A cold and quiet brain: mechanisms of insect CNS arrest at low temperatures

Robertson, R. Meldrum; MacMillan, Heath A; Andersen, Mads K

doi:10.1016/j.cois.2023.101055

Cited by 16 publications

(7 citation statements)

References 80 publications

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“…1; see ( 1) and ( 42)). However, the properties of this waveform are not constant and are affected by a wide range of factors including thermal acclimation (see Andersen, Robertson and MacMillan (37) and the review by Robertson, MacMillan and Andersen (10)), which makes it challenging to directly compare waveforms from different acclimation groups. Furthermore, because the event itself occurs at different temperatures, the effect of acclimation cannot be separated from any direct effects of temperature.…”

Section: Discussionmentioning

confidence: 99%

“…In ectothermic animals, however, it is often found associated with abiotic stress tolerance. In insects, for example, SD limits organismal tolerance to heat, cold, and anoxia by inducing a state of neuromuscular paralysis (4,(8)(9)(10)(11). SD similarly occurs at the limit for acute heat tolerance in fish (although the order of events is slightly different, see Andreassen et al (12)).…”

Section: Introductionmentioning

confidence: 99%

“…In the case of anoxia-induced SD there is also a small positive shift in TPP immediately before the SD and a small negative shift immediately before the recovery of the TPP. Combined, these parameters make up and characterize the TPP waveform of the SD and can be used to infer changes regarding the integrity of the glial blood-brain barrier, interstitial ion concentrations, and adaptive changes to electrogenic transporters (10,32,33).…”

Section: Introductionmentioning

confidence: 99%

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Thermal acclimation of spreading depolarization in the CNS ofDrosophila melanogaster

Andersen,

Robertson,

MacMillan

2024

Preprint

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During exposure to extreme stress, the CNS of mammals and insects fails through a phenomenon known as spreading depolarization (SD). SD is characterized by an abrupt disruption of ion gradients across neural and glial membranes that spreads through the CNS, silencing neural activity. In humans, SD is associated with neuropathological conditions like migraine and stroke. In insects, it is coincident with critical thermal limits for activity and can be conveniently monitored by observing the transperineurial potential (TPP). We used the TPP to explore the temperature-dependence and plasticity of SD thresholds and SD-induced changes to the TPP in fruit flies (Drosophila melanogaster) acclimated to different temperatures. Specifically, we characterized the effects of thermal acclimation on the TPP characteristics of cold-induced SD, after which we induced SDviaanoxia at different temperatures in both acclimation groups to examine the interactive effects of temperature and acclimation status. Lastly, we investigated these effects on the rate of SD propagation across the fruit fly CNS. Cold acclimation enhanced resistance to both cold- and anoxic SD and our TPP measurements revealed independent and interactive effects of temperature and acclimation on the TPP and SD propagation. This suggests thermodynamic processes and physiological mechanisms interact to modulate the threshold for activity through SD and its electrophysiological phenomenology. These findings are discussed in relation to conceptual models for SD and established mechanisms for variation in the thermal threshold for SD.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Thermal acclimation of spreading depolarization in the CNS ofDrosophila melanogaster

Andersen,

Robertson,

MacMillan

2024

Preprint

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“…Temperature is a critical environmental factor that profoundly influences the physiological processes and behaviors of organisms ( Hofmann and Todgham, 2010 ). The nervous system is particularly affected by temperature changes since these can significantly disrupt cellular and circuit activity ( Robertson and Money, 2012 ; Harding et al, 2019 ; Marder and Rue, 2021 ; Robertson et al, 2023 ) with far-reaching consequences for animal survival and performance. Recent research focusing on understanding the effects of temperature on neural circuits in poikilothermic invertebrates, animals that are especially susceptible to climate change-induced global warming and the associated severe weather events ( Reid et al, 2009 ; Somero, 2010 ; Somero, 2012 ; Mann et al, 2018 ; Oliver et al, 2018 ), has revealed that some neural circuits display automatic robustness to acute temperature perturbations.…”

Section: Introductionmentioning

confidence: 99%

Thermal acclimation and habitat-dependent differences in temperature robustness of a crustacean motor circuit

Stein,

Torres,

Giménez

et al. 2023

Front. Cell. Neurosci.

