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PMID: 12223559 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Distally directed dendrotoxicity induced by kainic Acid in hippocampal interneurons of green fluorescent protein-expressing transgenic mice.

Oliva AA, Lam TT, Swann JW

Abstract

Excitotoxicity, resulting from the excessive release of glutamate, is thought to contribute to a variety of neurological disorders, including epilepsy. Excitotoxic damage to dendrites, i.e., dendrotoxicity, is often characterized by the formation of large dendritic swellings, or "beads." Here, we show that hippocampal interneurons that express the neuropeptide somatostatin are highly vulnerable to the excitotoxic effects of the ionotropic glutamate receptor agonist kainate. Brief, focal iontophoretic application of kainate rapidly induced bead formation in dendrites of somatostatinergic interneurons that express green fluorescent protein (GFP) from mice of the transgenic line GIN (GFP-expressing inhibitory neurons). Surprisingly, beads often did not form at the site of kainate application or even in the dendritic segment to which kainate was applied; instead, dendritic beading occurred more distally, often encompassing all branches distal to the application site. We have termed this phenomena, "distally directed dendrotoxicity." Distally directed beading was induced regardless of the branch order of the site of application and was found to be dependent on activation of voltage-gated sodium channels. Subsequent to induction, distally directed beading would reverse in most cells; in other cells, however, beading irreversibly invaded proximal dendritic segments and gradually encompassed the entire dendritic tree. These results demonstrate that distal dendritic segments are highly vulnerable to excitotoxic injury and imply that excessive excitatory activity originating in one synaptic pathway can impact synapses at more distal dendritic segments of the same neuron. The discovery of this phenomenon will likely be important in understanding interneuronal dysfunction following excitotoxic injury.

MeSH Terms
Animals Biolistics Calcium Channel Blockers/pharmacology Dendrites/drug effects,pathology,ultrastructure Dose-Response Relationship, Drug Excitatory Amino Acid Agonists/toxicity Excitatory Amino Acid Antagonists/pharmacology Green Fluorescent Proteins Hippocampus/drug effects,metabolism,pathology In Vitro Techniques Interneurons/drug effects,metabolism,pathology Iontophoresis Kainic Acid/toxicity Lidocaine/pharmacology Luminescent Proteins/biosynthesis,genetics Mice Mice, Transgenic Neural Inhibition Pyramidal Cells/drug effects,pathology Receptors, AMPA/drug effects,metabolism Sodium Channel Blockers/pharmacology Sodium Channels/metabolism Somatostatin/biosynthesis Tetrodotoxin/pharmacology Transfection
Chemicals
Calcium Channel Blockers Excitatory Amino Acid Agonists Excitatory Amino Acid Antagonists Luminescent Proteins Receptors, AMPA Sodium Channel Blockers Sodium Channels Green Fluorescent Proteins Tetrodotoxin Somatostatin Lidocaine Kainic Acid
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Oliva Anthony A
The Cain Foundation Laboratories, Division of Neuroscience, and Department of Pediatrics, Baylor College of Medicine, Houston, Texas 77030, USA.
Lam Trang T
Swann John W
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Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
2002-09-15
Pages
8052-62
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6758103
Subset
IM
Grants
NINDS NIH HHS · R01 NS018309 · United States
NINDS NIH HHS · NS18309 · United States
NINDS NIH HHS · NS34504 · United States
NICHD NIH HHS · HD24064 · United States
NINDS NIH HHS · R01 NS037171 · United States
NINDS NIH HHS · NS37171 · United States
NICHD NIH HHS · P30 HD024064 · United States
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