Disruption of layer-specific visual processing in a model of focal neocortical epilepsy

Author:

Panarese Alessandro12,Vissani Matteo12,Meneghetti Nicolò12ORCID,Vannini Eleonora3,Cracchiolo Marina12,Micera Silvestro124,Caleo Matteo35,Mazzoni Alberto12,Restani Laura3

Affiliation:

1. The Biorobotics Institute, Scuola Superiore Sant’Anna , viale Rinaldo Piaggio 34, 56025 Pontedera , Italy

2. Department of Excellence in Robotics and Artificial Intelligence, Scuola Superiore Sant’Anna , Piazza Martiri della Libertà, 56127 Pisa , Italy

3. Neuroscience Institute, National Research Council (CNR) , via G. Moruzzi 1, 56124 Pisa , Italy

4. Bertarelli Foundation Chair in Translational Neuroengineering, Centre for Neuroprosthetics and Institute of Bioengineering, School of Engineering, École Polytechnique Fédérale de Lausanne (EPFL), Campus Biotech , Chemin des Mines 9, 1202 Geneva , Switzerland

5. Department of Biomedical Sciences, University of Padua , via G. Colombo 3, 35121 Padua , Italy

Abstract

Abstract The epileptic brain is the result of a sequence of events transforming normal neuronal populations into hyperexcitable networks supporting recurrent seizure generation. These modifications are known to induce fundamental alterations of circuit function and, ultimately, of behavior. However, how hyperexcitability affects information processing in cortical sensory circuits is not yet fully understood. Here, we investigated interlaminar alterations in sensory processing of the visual cortex in a mouse model of focal epilepsy. We found three main circuit dynamics alterations in epileptic mice: (i) a spreading of visual contrast-driven gamma modulation across layers, (ii) an increase in firing rate that is layer-unspecific for excitatory units and localized in infragranular layers for inhibitory neurons, and (iii) a strong and contrast-dependent locking of firing units to network activity. Altogether, our data show that epileptic circuits display a functional disruption of layer-specific organization of visual sensory processing, which could account for visual dysfunction observed in epileptic subjects. Understanding these mechanisms paves the way to circuital therapeutic interventions for epilepsy.

Funder

Italian Ministry of Education, University and Research

Italian National Research Council

European Brain Research Institute

Publisher

Oxford University Press (OUP)

Subject

Cellular and Molecular Neuroscience,Cognitive Neuroscience

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