Loss of Potassium Homeostasis Underlies Hyperthermic Conduction Failure in Control and Preconditioned Locusts

Abstract

At extreme temperature, neurons cease to function appropriately. Prior exposure to a heat stress (heat shock [HS]) can extend the temperature range for action potential conduction in the axon, but how this occurs is not well understood. Here we use electrophysiological recordings from the axon of a locust visual interneuron, the descending contralateral movement detector (DCMD), to examine what physiological changes result in conduction failure and what modifications allow for the observed plasticity following HS. We show that at high temperature, conduction failure in the DCMD occurred preferentially where the axon passes through the thoracic ganglia rather than in the connective. Although the membrane potential hyperpolarized with increasing temperature, we observed a modest depolarization (3-6 mV) in the period preceding the failure. Prior to the conduction block, action potential amplitude decreased and half-width increased. Both of these failure-associated effects were attenuated following HS. Extracellular potassium concentration ([K+]o) increased sharply at failure and the failure event could be mimicked by the application of high [K+]o. Surges in [K+]o were muted following HS, suggesting that HS may act to stabilize ion distribution. Indeed, experimentally increased [K+]o lowered failure temperature significantly more in control animals than in HS animals and experimentally maintained [K+]o was found to be protective. We suggest that the more attenuated effects of failure on the membrane properties of the DCMD axon in HS animals is consistent with a decrease in the disruptive nature of the [K+]o-dependent failure event following HS and thus represents an adaptive mechanism to cope with thermal stress.

Alleviating Brain Stress: What Alternative Animal Models Have Revealed About Therapeutic Targets For Hypoxia and Anoxia

“…This raises the question of why these insects, and potentially animals in general, adapted to destabilize cellular homeostasis in response to anoxic stress. It is worth noting that this physiological response to anoxia similarly occurs in insects exposed to hypothermic and hyperthermic stress [92,93,102]. When examining the common links between these stressors in insects and in the anoxic turtle brain, it is clear that a key factor is maintaining the balance between ATP supply and demand [9], as the Na + /K + ATPase in the human nervous system consumes approximately two-thirds of all ATP produced [103].…”

“…Heat shock (HS) is one such stressor that results in the PC phenotype, although the neurophysiological consequences resulting from the upregulation of HSPs are unclear. One mechanism that has been described occurs in neurons of the insect Locusta migratoria , where a prior HS of 45°C for 3 h and a 1-h recovery leads to the transcription and translation of a number of HSPs with a concomitant reduction in whole-cell K + conductance in the brain [102,104]. The whole-cell peak current (A current) of the K + channels is not disturbed, while the prolonged transient current (B current) is significantly reduced [105].…”

“…Fruit flies that have lower PKG expression due to genetic variation or by modulating activity through pharmacological treatment show prolonged activity in response to acute anoxia [87]. Similarly, when PKG is pharmacologically inhibited by PKG pathway blockers, the locust nervous systems exposed to acute anoxia exhibit neural protection through extended function and a delay in the increase in extracellular K + ; modulating ion channels in this fashion strengthens the membrane’s ability to maintain homeostasis [102,110]. This ‘ionic fortification’ via K + channel conductance inhibition is of importance since it is now possible to mimic the K + channel conductance dynamics of a heat shocked animal (upregulated HSPs) via an acute pharmacological treatment in only seconds, whereas natural induction after HS takes hours [105,109].…”

Neural Thermal Performance in Porcelain Crabs, GenusPetrolisthes

“…Distinct differences in neural thermal tolerance can be explained by changes in enzyme isoform and membrane restructuring but can also result from changes in neural K ϩ conductance (a hypothesis that is based upon previous work in insect models; Wu et al 2001;Robertson 2004aRobertson , 2004bMoney et al 2009). For insects, it has been demonstrated that increasing temperature in Locusta migratoria increases the K ϩ conductance of neurons, resulting in nerve transmission failures; that similar failures can be induced by adding K ϩ to the extracellular fluid (simulating increased K ϩ conductance; Money et al 2009); and that such failures can be prevented by pharmacologically blocking K ϩ channels (Wu et al 2001).…”

“…For insects, it has been demonstrated that increasing temperature in Locusta migratoria increases the K ϩ conductance of neurons, resulting in nerve transmission failures; that similar failures can be induced by adding K ϩ to the extracellular fluid (simulating increased K ϩ conductance; Money et al 2009); and that such failures can be prevented by pharmacologically blocking K ϩ channels (Wu et al 2001). Additionally, increased survival after sublethal heat stress has also been associated with a decrease in nerve membrane K ϩ conductance (Ramirez et al 1999;Money et al 2009). Differences in K ϩ conductance have been shown to correlate with a species' habitat temperature (Rosenthal and Bezanilla 2002).…”