From synaptic input to muscle contraction: arm muscle cells of Octopus vulgaris show unique neuromuscular junction and excitation–contraction coupling properties

Nir Nesher, Federica Maiole, T. Shomrat, B. Hochner, L. Zullo
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引用次数: 15

Abstract

The muscular-hydrostat configuration of octopus arms allows high manoeuvrability together with the efficient motor performance necessary for its multitasking abilities. To control this flexible and hyper-redundant system the octopus has evolved unique strategies at the various levels of its brain-to-body organization. We focus here on the arm neuromuscular junction (NMJ) and excitation–contraction (E-C) properties of the arm muscle cells. We show that muscle cells are cholinergically innervated at single eye-shaped locations where acetylcholine receptors (AChR) are concentrated, resembling the vertebrate neuromuscular endplates. Na+ and K+ contribute nearly equally to the ACh-activated synaptic current mediating membrane depolarization, thereby activating voltage-dependent L-type Ca2+ channels. We show that cell contraction can be mediated directly by the inward Ca2+ current and also indirectly by calcium-induced calcium release (CICR) from internal stores. Indeed, caffeine-induced cell contraction and immunohistochemical staining revealed the presence and close association of dihydropyridine (DHPR) and ryanodine (RyR) receptor complexes, which probably mediate the CICR. We suggest that the dynamics of octopus arm contraction can be controlled in two ways; motoneurons with large synaptic inputs activate vigorous contraction via activation of the two routs of Ca2+ induced contraction, while motoneurons with lower-amplitude inputs may regulate a graded contraction through frequency-dependent summation of EPSP trains that recruit the CICR. Our results thus suggest that these motoneuronal pools are likely to be involved in the activation of different E-C coupling modes, thus enabling a dynamics of muscles activation appropriate for various tasks such as stiffening versus motion generation.
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从突触输入到肌肉收缩:寻常章鱼臂肌细胞表现出独特的神经肌肉连接和兴奋-收缩耦合特性
章鱼臂的肌肉-静水器配置允许高机动性以及有效的运动性能,这是多任务处理能力所必需的。为了控制这个灵活且高度冗余的系统,章鱼在其脑-体组织的各个层面上进化出了独特的策略。我们在这里着重于手臂神经肌肉连接(NMJ)和手臂肌肉细胞的兴奋-收缩(E-C)特性。我们发现,在乙酰胆碱受体(AChR)集中的单个眼形位置,肌肉细胞受胆碱能支配,类似于脊椎动物的神经肌肉终板。Na+和K+对ach激活的突触电流介导膜去极化的贡献几乎相等,从而激活电压依赖性的l型Ca2+通道。我们发现细胞收缩可以由向内的Ca2+电流直接介导,也可以通过钙诱导的钙释放(CICR)从内部储存间接介导。事实上,咖啡因诱导的细胞收缩和免疫组化染色显示了二氢吡啶(DHPR)和红嘌呤(RyR)受体复合物的存在和密切关联,它们可能介导了CICR。我们认为章鱼臂收缩的动力学可以通过两种方式控制;具有大突触输入的运动神经元通过激活Ca2+诱导的两条路径来激活剧烈收缩,而具有低振幅输入的运动神经元可能通过频率依赖的EPSP序列累加CICR来调节渐变收缩。因此,我们的研究结果表明,这些运动神经元池可能参与不同的E-C耦合模式的激活,从而使肌肉激活的动态适合于各种任务,如僵硬与运动产生。
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