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      Suppression of Spreading Depression-Like Events in Locusts by Inhibition of the NO/cGMP/PKG Pathway

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          Abstract

          Despite considerable research attention focused on mechanisms underlying neural spreading depression (SD), because of its association with important human CNS pathologies, such as stroke and migraine, little attention has been given to explaining its occurrence and regulation in invertebrates. In the locust metathoracic ganglion (MTG), an SD-like event occurs during heat and anoxia stress, which results in cessation of neuronal output for the duration of the applied stress. SD-like events were characterized by an abrupt rise in extracellular potassium ion concentration ([K +] o) from a baseline concentration of ∼8 to >30 m m, which returned to near baseline concentrations after removal of the applied stress. After return to baseline [K +] o, neuronal output (ventilatory motor pattern activity) from the MTG recovered. Unlike mammalian neurons, which depolarize almost completely during SD, locust neurons only partially depolarized. SD-like events in the locust CNS were suppressed by pharmacological inhibition of the nitric oxide/cyclic guanosine monophosphate/protein kinase G (NO/cGMP/PKG) pathway and were exacerbated by its activation. Also, environmental stressors such as heat and anoxia increased production of nitric oxide in the locust CNS. Finally, for the intact animal, manipulation of the pathway affected the speed of recovery from suffocation by immersion under water. We propose that SD-like events in locusts provide an adaptive mechanism for surviving extreme environmental conditions. The highly conserved nature of the NO/cGMP/PKG signaling pathway suggests that it may be involved in modulating SD in other organisms, including mammals.

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          Author and article information

          Journal
          J Neurosci
          J. Neurosci
          jneuro
          jneurosci
          J. Neurosci
          The Journal of Neuroscience
          Society for Neuroscience
          0270-6474
          1529-2401
          24 June 2009
          : 29
          : 25
          : 8225-8235
          Affiliations
          [1]Department of Biology, Queen's University, Kingston, Ontario K7L 3N6, Canada
          Author notes
          Correspondence should be addressed to R. Meldrum Robertson, Department of Biology, Queen's University, Biosciences Complex, Kingston, ON K7L 3N6, Canada. robertrm@ 123456queensu.ca
          Article
          PMC6666049 PMC6666049 6666049 3500946
          10.1523/JNEUROSCI.1652-09.2009
          6666049
          19553462
          95d2ef9b-1b0a-422a-a256-0bf4cc2fd33e
          Copyright © 2009 Society for Neuroscience 0270-6474/09/298225-11$15.00/0
          History
          : 6 April 2009
          : 20 May 2009
          : 22 May 2009
          Categories
          Articles
          Behavioral/Systems/Cognitive

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