Optogenetic induction of cortical spreading depression in anesthetized and freely behaving mice

Cortical spreading depression, which plays an important role in multiple neurological disorders, has been studied primarily with experimental models that use highly invasive methods. We developed a relatively non-invasive optogenetic model to induce cortical spreading depression by transcranial stim...

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Veröffentlicht in:	Journal of cerebral blood flow and metabolism Jg. 37; H. 5; S. 1641 - 1655
Hauptverfasser:	Houben, Thijs, Loonen, Inge Cm, Baca, Serapio M, Schenke, Maarten, Meijer, Johanna H, Ferrari, Michel D, Terwindt, Gisela M, Voskuyl, Rob A, Charles, Andrew, van den Maagdenberg, Arn Mjm, Tolner, Else A
Format:	Journal Article
Sprache:	Englisch
Veröffentlicht:	United States 01.05.2017
Schlagworte:	Action Potentials - physiology Anesthesia Animals Bacterial Proteins - genetics Behavior, Animal - physiology Cerebrovascular Circulation - physiology Channelrhodopsins Cortical Spreading Depression - physiology Female Laser-Doppler Flowmetry Luminescent Proteins - genetics Male Mice, Transgenic Optogenetics Photic Stimulation Recombinant Fusion Proteins - genetics vascular dynamics non-invasive Behavior electrophysiology optogenetics
ISSN:	1559-7016
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Abstract	Cortical spreading depression, which plays an important role in multiple neurological disorders, has been studied primarily with experimental models that use highly invasive methods. We developed a relatively non-invasive optogenetic model to induce cortical spreading depression by transcranial stimulation of channelrhodopsin-2 ion channels expressed in cortical layer 5 neurons. Light-evoked cortical spreading depression in anesthetized and freely behaving mice was studied with intracortical DC-potentials, multi-unit activity and/or non-invasive laser Doppler flowmetry, and optical intrinsic signal imaging. In anesthetized mice, cortical spreading depression induction thresholds and propagation rates were similar for invasive (DC-potential) and non-invasive (laser Doppler flowmetry) recording paradigms. Cortical spreading depression-related vascular and parenchymal optical intrinsic signal changes were similar to those evoked with KCl. In freely behaving mice, DC-potential and multi-unit activity recordings combined with laser Doppler flowmetry revealed cortical spreading depression characteristics comparable to those under anesthesia, except for a shorter cortical spreading depression duration. Cortical spreading depression resulted in a short increase followed by prolonged reduction of spontaneous active behavior. Motor function, as assessed by wire grip tests, was transiently and unilaterally suppressed following a cortical spreading depression. Optogenetic cortical spreading depression induction has significant advantages over current models in that multiple cortical spreading depression events can be elicited in a non-invasive and cell type-selective fashion.
AbstractList	Cortical spreading depression, which plays an important role in multiple neurological disorders, has been studied primarily with experimental models that use highly invasive methods. We developed a relatively non-invasive optogenetic model to induce cortical spreading depression by transcranial stimulation of channelrhodopsin-2 ion channels expressed in cortical layer 5 neurons. Light-evoked cortical spreading depression in anesthetized and freely behaving mice was studied with intracortical DC-potentials, multi-unit activity and/or non-invasive laser Doppler flowmetry, and optical intrinsic signal imaging. In anesthetized mice, cortical spreading depression induction thresholds and propagation rates were similar for invasive (DC-potential) and non-invasive (laser Doppler flowmetry) recording paradigms. Cortical spreading depression-related vascular and parenchymal optical intrinsic signal changes were similar to those evoked with KCl. In freely behaving mice, DC-potential and multi-unit activity recordings combined with laser Doppler flowmetry revealed cortical spreading depression characteristics comparable to those under anesthesia, except for a shorter cortical spreading depression duration. Cortical spreading depression resulted in a short increase followed by prolonged reduction of spontaneous active behavior. Motor function, as assessed by wire grip tests, was transiently and unilaterally suppressed following a cortical spreading depression. Optogenetic cortical spreading depression induction has significant advantages over current models in that multiple cortical spreading depression events can be elicited in a non-invasive and cell type-selective fashion.
Author	Baca, Serapio M Loonen, Inge Cm van den Maagdenberg, Arn Mjm Tolner, Else A Schenke, Maarten Voskuyl, Rob A Terwindt, Gisela M Charles, Andrew Ferrari, Michel D Meijer, Johanna H Houben, Thijs
Author_xml	– sequence: 1 givenname: Thijs surname: Houben fullname: Houben, Thijs organization: 1 Department of Neurology, Leiden University Medical Center, Leiden, The Netherlands – sequence: 2 givenname: Inge Cm surname: Loonen fullname: Loonen, Inge Cm organization: 2 Department of Human Genetics, Leiden University Medical Center, Leiden, The Netherlands – sequence: 3 givenname: Serapio M surname: Baca fullname: Baca, Serapio M organization: 3 Department of Neurology, David Geffen School of Medicine at UCLA, Los Angeles, USA – sequence: 4 givenname: Maarten surname: Schenke fullname: Schenke, Maarten organization: 2 Department of Human Genetics, Leiden University Medical Center, Leiden, The Netherlands – sequence: 5 givenname: Johanna H surname: Meijer fullname: Meijer, Johanna H organization: 4 Laboratory for Neurophysiology, Department of Molecular Cell Biology, Leiden University Medical Center, Leiden, The Netherlands – sequence: 6 givenname: Michel D surname: Ferrari fullname: Ferrari, Michel D organization: 1 Department of Neurology, Leiden University Medical Center, Leiden, The Netherlands – sequence: 7 givenname: Gisela M surname: Terwindt fullname: Terwindt, Gisela M organization: 1 Department of Neurology, Leiden University Medical Center, Leiden, The Netherlands – sequence: 8 givenname: Rob A surname: Voskuyl fullname: Voskuyl, Rob A organization: 2 Department of Human Genetics, Leiden University Medical Center, Leiden, The Netherlands – sequence: 9 givenname: Andrew surname: Charles fullname: Charles, Andrew organization: 3 Department of Neurology, David Geffen School of Medicine at UCLA, Los Angeles, USA – sequence: 10 givenname: Arn Mjm surname: van den Maagdenberg fullname: van den Maagdenberg, Arn Mjm organization: 2 Department of Human Genetics, Leiden University Medical Center, Leiden, The Netherlands – sequence: 11 givenname: Else A surname: Tolner fullname: Tolner, Else A organization: 2 Department of Human Genetics, Leiden University Medical Center, Leiden, The Netherlands
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SubjectTerms	Action Potentials - physiology Anesthesia Animals Bacterial Proteins - genetics Behavior, Animal - physiology Cerebrovascular Circulation - physiology Channelrhodopsins Cortical Spreading Depression - physiology Female Laser-Doppler Flowmetry Luminescent Proteins - genetics Male Mice, Transgenic Optogenetics Photic Stimulation Recombinant Fusion Proteins - genetics
Title	Optogenetic induction of cortical spreading depression in anesthetized and freely behaving mice
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