Activity-dependence of spreading depression in the locust CNS

Spong, Kristin E.; Mazzetti, Tom; Robertson, R. Meldrum

doi:10.1242/jeb.132456

Cited by 11 publications

(8 citation statements)

References 14 publications

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“…reduce the leakage of K + from the intracellular space), (3) reduced neural activity (i.e. reduced accumulation of K + caused by neurons firing; see Spong et al, 2016a), and (4) increased Na + /K + -ATPase activity (i.e. increasing the rate of K + clearance; see Armstrong et al, 2011).…”

Section: Mechanisms Of Variation In Cns Shutdownmentioning

confidence: 99%

Central nervous shutdown underlies acute cold tolerance in tropical and temperateDrosophilaspecies

Andersen

Jensen

Robertson

et al. 2018

Journal of Experimental Biology

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When cooled, insects first lose their ability to perform coordinated movements (CT) after which they enter chill coma (chill coma onset, CCO). Both these behaviours are popular measures of cold tolerance that correlate remarkably well with species distribution. To identify and understand the neuromuscular impairment that causes CT and CCO we used inter- and intraspecific model systems of species that have varying cold tolerance as a consequence of adaptation or cold acclimation. Our results demonstrate that CT and CCO correlate strongly with a spreading depolarization (SD) within the central nervous system (CNS). We show that this SD is associated with a rapid increase in extracellular [K] within the CNS causing neuronal depolarization that silences the CNS. The CNS shutdown is likely to be caused by a mismatch between passive and active ion transport within the CNS and in a different set of experiments we examine inter- and intraspecific differences in sensitivity to SD events during anoxic exposure. These experiments show that cold adapted or acclimated flies are better able to maintain ionoregulatory balance when active transport is compromised within the CNS. Combined, we demonstrate that a key mechanism underlying chill coma entry of is CNS shutdown, and the ability to prevent this CNS shutdown is therefore an important component of acute cold tolerance, thermal adaptation and cold acclimation in insects.

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Section: Mechanisms Of Variation In Cns Shutdownmentioning

confidence: 99%

Central nervous shutdown underlies acute cold tolerance in tropical and temperateDrosophilaspecies

Andersen

Jensen

Robertson

et al. 2018

Journal of Experimental Biology

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“…SD is characterized by a collapse of CNS ion homeostasis resulting in major changes in CNS ion concentrations, neuronal and glial depolarization and a negative DC shift in the extracellular field potential (FP) 23 . It appears to be triggered when extracellular potassium ion concentration ([K + ] o ) surpasses a critical threshold and is thus dependent on activity levels in the CNS 24 – 26 .…”

Section: Introductionmentioning

confidence: 99%

Chill coma in the locust, Locusta migratoria, is initiated by spreading depolarization in the central nervous system

Robertson

Spong

Srithiphaphirom

2017

Sci Rep

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The ability of chill-sensitive insects to function at low temperatures limits their geographic ranges. They have species-specific temperatures below which movements become uncoordinated prior to entering a reversible state of neuromuscular paralysis. In spite of decades of research, which in recent years has focused on muscle function, the role of neural mechanisms in determining chill coma is unknown. Spreading depolarization (SD) is a phenomenon that causes a shutdown of neural function in the integrating centres of the central nervous system. We investigated the role of SD in the process of entering chill coma in the locust, Locusta migratoria. We used thermolimit respirometry and electromyography in whole animals and extracellular and intracellular recording techniques in semi-intact preparations to characterize neural events during chilling. We show that chill-induced SD in the central nervous system is the mechanism underlying the critical thermal minimum for coordinated movement in locusts. This finding will be important for understanding how insects adapt and acclimate to changing environmental temperatures.

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“…Oxidative stress [ 11 ], ATP depletion [ 12 ], spreading depression [ 6 ], anoxia [ 10 ] and hyperthermia [ 8 , 9 ] all exhibit the same [K + ] e surge upon neuronal failure. In many cases, a gradual rise in [K + ] e occurs during stress application until the ultimate loss of K + homeostasis [ 4 , 7 , 37 , 38 ]. Similarly, there is a gradual rise in [Ca 2+ ] i during hyperthermia [ 39 , 40 ], hypoxia [ 41 ], and oxidative stress [ 42 ].…”

Section: Discussionmentioning

confidence: 99%

cGMP-Dependent Protein Kinase Inhibition Extends the Upper Temperature Limit of Stimulus-Evoked Calcium Responses in Motoneuronal Boutons of Drosophila melanogaster Larvae

Krill

2016

PLoS ONE

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While the mammalian brain functions within a very narrow range of oxygen concentrations and temperatures, the fruit fly, Drosophila melanogaster, has employed strategies to deal with a much wider range of acute environmental stressors. The foraging (for) gene encodes the cGMP-dependent protein kinase (PKG), has been shown to regulate thermotolerance in many stress-adapted species, including Drosophila, and could be a potential therapeutic target in the treatment of hyperthermia in mammals. Whereas previous thermotolerance studies have looked at the effects of PKG variation on Drosophila behavior or excitatory postsynaptic potentials at the neuromuscular junction (NMJ), little is known about PKG effects on presynaptic mechanisms. In this study, we characterize presynaptic calcium ([Ca2+]i) dynamics at the Drosophila larval NMJ to determine the effects of high temperature stress on synaptic transmission. We investigated the neuroprotective role of PKG modulation both genetically using RNA interference (RNAi), and pharmacologically, to determine if and how PKG affects presynaptic [Ca2+]i dynamics during hyperthermia. We found that PKG activity modulates presynaptic neuronal Ca2+ responses during acute hyperthermia, where PKG activation makes neurons more sensitive to temperature-induced failure of Ca2+ flux and PKG inhibition confers thermotolerance and maintains normal Ca2+ dynamics under the same conditions. Targeted motoneuronal knockdown of PKG using RNAi demonstrated that decreased PKG expression was sufficient to confer thermoprotection. These results demonstrate that the PKG pathway regulates presynaptic motoneuronal Ca2+ signaling to influence thermotolerance of presynaptic function during acute hyperthermia.

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Activity-dependence of spreading depression in the locust CNS

Cited by 11 publications

References 14 publications

Central nervous shutdown underlies acute cold tolerance in tropical and temperateDrosophilaspecies

Central nervous shutdown underlies acute cold tolerance in tropical and temperateDrosophilaspecies

Chill coma in the locust, Locusta migratoria, is initiated by spreading depolarization in the central nervous system

cGMP-Dependent Protein Kinase Inhibition Extends the Upper Temperature Limit of Stimulus-Evoked Calcium Responses in Motoneuronal Boutons of Drosophila melanogaster Larvae

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