Cold-induced depolarization of insect muscle: differing roles of extracellular K+ during acute and chronic chilling

TY - JOUR

T1 - Cold-induced depolarization of insect muscle

T2 - differing roles of extracellular K+ during acute and chronic chilling

AU - MacMillan, Heath Andrew

AU - Findsen, Anders

AU - Pedersen, Thomas Holm

AU - Overgaard, Johannes

PY - 2014/8

Y1 - 2014/8

N2 - Insects enter chill coma, a reversible state of paralysis, at temperatures below their critical thermal minimum (CTmin), and the time required for an insect to recover after a cold exposure is termed chill coma recovery time (CCRT). The CTmin and CCRT are both important metrics of insect cold tolerance that are used interchangeably, although chill coma recovery is not necessarily permitted by a direct reversal of the mechanism causing chill coma onset. Nevertheless, onset and recovery of coma have been attributed to loss of neuromuscular function due to depolarization of muscle fibre membrane potential (V-m). Here we test the hypothesis that muscle depolarization at chill coma onset and repolarization during chill coma recovery are caused by changes in extracellular [K+] and/or other effects of low temperature. Using Locusta migratoria, we measured in vivo muscle resting potentials of the extensor tibialis during cooling, following prolonged exposure to -2 degrees C and during chill coma recovery, and related changes in V-m to transmembrane [K+] balance and temperature. Although V-m was rapidly depolarized by cooling, hemolymph [K+] did not rise until locusts had spent considerable time in the cold. Nonetheless, a rise in hemolymph [K+] during prolonged cold exposure further depressed muscle resting potential and slowed recovery from chill coma upon rewarming. Muscle resting potentials had a bimodal distribution, and with elevation of extracellular [K+] (but not temperature) muscle resting potentials become unimodal. Thus, a disruption of extracellular [K+] does depolarize muscle resting potential and slow CCRT following prolonged cold exposure. However, onset of chill coma at the CTmin relates to an as-yet-unknown effect of temperature on neuromuscular function.

AB - Insects enter chill coma, a reversible state of paralysis, at temperatures below their critical thermal minimum (CTmin), and the time required for an insect to recover after a cold exposure is termed chill coma recovery time (CCRT). The CTmin and CCRT are both important metrics of insect cold tolerance that are used interchangeably, although chill coma recovery is not necessarily permitted by a direct reversal of the mechanism causing chill coma onset. Nevertheless, onset and recovery of coma have been attributed to loss of neuromuscular function due to depolarization of muscle fibre membrane potential (V-m). Here we test the hypothesis that muscle depolarization at chill coma onset and repolarization during chill coma recovery are caused by changes in extracellular [K+] and/or other effects of low temperature. Using Locusta migratoria, we measured in vivo muscle resting potentials of the extensor tibialis during cooling, following prolonged exposure to -2 degrees C and during chill coma recovery, and related changes in V-m to transmembrane [K+] balance and temperature. Although V-m was rapidly depolarized by cooling, hemolymph [K+] did not rise until locusts had spent considerable time in the cold. Nonetheless, a rise in hemolymph [K+] during prolonged cold exposure further depressed muscle resting potential and slowed recovery from chill coma upon rewarming. Muscle resting potentials had a bimodal distribution, and with elevation of extracellular [K+] (but not temperature) muscle resting potentials become unimodal. Thus, a disruption of extracellular [K+] does depolarize muscle resting potential and slow CCRT following prolonged cold exposure. However, onset of chill coma at the CTmin relates to an as-yet-unknown effect of temperature on neuromuscular function.

KW - Ion balance

KW - Thermal limits

KW - Neuromuscular system

KW - Potassium

KW - DROSOPHILA-MELANOGASTER

KW - ION HOMEOSTASIS

KW - COMA RECOVERY

KW - LOCUSTA-MIGRATORIA

KW - LOW-TEMPERATURE

KW - GRYLLUS-PENNSYLVANICUS

KW - NA+/K+-ATPASE

KW - TOLERANCE

KW - MECHANISMS

KW - ADAPTATION

U2 - 10.1242/jeb.107516

DO - 10.1242/jeb.107516

M3 - Journal article

C2 - 24902750

SN - 0022-0949

VL - 217

SP - 2930

EP - 2938

JO - Journal of Experimental Biology

JF - Journal of Experimental Biology

IS - 16

ER -