Coma in response to environmental stress in the locust: A model for cortical spreading depression

Rodgers, Corinne I.; Armstrong, Gary A. B.; Robertson, R. Meldrum

doi:10.1016/j.jinsphys.2010.03.030

Cited by 96 publications

(127 citation statements)

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“…We found that inhibition of AMPK using compound-C suppressed SD in 70% of preparations. (Rodgers et al, 2010) that ouabaininduced repetitive SD in the locust resembles peri-infarct depolarizations that prevent the restoration of energy and increase the size of the cortical infarct (Fabricius et al, 2006;Dohmen et al, 2008;Dreier et al, 2009). Given the similarity between locust and mammalian SD phenomena, the modulatory effects of AMPK in our study are highly relevant for understanding the pathology of stroke and seizures.…”

Section: Discussionmentioning

confidence: 77%

“…Moreover, AMPK activation did not induce a coma or SD, but the AMPK signal rendered the system more susceptible to SD, which is important because of the involvement of SD in the etiology of human disorders such as migraine and stroke. SDlike events in the locust ventilatory neuropile share most of the major characteristics of SD in mammalian cortical tissue, including loss of ion homeostasis and electrical activity that spreads across tissue (see Rodgers et al, 2010, for a more thorough comparison). These results are discussed in more detail below.…”

Section: Discussionmentioning

confidence: 99%

“…These are characterized by abrupt 50 -80 mM increases in extracellular potassium concentration ([K ϩ ] o ) within the ventilatory neuropile that coincide with vCPG shutdown. Our hypothesis is that stress-induced comas and associated SD-like events in the locust represent a protective strategy to cope with environmental stress by preventing neuronal hyperexcitation and energy collapse (Rodgers et al, 2010). Conceivably, energy levels would be maintained by entering a state of coma during which energyusing mechanisms that restore ion gradients are suspended (Rodgers et al, 2007;Staples and Buck, 2009).…”

Section: Introductionmentioning

confidence: 99%

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Metabolic Stress Modulates Motor Patterning via AMP-Activated Protein Kinase

Rodgers-Garlick

Armstrong²,

Robertson³

2011

J. Neurosci.

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Neural circuits are especially vulnerable to metabolic stress. The locust (Locusta migratoria) responds to anoxia by entering a coma during which neural and muscular systems shut down. During anoxic coma, arrest of the ventilatory central pattern generator is tightly correlated with an abrupt spreading depression (SD)-like increase in extracellular potassium concentration within the metathoracic neuropile. We examined the role of the AMP-activated protein kinase (AMPK), an evolutionarily conserved sensor of cellular energy status, in anoxia-induced ventilatory arrest and SD-like events in the locust. Perfusion of sodium azide (NaN 3 ; mitochondrial toxin) induced SD, temporary coma, and profound changes in the ventilatory motor pattern characterized as a rapid rhythm before coma and a slower rhythm following recovery. AMPK activation using 5-aminoimidazole-4-carboxamide ribonucleoside (AICAR) mimicked the motor pattern changes induced by NaN 3 but did not induce SD and coma. The effects of NaN 3 on the ventilatory rhythm were reversed by perfusion of compound-C (AMPK inhibitor) or glucose, and the effects of AICAR were also reversed by compound-C, confirming the modulatory roles of AMPK and energy status. Ouabain-induced recurring SD was suppressed by inhibition of AMPK and exacerbated by its activation. We show that the motor pattern changes induced by metabolic stress are not the result of SD alone, but that AMPK is necessary and sufficient for these changes and that AMPK activity strongly influences susceptibility to SD.

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Section: Discussionmentioning

confidence: 77%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Metabolic Stress Modulates Motor Patterning via AMP-Activated Protein Kinase

Rodgers-Garlick

Armstrong²,

Robertson³

2011

J. Neurosci.

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“…Unlike muscle, insect nervous tissue is protected from transient alterations in hemolymph composition by the blood-brain and blood-nerve barriers (30), which suggests that this hemolymph-composition-driven loss of excitability may primarily affect the muscle. However, declining temperatures do increase extracellular [K + ] of locust neurons in vitro, which would lead to temperature-sensitive electrical silence of the nervous system as well (31).…”

Section: Resultsmentioning

confidence: 99%

Reestablishment of ion homeostasis during chill-coma recovery in the cricketGryllus pennsylvanicus

MacMillan

Williams

Staples

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

155

158

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The time required to recover from cold-induced paralysis (chill-coma) is a common measure of insect cold tolerance used to test central questions in thermal biology and predict the effects of climate change on insect populations. The onset of chill-coma in the fall field cricket (Gryllus pennsylvanicus, Orthoptera: Gryllidae) is accompanied by a progressive drift of Na + and water from the hemolymph to the gut, but the physiological mechanisms underlying recovery from chill-coma are not understood for any insect. Using a combination of gravimetric methods and atomic absorption spectroscopy, we demonstrate that recovery from chill-coma involves a reestablishment of hemolymph ion content and volume driven by removal of Na + and water from the gut. Recovery is associated with a transient elevation of metabolic rate, the time span of which increases with increasing cold exposure duration and closely matches the duration of complete osmotic recovery. Thus, complete recovery from chill-coma is metabolically costly and encompasses a longer period than is required for the recovery of muscle potentials and movement. These findings provide evidence that physiological mechanisms of hemolymph ion content and volume regulation, such as ion-motive ATPase activity, are instrumental in chill-coma recovery and may underlie natural variation in insect cold tolerance.ionoregulation | metabolism | osmotic homeostasis | thermal limits | stress resistance

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“…5 In the present paper, Spong et al 4 show that the hallmarks characteristic of SD can be recorded in the fly brain after treatment with ouabain to reduce activity of the Na C /K C -ATPase. In addition, using genetic strains of flies that differ in levels of PKG activity, the authors demonstrate that reduction of activity of cyclic GMP-dependent protein kinase (PKG) attenuates SD and suggest that the PKG pathway might have a similar modulatory role for SD in mammals, an idea that has not yet been tested.…”

mentioning

confidence: 51%