Abstract

In a quest for direct evidence of oscillation entrainment, we analyzed intracerebral electroencephalographic recordings obtained during intracranial electrical stimulation in a cohort of three medication-resistant epilepsy patients tested pre-surgically. Spectral analyses of non-epileptogenic cerebral sites stimulated directly with high frequency electrical bursts yielded episodic local enhancements of frequency-specific rhythmic activity, phase-locked to each individual pulse. These outcomes reveal an entrainment of physiological oscillatory activity within a frequency band dictated by the rhythm of the stimulation source. Our results support future uses of rhythmic stimulation to elucidate the causal contributions of synchrony to specific aspects of human cognition and to further develop the therapeutic manipulation of dysfunctional rhythmic activity subtending the symptoms of some neuropsychiatric conditions.

Highlights

  • Magnetoencephalography (MEG)[22] recordings have contributed to ignite an interest in causally exploring the electrophysiological underpinnings of oscillatory entrainment

  • Notwithstanding, the poor focality provided by non-invasive stimulation technologies which can be estimated using computational models but not measured directly by monitoring changes in brain activity entrained during the delivery of stimulation[28,29] and the limited spatial resolution of non-invasive scalp recordings which do not always allow a precise localization of the entrained oscillatory activity as emerging from specific brain sites[30], limit their ability to explore in further detail the physiology of oscillatory entrainment in well-circumscribed brain sites

  • At the expense of losing the significant advantage of non-invasiveness for exploratory and clinical human applications, intracranial brain stimulation coupled to intracranial EEG recordings allows measuring the local effects of frequency-tuned direct electrical stimulation with a high degree of spatial certainty, which could be in a near future associated with the cytoarchitectural properties of the stimulated tissue and its precise connectivity patterns

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Summary

Introduction

Magnetoencephalography (MEG)[22] recordings have contributed to ignite an interest in causally exploring the electrophysiological underpinnings of oscillatory entrainment. At the expense of losing the significant advantage of non-invasiveness for exploratory and clinical human applications, intracranial brain stimulation coupled to intracranial EEG recordings (iEEG) allows measuring the local effects of frequency-tuned direct electrical stimulation with a high degree of spatial certainty, which could be in a near future associated with the cytoarchitectural properties of the stimulated tissue and its precise connectivity patterns To this regard, an existing clinical model that may facilitate an intracranial exploration of local neural entrainment in awake human systems is the one provided by pre-surgical mapping of medication-resistant implanted human epilepsy patients[31,32]. Aiming to supplement prior evidence on entrainment mainly provided with non-invasive methods, and obtain evidence in support of focal oscillatory entrainment in humans directly from well-circumscribed brain regions, we analyzed iEEG recordings from sets of multi-electrodes implanted in a group of three epilepsy patients who received focal intracranial stimulation patterns performed during an awake causal mapping procedure aiming to localize and characterize epileptogenic cerebral loci, prior to considering their surgical removal

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