Hibernation reduces GABA signaling in the brainstem to enhance motor activity of breathing at cool temperatures.

IF 4.4 1区 生物学 Q1 BIOLOGY BMC Biology Pub Date : 2024-11-04 DOI:10.1186/s12915-024-02050-5
Sandy E Saunders, Joseph M Santin
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Abstract

Background: Neural circuits produce reliable activity patterns despite disturbances in the environment. For this to occur, neurons elicit synaptic plasticity during perturbations. However, recent work suggests that plasticity not only regulates circuit activity during disturbances, but these modifications may also linger to stabilize circuits during future perturbations. The implementation of such a regulation scheme for real-life environmental challenges of animals remains unclear. Amphibians provide insight into this problem in a rather extreme way, as circuits that generate breathing are inactive for several months during underwater hibernation and use compensatory plasticity to promote ventilation upon emergence.

Results: Using ex vivo brainstem preparations and electrophysiology, we find that hibernation in American bullfrogs reduces GABAA receptor (GABAAR) inhibition in respiratory rhythm generating circuits and motor neurons, consistent with a compensatory response to chronic inactivity. Although GABAARs are normally critical for breathing, baseline network output at warm temperatures was not affected. However, when assessed across a range of temperatures, hibernators with reduced GABAAR signaling had greater activity at cooler temperatures, enhancing respiratory motor output under conditions that otherwise strongly depress breathing.

Conclusions: Hibernation reduces GABAAR signaling to promote robust respiratory output only at cooler temperatures. Although frogs do not ventilate lungs during underwater hibernation, we suggest this would be beneficial for stabilizing breathing when the animal passes through a large temperature range during emergence in the spring. More broadly, these results demonstrate that compensatory synaptic plasticity can increase the operating range of circuits in harsh environments, thereby promoting adaptive behavior in conditions that suppress activity.

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冬眠会减少脑干中的 GABA 信号,从而在低温条件下增强呼吸运动。
背景:尽管环境受到干扰,神经回路仍能产生可靠的活动模式。为了实现这一点,神经元在受到干扰时会产生突触可塑性。然而,最近的研究表明,可塑性不仅能在干扰期间调节神经回路的活动,而且在未来的干扰期间,这些可塑性还能稳定神经回路。针对动物在现实生活中面临的环境挑战,如何实施这种调节方案仍不清楚。两栖动物以一种相当极端的方式深入探讨了这一问题,因为在水下冬眠期间,产生呼吸的回路在几个月内都处于不活跃状态,而在出现时,它们会利用补偿可塑性来促进通气:通过体外脑干制备和电生理学研究,我们发现美国牛蛙冬眠会降低呼吸节律产生回路和运动神经元中的 GABAA 受体(GABAAR)抑制作用,这与长期不活动的代偿反应一致。虽然 GABAAR 通常对呼吸至关重要,但在温暖温度下,基线网络输出不受影响。然而,当在一定温度范围内进行评估时,GABAAR信号减少的冬眠者在较低温度下有更大的活动,从而在原本强烈抑制呼吸的条件下增强了呼吸运动输出:结论:冬眠减少了 GABAAR 信号传导,只有在温度较低时才能促进呼吸输出。虽然青蛙在水下冬眠期间不会对肺部进行换气,但我们认为,当动物在春季萌发时经过较大的温度范围时,这将有利于稳定呼吸。更广泛地说,这些结果表明,补偿性突触可塑性可以增加电路在恶劣环境中的工作范围,从而促进在抑制活动的条件下的适应行为。
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来源期刊
BMC Biology
BMC Biology 生物-生物学
CiteScore
7.80
自引率
1.90%
发文量
260
审稿时长
3 months
期刊介绍: BMC Biology is a broad scope journal covering all areas of biology. Our content includes research articles, new methods and tools. BMC Biology also publishes reviews, Q&A, and commentaries.
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