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, 2014;Findsen, Overgaard, & Pedersen, 2016;Overgaard & MacMillan, 2017;Parker et al, 2018;Teets, Yi, Lee, & Denlinger, 2013). 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, 2015;Findsen et al, 2016), as well as changes in extracellular potassium that spreads depolarization across cell membranes (Robertson et al, 2017). 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 related to the nervous system are generally important for maintaining activity at temperature extremes (Robertson, Spong, & Srithiphaphirom, 2017), with those involved in neuromuscular function obvious candidates because of the importance of flight muscle (Esch & Goller, 1991;Goller & Esch, 1990;Kammer & Heinrich, 1972;MacMillan et al, 2016). 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, 2015;Overgaard & MacMillan, 2017;Robertson et al, 2017).…”

“…Genes related to the nervous system are generally important for maintaining activity at temperature extremes (Robertson, Spong, & Srithiphaphirom, 2017), with those involved in neuromuscular function obvious candidates because of the importance of flight muscle (Esch & Goller, 1991;Goller & Esch, 1990;Kammer & Heinrich, 1972;MacMillan et al, 2016). 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, 2015;Overgaard & MacMillan, 2017;Robertson et al, 2017). 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, 2011), including genes related to cuticle composition and minimizing water loss from respiration (e.g., tracheal or spiracle development) (Gibbs, Chippindale, & Rose, 1997;Gibbs, Fukuzato, & Matzkin, 2003;Telonis-Scott, Gane, DeGaris, Sgró, & Hoffmann, 2012).…”

An impressive capacity for cold tolerance plasticity protects against ionoregulatory collapse in the disease vector,Aedes aegypti

“…1A), despite being more tolerant of chilling by every other measure. The CCO, CCRT, and chilling injury are all thought to be related to the capacity to maintain ion and water balance, but are mediated by different specific physiological mechanisms of failure occurring in different organs and across different time scales (MacMillan, 2019; Overgaard & MacMillan, 2017; Robertson et al, 2017). Our results in the present study thus suggest that acclimation alters mechanisms underlying CCRT and the development of chilling injury without impacting the temperature that causes paralysis.…”

“…Consequently, measures of cold tolerance relevant to freeze avoidant and freeze tolerant insects, such as the supercooling point (the temperature of spontaneous ice formation within the body) or survival following freezing, are irrelevant to characterizing the thermal limits of chill susceptible insects (Overgaard & MacMillan, 2017). When cooled below a critical threshold temperature, chill susceptible insects suffer a local loss of ion homeostasis in the nervous system, leading to nerve depolarization (spreading depression) and a state of complete neuromuscular silence termed chill coma (MacMillan & Sinclair, 2011a; Mellanby, 1939; Robertson, Spong, & Srithiphaphirom, 2017). The temperature at which this paralytic state occurs is called the chill coma onset temperature (CCO) (Overgaard & MacMillan, 2017).…”