Oxygen and seizure dynamics: I. experiments

Justin Ingram, Chunfeng Zhang, John R. Cressman, Anupam Hazra, Yina Wei, Yong Eun Koo, Jokubas Žiburkus, Raoul Kopelman, Jian Xu, Steven J. Schiff

Research output: Contribution to journalArticle

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Abstract

We utilized a novel ratiometric nanoquantum dot fluorescence resonance energy transfer (NQD-FRET) optical sensor to quantitatively measure oxygen dynamics from single cell microdomains during hypoxic episodes as well as during 4-aminopyridine (4-AP)-induced spontaneous seizure- like events in rat hippocampal slices. Coupling oxygen sensing with electrical recordings, we found the greatest reduction in the O2 concentration ([O2]) in the densely packed cell body stratum (st.) pyramidale layer of the CA1 and differential layer-specific O2 dynamics between the st. pyramidale and st. oriens layers. These hypoxic decrements occurred up to several seconds before seizure onset could be electrically measured extracellularly. Without 4-AP, we quantified a narrow range of [O2], similar to the endogenous hypoxia found before epileptiform activity, which permits a quiescent network to enter into a seizure-like state. We demonstrated layerspecific patterns of O2 utilization accompanying layer-specific neuronal interplay in seizure. None of the oxygen overshoot artifacts seen with polarographic measurement techniques were observed. We therefore conclude that endogenously generated hypoxia may be more than just a consequence of increased cellular excitability but an influential and critical factor for orchestrating network dynamics associated with epileptiform activity.

Original languageEnglish (US)
Pages (from-to)205-212
Number of pages8
JournalJournal of neurophysiology
Volume112
Issue number2
DOIs
StatePublished - Jul 15 2014

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Seizures
Oxygen
4-Aminopyridine
Hippocampal CA1 Region
Fluorescence Resonance Energy Transfer
Artifacts
Hypoxia

All Science Journal Classification (ASJC) codes

  • Neuroscience(all)
  • Physiology

Cite this

Ingram, J., Zhang, C., Cressman, J. R., Hazra, A., Wei, Y., Koo, Y. E., ... Schiff, S. J. (2014). Oxygen and seizure dynamics: I. experiments. Journal of neurophysiology, 112(2), 205-212. https://doi.org/10.1152/jn.00540.2013
Ingram, Justin ; Zhang, Chunfeng ; Cressman, John R. ; Hazra, Anupam ; Wei, Yina ; Koo, Yong Eun ; Žiburkus, Jokubas ; Kopelman, Raoul ; Xu, Jian ; Schiff, Steven J. / Oxygen and seizure dynamics : I. experiments. In: Journal of neurophysiology. 2014 ; Vol. 112, No. 2. pp. 205-212.
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Ingram, J, Zhang, C, Cressman, JR, Hazra, A, Wei, Y, Koo, YE, Žiburkus, J, Kopelman, R, Xu, J & Schiff, SJ 2014, 'Oxygen and seizure dynamics: I. experiments', Journal of neurophysiology, vol. 112, no. 2, pp. 205-212. https://doi.org/10.1152/jn.00540.2013

Oxygen and seizure dynamics : I. experiments. / Ingram, Justin; Zhang, Chunfeng; Cressman, John R.; Hazra, Anupam; Wei, Yina; Koo, Yong Eun; Žiburkus, Jokubas; Kopelman, Raoul; Xu, Jian; Schiff, Steven J.

In: Journal of neurophysiology, Vol. 112, No. 2, 15.07.2014, p. 205-212.

Research output: Contribution to journalArticle

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AU - Kopelman, Raoul

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AU - Schiff, Steven J.

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Ingram J, Zhang C, Cressman JR, Hazra A, Wei Y, Koo YE et al. Oxygen and seizure dynamics: I. experiments. Journal of neurophysiology. 2014 Jul 15;112(2):205-212. https://doi.org/10.1152/jn.00540.2013