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Articles, Development/Plasticity/Repair

Long-Term Seizure Suppression and Optogenetic Analyses of Synaptic Connectivity in Epileptic Mice with Hippocampal Grafts of GABAergic Interneurons

Katharine W. Henderson, Jyoti Gupta, Stephanie Tagliatela, Elizabeth Litvina, XiaoTing Zheng, Meghan A. Van Zandt, Nicholas Woods, Ethan Grund, Diana Lin, Sara Royston, Yuchio Yanagawa, Gloster B. Aaron and Janice R. Naegele
Journal of Neuroscience 1 October 2014, 34 (40) 13492-13504; https://doi.org/10.1523/JNEUROSCI.0005-14.2014
Katharine W. Henderson
1Department of Biology, Program in Neuroscience and Behavior, Hall-Atwater Laboratory, Wesleyan University, Middletown, Connecticut 06459-0170,
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Jyoti Gupta
1Department of Biology, Program in Neuroscience and Behavior, Hall-Atwater Laboratory, Wesleyan University, Middletown, Connecticut 06459-0170,
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Stephanie Tagliatela
1Department of Biology, Program in Neuroscience and Behavior, Hall-Atwater Laboratory, Wesleyan University, Middletown, Connecticut 06459-0170,
2Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139-4307,
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Elizabeth Litvina
1Department of Biology, Program in Neuroscience and Behavior, Hall-Atwater Laboratory, Wesleyan University, Middletown, Connecticut 06459-0170,
3Department of Neurobiology, Harvard Medical School, Boston, Massachusetts 02115-5701,
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XiaoTing Zheng
1Department of Biology, Program in Neuroscience and Behavior, Hall-Atwater Laboratory, Wesleyan University, Middletown, Connecticut 06459-0170,
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Meghan A. Van Zandt
1Department of Biology, Program in Neuroscience and Behavior, Hall-Atwater Laboratory, Wesleyan University, Middletown, Connecticut 06459-0170,
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Nicholas Woods
1Department of Biology, Program in Neuroscience and Behavior, Hall-Atwater Laboratory, Wesleyan University, Middletown, Connecticut 06459-0170,
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Ethan Grund
1Department of Biology, Program in Neuroscience and Behavior, Hall-Atwater Laboratory, Wesleyan University, Middletown, Connecticut 06459-0170,
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Diana Lin
1Department of Biology, Program in Neuroscience and Behavior, Hall-Atwater Laboratory, Wesleyan University, Middletown, Connecticut 06459-0170,
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Sara Royston
1Department of Biology, Program in Neuroscience and Behavior, Hall-Atwater Laboratory, Wesleyan University, Middletown, Connecticut 06459-0170,
4Medical Scholars Program, Neuroscience Program, University of Illinois Urbana-Champaign, Urbana, Illinois 61801-6210, and
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Yuchio Yanagawa
5Department of Genetic and Behavioral Neuroscience, Gunma University Graduate School of Medicine, Japan and Japan Science and Technology Agency, CREST, Tokyo 102-0075, Japan
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Gloster B. Aaron
1Department of Biology, Program in Neuroscience and Behavior, Hall-Atwater Laboratory, Wesleyan University, Middletown, Connecticut 06459-0170,
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Janice R. Naegele
1Department of Biology, Program in Neuroscience and Behavior, Hall-Atwater Laboratory, Wesleyan University, Middletown, Connecticut 06459-0170,
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This article has a correction. Please see:

  • Correction: Henderson et al., Long-term Seizure Suppression and Optogenetic Analyses of Synaptic Connectivity in Epileptic Mice with Hippocampal Grafts of GABAergic Interneurons - May 11, 2016

Abstract

Studies in rodent epilepsy models suggest that GABAergic interneuron progenitor grafts can reduce hyperexcitability and seizures in temporal lobe epilepsy (TLE). Although integration of the transplanted cells has been proposed as the underlying mechanism for these disease-modifying effects, prior studies have not explicitly examined cell types and synaptic mechanisms for long-term seizure suppression. To address this gap, we transplanted medial ganglionic eminence (MGE) cells from embryonic day 13.5 VGAT-Venus or VGAT-ChR2-EYFP transgenic embryos into the dentate gyrus (DG) of adult mice 2 weeks after induction of TLE with pilocarpine. Beginning 3–4 weeks after status epilepticus, we conducted continuous video-electroencephalographic recording until 90–100 d. TLE mice with bilateral MGE cell grafts in the DG had significantly fewer and milder electrographic seizures, compared with TLE controls. Immunohistochemical studies showed that the transplants contained multiple neuropeptide or calcium-binding protein-expressing interneuron types and these cells established dense terminal arborizations onto the somas, apical dendrites, and axon initial segments of dentate granule cells (GCs). A majority of the synaptic terminals formed by the transplanted cells were apposed to large postsynaptic clusters of gephyrin, indicative of mature inhibitory synaptic complexes. Functionality of these new inhibitory synapses was demonstrated by optogenetically activating VGAT-ChR2-EYFP-expressing transplanted neurons, which generated robust hyperpolarizations in GCs. These findings suggest that fetal GABAergic interneuron grafts may suppress pharmacoresistant seizures by enhancing synaptic inhibition in DG neural circuits.

  • EEG
  • epilepsy
  • GABA
  • seizures
  • transplantation
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The Journal of Neuroscience: 34 (40)
Journal of Neuroscience
Vol. 34, Issue 40
1 Oct 2014
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Long-Term Seizure Suppression and Optogenetic Analyses of Synaptic Connectivity in Epileptic Mice with Hippocampal Grafts of GABAergic Interneurons
Katharine W. Henderson, Jyoti Gupta, Stephanie Tagliatela, Elizabeth Litvina, XiaoTing Zheng, Meghan A. Van Zandt, Nicholas Woods, Ethan Grund, Diana Lin, Sara Royston, Yuchio Yanagawa, Gloster B. Aaron, Janice R. Naegele
Journal of Neuroscience 1 October 2014, 34 (40) 13492-13504; DOI: 10.1523/JNEUROSCI.0005-14.2014

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Long-Term Seizure Suppression and Optogenetic Analyses of Synaptic Connectivity in Epileptic Mice with Hippocampal Grafts of GABAergic Interneurons
Katharine W. Henderson, Jyoti Gupta, Stephanie Tagliatela, Elizabeth Litvina, XiaoTing Zheng, Meghan A. Van Zandt, Nicholas Woods, Ethan Grund, Diana Lin, Sara Royston, Yuchio Yanagawa, Gloster B. Aaron, Janice R. Naegele
Journal of Neuroscience 1 October 2014, 34 (40) 13492-13504; DOI: 10.1523/JNEUROSCI.0005-14.2014
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Keywords

  • EEG
  • epilepsy
  • GABA
  • seizures
  • transplantation

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