Effect of temperature change on synaptic transmission at crayfish neuromuscular junctions

Abstract

Ectothermic animals in areas characterised by seasonal changes are susceptible to extreme fluctuations in temperature. To survive through varied temperatures, ectotherms have developed unique strategies. This study focuses on synaptic transmission function at cold temperatures, as it is a vital component of ectothermic animals' survival. For determining how synaptic transmission is influenced by an acute change in temperature (20°C to 10°C within a minute) and chronic cold (10°C), the crayfish (Procambarus clarkii) neuromuscular junction (NMJ) was used as a model. To simulate chronic cold conditions, crayfish were acclimated to 15°C for 1 week and then to 10°C for 1 week. They were then used to examine the synaptic properties associated with the low output nerve terminals on the opener muscle in the walking legs and high output innervation on the abdominal deep extensor muscle. The excitatory postsynaptic potentials (EPSPs) of the opener NMJs increased in amplitude with acute warming (20°C) after being acclimated to cold; however, the deep extensor muscles showed varied changes in EPSP amplitude. Synaptic transmission at both NMJs was enhanced with exposure to the modulators serotonin or octopamine. The membrane resistance of the muscles decreased 33% and the resting membrane potential hyperpolarised upon warm exposure. Analysis of haemolymph indicated that octopamine increases during cold exposure. These results suggest bioamine modulation as a possible mechanism for ensuring that synaptic transmission remains functional at low temperatures.

Neuromuscular Transmission in a Biological Context

“…Few systematic studies of the effects of temperature on neuromuscular transmission have been made in invertebrates. However, in a recent study in crayfish, no consistent change in EJP amplitude was observed as the temperature was acutely decreased from 20 to 10 °C, in either tonic (walking leg opener) or phasic (deep abdominal lateral extensor) muscles (535).…”

Neuromuscular Transmission in a Biological Context

“…Few systematic studies of the effects of temperature on neuromuscular transmission have been made in invertebrates. However, in a recent study in crayfish, no consistent change in EJP amplitude was observed as the temperature was acutely decreased from 20 to 10 °C, in either tonic (walking leg opener) or phasic (deep abdominal lateral extensor) muscles (535).…”

Neuromodulation Enables Temperature Robustness and Coupling Between Fast and Slow Oscillator Circuits

“…Consequently, modulation of leak currents by neurotransmitters has been proposed to contribute to the regulation of neuronal excitability ( Aller et al, 2005 ; Kim, 2005 ; Pratt and Aizenman, 2007 ). There are also several examples where neuromodulators, and neuropeptides in particular, have been implicated in supporting robust activity in several pattern-generating networks ( Gray et al, 1999 ; Mutolo et al, 2010 ; Zhao et al, 2011 ; Zhu et al, 2018 ; Ellingson et al, 2021 ; Shi et al, 2021 ). Increasing the robustness of a circuit through extrinsic modulation may be especially meaningful when perturbations occur rapidly, like in intertidal species that experience substantial temperature variations within a few minutes ( Stein and Harzsch, 2021 ).…”

Effect of Temperature on Heart Rate for Lucilia sericata (syn Phaenicia sericata) and Drosophila melanogaster with Altered Expression of the TrpA1 Receptors

“…Hyperpolarization of the membrane potential with increased temperatures are documented in various studies in arthropods. The relative change is approximately 1 to 1.3 mV/1 °C change in body wall muscles of crustaceans [ 51 , 52 , 53 , 54 , 55 ].…”

Neuromuscular Transmission in a Biological Context

“…Few systematic studies of the effects of temperature on neuromuscular transmission have been made in invertebrates. However, in a recent study in crayfish, no consistent change in EJP amplitude was observed as the temperature was acutely decreased from 20 to 10 °C, in either tonic (walking leg opener) or phasic (deep abdominal lateral extensor) muscles (535).…”

Neuromodulation Enables Temperature Robustness and Coupling Between Fast and Slow Oscillator Circuits

“…Consequently, modulation of leak currents by neurotransmitters has been proposed to contribute to the regulation of neuronal excitability ( Aller et al, 2005 ; Kim, 2005 ; Pratt and Aizenman, 2007 ). There are also several examples where neuromodulators, and neuropeptides in particular, have been implicated in supporting robust activity in several pattern-generating networks ( Gray et al, 1999 ; Mutolo et al, 2010 ; Zhao et al, 2011 ; Zhu et al, 2018 ; Ellingson et al, 2021 ; Shi et al, 2021 ). Increasing the robustness of a circuit through extrinsic modulation may be especially meaningful when perturbations occur rapidly, like in intertidal species that experience substantial temperature variations within a few minutes ( Stein and Harzsch, 2021 ).…”

Effect of Temperature on Heart Rate for Lucilia sericata (syn Phaenicia sericata) and Drosophila melanogaster with Altered Expression of the TrpA1 Receptors

“…Hyperpolarization of the membrane potential with increased temperatures are documented in various studies in arthropods. The relative change is approximately 1 to 1.3 mV/1 °C change in body wall muscles of crustaceans [ 51 , 52 , 53 , 54 , 55 ].…”

Neuromuscular Transmission in a Biological Context

“…Few systematic studies of the effects of temperature on neuromuscular transmission have been made in invertebrates. However, in a recent study in crayfish, no consistent change in EJP amplitude was observed as the temperature was acutely decreased from 20 to 10 °C, in either tonic (walking leg opener) or phasic (deep abdominal lateral extensor) muscles (535).…”

Neuromodulation Enables Temperature Robustness and Coupling Between Fast and Slow Oscillator Circuits

“…Consequently, modulation of leak currents by neurotransmitters has been proposed to contribute to the regulation of neuronal excitability ( Aller et al, 2005 ; Kim, 2005 ; Pratt and Aizenman, 2007 ). There are also several examples where neuromodulators, and neuropeptides in particular, have been implicated in supporting robust activity in several pattern-generating networks ( Gray et al, 1999 ; Mutolo et al, 2010 ; Zhao et al, 2011 ; Zhu et al, 2018 ; Ellingson et al, 2021 ; Shi et al, 2021 ). Increasing the robustness of a circuit through extrinsic modulation may be especially meaningful when perturbations occur rapidly, like in intertidal species that experience substantial temperature variations within a few minutes ( Stein and Harzsch, 2021 ).…”

Effect of Temperature on Heart Rate for Lucilia sericata (syn Phaenicia sericata) and Drosophila melanogaster with Altered Expression of the TrpA1 Receptors

“…Hyperpolarization of the membrane potential with increased temperatures are documented in various studies in arthropods. The relative change is approximately 1 to 1.3 mV/1 °C change in body wall muscles of crustaceans [ 51 , 52 , 53 , 54 , 55 ].…”