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

Bakiri, Y; Karadottir, R; Cossell, L; Attwell, D; (2011) Morphological and electrical properties of oligodendrocytes in the white matter of the corpus callosum and cerebellum. J PHYSIOL-LONDON , 589 (3) 559 - 573. 10.1113/jphysiol.2010.201376.

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Abstract

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.

Type: Article
Title: Morphological and electrical properties of oligodendrocytes in the white matter of the corpus callosum and cerebellum
DOI: 10.1113/jphysiol.2010.201376
Keywords: CENTRAL-NERVOUS-SYSTEM, RAT OPTIC-NERVE, SPINAL-CORD, POTASSIUM CHANNELS, MYELINATED NERVE, GLIAL-CELLS, LUCIFER-YELLOW, GAP-JUNCTIONS, NEURONS, FIBERS
UCL classification: UCL > School of Life and Medical Sciences
UCL > School of Life and Medical Sciences > Faculty of Brain Sciences
UCL > School of Life and Medical Sciences > Faculty of Brain Sciences > Institute of Neurology
UCL > School of Life and Medical Sciences > Faculty of Brain Sciences > Institute of Neurology > Clinical and Experimental Epilepsy
UCL > School of Life and Medical Sciences > Faculty of Life Sciences
URI: http://discovery.ucl.ac.uk/id/eprint/402076
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