Morphological and electrical properties of oligodendrocytes in the white matter of the corpus callosum and cerebellum

Morphological and electrical properties of oligodendrocytes in the white matter of the corpus callosum and cerebellum
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DOI:
10.1113/jphysiol.2010.201376
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发表时间:
2011-02-01
影响因子:
5.5
通讯作者:
Attwell, David
Attwell, David
中科院分区:
医学1区
文献类型:
--
作者:
Bakiri, Yamina;Karadottir, Ragnhildur;Attwell, David

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在中枢神经系统中,电信号通过神经细胞被一种叫做少突胶质细胞的细胞加速,这种细胞用一种叫做髓磷脂的脂肪层包裹着神经细胞。这一层对于快速信息处理很重要,但常常在疾病中丢失,在多发性硬化症、中风、脑瘫和脊髓损伤中导致精神或身体损伤。髓磷脂以两种方式加速信息流,通过降低神经细胞的电容和增加其膜阻力,但髓磷脂功能的后一方面知之甚少。通过对少突胶质细胞的电记录和对其形态的成像,我们对其几何形状进行了表征,并首次对大脑中髓磷脂的抵抗力进行了表征。这揭示了两个脑区少突胶质细胞特性之间的差异,并确定髓磷脂的抵抗力足够高,可以防止电流通过髓磷脂泄漏导致神经电信号显著减慢。尽管教科书上描述少突胶质细胞“隔离”轴突,但少突胶质细胞节间膜的电阻率是未知的,并且对于髓鞘数量不同或位于不同脑区的少突胶质细胞的电学性质如何不同也是未知的。我们使用全细胞贴片夹紧和染色填充形态学来表征胼胝体和小脑白质中少突胶质细胞的电特性。出生后第12天,胼胝体的少突胶质细胞形成类似10个轴突的髓鞘,而小脑的少突胶质细胞形成类似7个轴突的髓鞘。胼胝体的节间长度比小脑短,而胼胝体和小脑少突胶质细胞的体直径相似。通过将少突胶质细胞的电导率与它们形成的结间的数量和长度相关联,我们估计了每个结间过程的电导率和少突胶质细胞结间膜单位面积的电导率。一个结间突的衍生阻力在胼胝体少突胶质细胞中类似于1.5 G,在小脑少突胶质细胞中类似于0.6 G。胼胝体少突胶质细胞的特异电导(取决于假设)为0.63-5.5 pS μ m-2,小脑少突胶质细胞的特异电导为0.28-5.0 pS μ m-2。在有髓鞘轴突动作电位传播的计算模型中,使用这些值来评估少突胶质细胞电导和解剖参数对动作电位传播速度的影响。测量的少突胶质细胞膜电导率没有通过短路髓鞘电容显著降低动作电位速度。在其他因素相同的情况下,小脑轴突的传导速度是胼胝体轴突的两倍,这与轴突直径、髓鞘包裹数和节间长度的差异有关。
Non-technical summaryIn the central nervous system, electrical signals passing along nerve cells are speeded by cells called oligodendrocytes, which wrap the nerve cells with a fatty layer called myelin. This layer is important for rapid information processing, and is often lost in disease, causing mental or physical impairment in multiple sclerosis, stroke, cerebral palsy and spinal cord injury. The myelin speeds the information flow in two ways, by decreasing the capacitance of the nerve cell and by increasing its membrane resistance, but little is known about the latter aspect of myelin function. By recording electrically from oligodendrocytes and imaging their morphology we characterised the geometry and, for the first time, the resistance of myelin in the brain. This revealed differences between the properties of oligodendrocytes in two brain areas and established that the resistance of myelin is sufficiently high to prevent significant slowing of the nerve electrical signal by current leakage through the myelin.Despite the textbook description that oligodendrocytes 'insulate' axons, the resistivity of the oligodendrocyte internodal membrane is unknown, and it is unknown how the electrical properties differ for oligodendrocytes which myelinate different numbers of axons or are located in different brain areas. We used whole-cell patch-clamping and dye-fill morphology to characterize the electrical properties of oligodendrocytes in the corpus callosum and the white matter of the cerebellum. At postnatal day 12, oligodendrocytes in the corpus callosum myelinated similar to 10 axons, while oligodendrocytes in the cerebellum myelinated similar to 7 axons. Internode lengths were shorter in the corpus callosum than in cerebellum, while the somata diameters of corpus callosal and cerebellar oligodendrocytes were similar. By correlating the conductance of the oligodendrocytes with the number and length of the internodes they made, we estimated the conductance of each internodal process and the conductivity per unit area of the oligodendrocyte internodal membrane. The derived resistance of one internodal process was similar to 1.5 G in corpus callosal oligodendrocytes and similar to 0.6 G in cerebellar oligodendrocytes. The specific conductance (depending on the assumptions made) was 0.63-5.5 pS mu m-2 for corpus callosal oligodendrocytes and 0.28-5.0 pS mu m-2 for cerebellar oligodendrocytes. These values were used, in a computational model of action potential propagation in a myelinated axon, to assess the effect of the oligodendrocyte conductance and anatomical parameters on the speed of action potential propagation. The measured oligodendrocyte membrane conductivity did not significantly lower the action potential speed by short circuiting the myelin capacitance. Differences in axon diameter, number of myelin wraps and internode length predict that, other factors being equal, the conduction speed for cerebellar axons will be twice that for corpus callosal axons.