Focal seizures induce spatiotemporally organized spiking activity in the human cortex

• Published in: Nature communications Vol. 15; no. 1; pp. 7075 - 15
• Main Authors: Diamond, Joshua M., Chapeton, Julio I., Xie, Weizhen, Jackson, Samantha N., Inati, Sara K., Zaghloul, Kareem A.
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 16.08.2024; Nature Publishing Group; Nature Portfolio
• Subjects: 631/378/1689/178; 692/617/375/178; 692/699/375/178; Action Potentials - physiology; Adult; Bursts; Cerebral cortex; Cerebral Cortex - physiology; Coding; Convulsions & seizures; Discharge; Electroencephalography; Epilepsy; Firing pattern; Humanities and Social Sciences; Humans; Information processing; Male; Middle Aged; multidisciplinary; Neural coding; Neurons; Neurons - physiology; Science; Science (multidisciplinary); Seizures; Seizures - physiopathology; Sequences; Spiking; Temporal lobe; Temporal variations; Traveling waves; Unit activity; Young Adult
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-024-51338-1

Epileptic seizures are debilitating because of the clinical symptoms they produce. These symptoms, in turn, may stem directly from disruptions in neural coding. Recent evidence has suggested that the specific temporal order, or sequence, of spiking across a population of cortical neurons may encode information. Here, we investigate how seizures disrupt neuronal spiking sequences in the human brain by recording multi-unit activity from the cerebral cortex in five male participants undergoing monitoring for seizures. We find that pathological discharges during seizures are associated with bursts of spiking activity across a population of cortical neurons. These bursts are organized into highly consistent and stereotyped temporal sequences. As the seizure evolves, spiking sequences diverge from the sequences observed at baseline and become more spatially organized. The direction of this spatial organization matches the direction of the ictal discharges, which spread over the cortex as traveling waves. Our data therefore suggest that seizures can entrain cortical spiking sequences by changing the spatial organization of neuronal firing, providing a possible mechanism by which seizures create symptoms. The precise mechanism by which seizures disrupt neural coding remains unclear. Here, the authors show that discharges arising from the seizure source travel macroscopic distances, where they go on to influence spiking sequences at the microscopic scale.