Mild metabolic stress is sufficient to disturb the formation of pyramidal cell ensembles during gamma oscillations

Author:

Elzoheiry Shehabeldin1,Lewen Andrea1,Schneider Justus1,Both Martin1,Hefter Dimitri12,Boffi Juan Carlos3,Hollnagel Jan-Oliver1ORCID,Kann Oliver14ORCID

Affiliation:

1. Institute of Physiology and Pathophysiology, University of Heidelberg, Heidelberg, Germany

2. RG Animal Models in Psychiatry, Clinic of Psychiatry and Psychotherapy, Central Institute of Mental Health, Mannheim, Germany

3. Institute for Anatomy and Cell Biology, University of Heidelberg, Heidelberg, Germany

4. Interdisciplinary Centre for Neurosciences (IZN), University of Heidelberg, Heidelberg, Germany

Abstract

Disturbances of cognitive functions occur rapidly during acute metabolic stress. However, the underlying mechanisms are not fully understood. Cortical gamma oscillations (30–100 Hz) emerging from precise synaptic transmission between excitatory principal neurons and inhibitory interneurons, such as fast-spiking GABAergic basket cells, are associated with higher brain functions, like sensory perception, selective attention and memory formation. We investigated the alterations of cholinergic gamma oscillations at the level of neuronal ensembles in the CA3 region of rat hippocampal slice cultures. We combined electrophysiology, calcium imaging (CamKII.GCaMP6f) and mild metabolic stress that was induced by rotenone, a lipophilic and highly selective inhibitor of complex I in the respiratory chain of mitochondria. The detected pyramidal cell ensembles showing repetitive patterns of activity were highly sensitive to mild metabolic stress. Whereas such synchronised multicellular activity diminished, the overall activity of individual pyramidal cells was unaffected. Additionally, mild metabolic stress had no effect on the rate of action potential generation in fast-spiking neural units. However, the partial disinhibition of slow-spiking neural units suggests that disturbances of ensemble formation likely result from alterations in synaptic inhibition. Our study bridges disturbances on the (multi-)cellular and network level to putative cognitive impairment on the system level.

Publisher

SAGE Publications

Subject

Cardiology and Cardiovascular Medicine,Clinical Neurology,Neurology

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