Induced neural phase precession through exogenous electric fields

Miles Wischnewski (), Harry Tran, Zhihe Zhao, Sina Shirinpour, Zachary J. Haigh, Jonna Rotteveel, Nipun D. Perera, Ivan Alekseichuk, Jan Zimmermann and Alexander Opitz ()
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Miles Wischnewski: University of Minnesota
Harry Tran: University of Minnesota
Zhihe Zhao: University of Minnesota
Sina Shirinpour: University of Minnesota
Zachary J. Haigh: University of Minnesota
Jonna Rotteveel: University of Minnesota
Nipun D. Perera: University of Minnesota
Ivan Alekseichuk: University of Minnesota
Jan Zimmermann: University of Minnesota
Alexander Opitz: University of Minnesota

Nature Communications, 2024, vol. 15, issue 1, 1-15

Abstract: Abstract The gradual shifting of preferred neural spiking relative to local field potentials (LFPs), known as phase precession, plays a prominent role in neural coding. Correlations between the phase precession and behavior have been observed throughout various brain regions. As such, phase precession is suggested to be a global neural mechanism that promotes local neuroplasticity. However, causal evidence and neuroplastic mechanisms of phase precession are lacking so far. Here we show a causal link between LFP dynamics and phase precession. In three experiments, we modulated LFPs in humans, a non-human primate, and computational models using alternating current stimulation. We show that continuous stimulation of motor cortex oscillations in humans lead to a gradual phase shift of maximal corticospinal excitability by ~90°. Further, exogenous alternating current stimulation induced phase precession in a subset of entrained neurons (~30%) in the non-human primate. Multiscale modeling of realistic neural circuits suggests that alternating current stimulation-induced phase precession is driven by NMDA-mediated synaptic plasticity. Altogether, the three experiments provide mechanistic and causal evidence for phase precession as a global neocortical process. Alternating current-induced phase precession and consequently synaptic plasticity is crucial for the development of novel therapeutic neuromodulation methods.

Date: 2024
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DOI: 10.1038/s41467-024-45898-5

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