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IntroductionAt the cellular level, acute temperature changes alter ionic conductances, ion channel kinetics, and the activity of entire neuronal circuits. This can result in severe consequences for neural function, animal behavior and survival. In poikilothermic animals, and particularly in aquatic species whose core temperature equals the surrounding water temperature, neurons experience rather rapid and wide-ranging temperature fluctuations. Recent work on pattern generating neural circuits in the crustacean stomatogastric nervous system have demonstrated that neuronal circuits can exhibit an intrinsic robustness to temperature fluctuations. However, considering the increased warming of the oceans and recurring heatwaves due to climate change, the question arises whether this intrinsic robustness can acclimate to changing environmental conditions, and whether it differs between species and ocean habitats.MethodsWe address these questions using the pyloric pattern generating circuits in the stomatogastric nervous system of two crab species, Hemigrapsus sanguineus and Carcinus maenas that have seen a worldwide expansion in recent decades.Results and discussionConsistent with their history as invasive species, we find that pyloric activity showed a broad temperature robustness (>30°C). Moreover, the temperature-robust range was dependent on habitat temperature in both species. Warm-acclimating animals shifted the critical temperature at which circuit activity breaks down to higher temperatures. This came at the cost of robustness against cold stimuli in H. sanguineus, but not in C. maenas. Comparing the temperature responses of C. maenas from a cold latitude (the North Sea) to those from a warm latitude (Spain) demonstrated that similar shifts in robustness occurred in natural environments. Our results thus demonstrate that neuronal temperature robustness correlates with, and responds to, environmental temperature conditions, potentially preparing animals for changing ecological conditions and shifting habitats.

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“…Tolerance to chilling in insects can be quantified in multiple ways. For example, chill coma onset (CCO) is the temperature at which an insect loses all capacity for movement and is indicative of the thermal limits of neuromuscular function (MacMillan and Sinclair, 2011; Robertson et al, 2023). It can be measured by gradually reducing ambient temperature and recording the temperature at which all movement ceases.…”

Section: Introductionmentioning

confidence: 99%

Effects of a high cholesterol diet onDrosophilachill tolerance are highly context-dependent

Allen,

Ritchie,

El-Saadi

et al. 2023

Preprint

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Chill susceptible insects are thought to be injured through different mechanisms depending on the duration and severity of chilling. While chronic chilling causes “indirect” injury through disruption of metabolic and ion homeostasis, acute chilling is suspected to cause “direct” injury, in part through phase transitions of cell membrane lipids. Dietary supplementation of cholesterol can reduce acute chilling injury inDrosophila melanogaster, but the generality of this effect and the mechanisms underlying it remain unclear. To better understand how and why cholesterol has this effect, we assessed how a high cholesterol diet and thermal acclimation independently and interactively impact several measures of chill tolerance in both male and female flies. Cholesterol supplementation positively affected tolerance to acute chilling in warm-acclimated flies (as reported previously). Conversely, feeding on the high-cholesterol diet negatively affected tolerance to chronic chilling in both cold and warm acclimated flies, as well as tolerance to acute chilling in cold acclimated flies. Cholesterol had no effect on the ability of flies to remain active in the cold or recover movement after a cold stress. Our findings support the idea that dietary cholesterol reduces mechanical injury to membranes caused by direct chilling injury, and that acute and chronic chilling are associated with distinct mechanisms of injury. Feeding on a high-cholesterol diet may interfere with mechanisms involved in cold acclimation, leaving cholesterol augmented flies more susceptible to chilling injury under some conditions.HighlightsCholesterol improves cold shock tolerance of warm-acclimated fliesCold acclimation and chronic cold instead lead to negative effects of cholesterol on chill toleranceCholesterol did not affect the ability of flies to remain active in the coldBoth sexes were similarly affected by a high cholesterol diet

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A cold and quiet brain: mechanisms of insect CNS arrest at low temperatures

Cited by 16 publications

References 80 publications

Thermal acclimation of spreading depolarization in the CNS ofDrosophila melanogaster

Thermal acclimation of spreading depolarization in the CNS ofDrosophila melanogaster

Thermal acclimation and habitat-dependent differences in temperature robustness of a crustacean motor circuit

Effects of a high cholesterol diet onDrosophilachill tolerance are highly context-dependent

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