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Research Articles, Neurobiology of Disease

Perturbed Information Processing Complexity in Experimental Epilepsy

Wesley Clawson, Benjamin Waked, Tanguy Madec, Antoine Ghestem, Pascale P. Quilichini, Demian Battaglia and Christophe Bernard
Journal of Neuroscience 20 September 2023, 43 (38) 6573-6587; DOI: https://doi.org/10.1523/JNEUROSCI.0383-23.2023
Wesley Clawson
1Aix Marseille Université, INSERM, INS, Institut de Neurosciences des Systèmes, Marseille, France
2Allen Discovery Center, Tufts University, Medford, Massachusetts
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Benjamin Waked
1Aix Marseille Université, INSERM, INS, Institut de Neurosciences des Systèmes, Marseille, France
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Tanguy Madec
1Aix Marseille Université, INSERM, INS, Institut de Neurosciences des Systèmes, Marseille, France
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Antoine Ghestem
1Aix Marseille Université, INSERM, INS, Institut de Neurosciences des Systèmes, Marseille, France
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Pascale P. Quilichini
1Aix Marseille Université, INSERM, INS, Institut de Neurosciences des Systèmes, Marseille, France
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Demian Battaglia
1Aix Marseille Université, INSERM, INS, Institut de Neurosciences des Systèmes, Marseille, France
3University of Strasbourg Institute for Advanced Studies, Strasbourg, France
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Christophe Bernard
1Aix Marseille Université, INSERM, INS, Institut de Neurosciences des Systèmes, Marseille, France
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Abstract

Comorbidities, such as cognitive deficits, which often accompany epilepsies, constitute a basal state, while seizures are rare and transient events. This suggests that neural dynamics, in particular those supporting cognitive function, are altered in a permanent manner in epilepsy. Here, we test the hypothesis that primitive processes of information processing at the core of cognitive function (i.e., storage and sharing of information) are altered in the hippocampus and the entorhinal cortex in experimental epilepsy in adult, male Wistar rats. We find that information storage and sharing are organized into substates across the stereotypic states of slow and theta oscillations in both epilepsy and control conditions. However, their internal composition and organization through time are disrupted in epilepsy, partially losing brain state selectivity compared with controls, and shifting toward a regimen of disorder. We propose that the alteration of information processing at this algorithmic level of computation, the theoretical intermediate level between structure and function, may be a mechanism behind the emergent and widespread comorbidities associated with epilepsy, and perhaps other disorders.

SIGNIFICANCE STATEMENT Comorbidities, such as cognitive deficits, which often accompany epilepsies, constitute a basal state, while seizures are rare and transient events. This suggests that neural dynamics, in particular those supporting cognitive function, are altered in a permanent manner in epilepsy. Here, we show that basic processes of information processing at the core of cognitive function (i.e., storage and sharing of information) are altered in the hippocampus and the entorhinal cortex (two regions involved in memory processes) in experimental epilepsy. Such disruption of information processing at the algorithmic level itself could underlie the general performance impairments in epilepsy.

  • algorithm
  • complexity
  • entorhinal cortex
  • epilepsy
  • hippocampus
  • information processing

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The Journal of Neuroscience: 43 (38)
Journal of Neuroscience
Vol. 43, Issue 38
20 Sep 2023
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Perturbed Information Processing Complexity in Experimental Epilepsy
Wesley Clawson, Benjamin Waked, Tanguy Madec, Antoine Ghestem, Pascale P. Quilichini, Demian Battaglia, Christophe Bernard
Journal of Neuroscience 20 September 2023, 43 (38) 6573-6587; DOI: 10.1523/JNEUROSCI.0383-23.2023

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Perturbed Information Processing Complexity in Experimental Epilepsy
Wesley Clawson, Benjamin Waked, Tanguy Madec, Antoine Ghestem, Pascale P. Quilichini, Demian Battaglia, Christophe Bernard
Journal of Neuroscience 20 September 2023, 43 (38) 6573-6587; DOI: 10.1523/JNEUROSCI.0383-23.2023
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Keywords

  • algorithm
  • complexity
  • entorhinal cortex
  • epilepsy
  • hippocampus
  • information processing

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