance. Slices expressed spontaneous rhythmic activity consistent with slow wave activity, comprising alternating active (Up) and silent (Down) states (Up-duration: 0.08 ± 0.03 s, Down-duration: 2.62 ± 2.12 s, frequency: 0.75 ± 0.39 Hz). Up states propagated from deep to superficial layers, with faster propagation speeds than in other species (vertical: 64.6 mm/s; horizontal: 65.9 mm/s). GABA_A blockade progressively transformed the emergent activity into epileptiform discharges, marked by higher firing rates, faster network recruitment and propagation, and infraslow rhythmicity (0.01 Hz). This dynamical characterization broadens our understanding of the mechanistic organization of the human cortical network at the micro- and mesoscale.