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

Abstract

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.

Local adaptation across a complex bioclimatic landscape in two montane bumble bee species

“…We also hypothesized that the cell membrane and ion transport could be important selection targets, especially relating to calcium and potassium ion balance (Cooper, Hammad, & Montooth, ; Findsen, Overgaard, & Pedersen, ; Overgaard & MacMillan, ; Parker et al, ; Teets, Yi, Lee, & Denlinger, ). Challenges to neural and muscular systems from low temperatures can result from inactivation of voltage‐sensitive calcium channels, which drive the action potential upstroke in insect muscle (Andersen et al, ; Findsen et al, ), as well as changes in extracellular potassium that spreads depolarization across cell membranes (Robertson et al, ). Therefore, adaptations to modulate the effects of ion channel thermal sensitivity may be critical to the maintenance of neuromuscular function across environmental temperatures within a species range.…”

“…Genes relating to thoracic muscle function are probably targets of selection from temperature variation across species ranges, as muscles are important both for flight and shivering thermogenesis in Bombus (Heinrich, ; Heinrich & Kammer, ; Hosler, Burns, & Esch, ). Genes related to the nervous system are generally important for maintaining activity at temperature extremes (Robertson, Spong, & Srithiphaphirom, ), with those involved in neuromuscular function obvious candidates because of the importance of flight muscle (Esch & Goller, ; Goller & Esch, ; Kammer & Heinrich, ; MacMillan et al, ). Finally, loss of nerve and muscle excitability at temperature extremes, especially cold, is associated with failure of membrane channels to maintain ion homeostasis, so ion channel genes are also likely candidates (Andersen, MacMillan, & Overgaard, ; Overgaard & MacMillan, ; Robertson et al, ).…”

“…Genes related to the nervous system are generally important for maintaining activity at temperature extremes (Robertson, Spong, & Srithiphaphirom, ), with those involved in neuromuscular function obvious candidates because of the importance of flight muscle (Esch & Goller, ; Goller & Esch, ; Kammer & Heinrich, ; MacMillan et al, ). Finally, loss of nerve and muscle excitability at temperature extremes, especially cold, is associated with failure of membrane channels to maintain ion homeostasis, so ion channel genes are also likely candidates (Andersen, MacMillan, & Overgaard, ; Overgaard & MacMillan, ; Robertson et al, ). Less is known about effects of aridity on Bombus , but from other insects we might expect desiccation tolerance to be an important selection target (Chown, Sørensen, & Terblanche, ), including genes related to cuticle composition and minimizing water loss from respiration (e.g., tracheal or spiracle development) (Gibbs, Chippindale, & Rose, ; Gibbs, Fukuzato, & Matzkin, ; Telonis‐Scott, Gane, DeGaris, Sgró, & Hoffmann, ).…”

Spreading depolarization and repolarization during cardiac arrest as an ultra-early marker of neurological recovery in a preclinical model

“…70,71 Indeed, multiple studies have shown beneficial properties of SD, including preconditioning, upregulation of growth factors, and neurogenesisis. [72][73][74][75][76][77] In addition, previous studies in insects [78][79][80][81] and rodents 72,73,82,83 suggest that SD may play a neuroprotective role during ischemia. 1,84 It is possible that this protection is enabled by a "neuronal silencing" mechanism associated with SD 85 wherein metabolism is quickly shut down, possibly to conserve residual energy and minimize production of reactive oxygen species, potentially leading to an improved survival and outcome in reversible processes.…”

Neural dysfunction correlates with heat coma and CTmax in Drosophila but does not set the boundaries for heat stress survival

“…Spreading depolarisation is triggered by failure 74 to maintain ion gradients between the intra-and extracellular compartments within the CNS, which results in 75 depolarization of neurons and glial cells and a surge of potassium ions in the extracellular space of the brain, 76 preventing neural activity (Robertson, 2004;Robertson et al (submitted); Spong et al, 2016). Furthermore, 77 studies have shown that inter-and intraspecific differences in cold coma are highly correlated with the loss 78 of CNS function in insects Robertson et al, 2017). Given the similarity in the 79 behavioural phenotypes of heat and cold coma there is an obvious possibility that the onset of heat coma is 80 also caused by CNS failure in insects.…”