Dynamic Modulation of Myelination in Response to Visual Stimuli Alters Optic Nerve Conduction Velocity

Myelin controls the time required for an action potential to travel from the neuronal soma to the axon terminal, defining the temporal manner in which information is processed within the CNS. The presence of myelin, the internodal length, and the thickness of the myelin sheath are powerful structura...

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Bibliographic Details
Published in:The Journal of neuroscience 2016-06, Vol.36 (26), p.6937-6948
Main Authors: Etxeberria, Ainhoa, Hokanson, Kenton C, Dao, Dang Q, Mayoral, Sonia R, Mei, Feng, Redmond, Stephanie A, Ullian, Erik M, Chan, Jonah R
Format: Article
Language:English
Subjects:
Action Potentials - physiology
Age Factors
Animals
Animals, Newborn
Antigens - genetics
Antigens - metabolism
Cholera Toxin - metabolism
Geniculate Bodies - cytology
Geniculate Bodies - physiology
Geniculate Bodies - ultrastructure
LIM-Homeodomain Proteins - genetics
LIM-Homeodomain Proteins - metabolism
Mice
Mice, Inbred C57BL
Mice, Transgenic
Myelin Sheath - metabolism
Myelin Sheath - ultrastructure
Nerve Fibers, Myelinated - physiology
Nerve Fibers, Myelinated - ultrastructure
Neural Conduction - genetics
Neural Conduction - physiology
Optic Nerve - physiology
Optic Nerve - ultrastructure
Organogenesis - genetics
Organogenesis - physiology
Photic Stimulation
Proteoglycans - genetics
Proteoglycans - metabolism
Retinal Ganglion Cells - metabolism
Synaptic Transmission - genetics
Transcription Factors - genetics
Transcription Factors - metabolism
Vesicular Glutamate Transport Protein 2 - genetics
Vesicular Glutamate Transport Protein 2 - metabolism
Vision, Monocular - physiology
Visual Pathways - physiology
Visual Pathways - ultrastructure
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Summary:Myelin controls the time required for an action potential to travel from the neuronal soma to the axon terminal, defining the temporal manner in which information is processed within the CNS. The presence of myelin, the internodal length, and the thickness of the myelin sheath are powerful structural factors that control the velocity and fidelity of action potential transmission. Emerging evidence indicates that myelination is sensitive to environmental experience and neuronal activity. Activity-dependent modulation of myelination can dynamically alter action potential conduction properties but direct functional in vivo evidence and characterization of the underlying myelin changes is lacking. We demonstrate that in mice long-term monocular deprivation increases oligodendrogenesis in the retinogeniculate pathway but shortens myelin internode lengths without affecting other structural properties of myelinated fibers. We also demonstrate that genetically attenuating synaptic glutamate neurotransmission from retinal ganglion cells phenocopies the changes observed after monocular deprivation, suggesting that glutamate may constitute a signal for myelin length regulation. Importantly, we demonstrate that visual deprivation and shortened internodes are associated with a significant reduction in nerve conduction velocity in the optic nerve. Our results reveal the importance of sensory input in the building of myelinated fibers and suggest that this activity-dependent alteration of myelination is important for modifying the conductive properties of brain circuits in response to environmental experience. Oligodendrocyte precursor cells differentiate into mature oligodendrocytes and are capable of ensheathing axons with myelin without molecular cues from neurons. However, this default myelination process can be modulated by changes in neuronal activity. Here, we show, for the first time, that experience-dependent activity modifies the length of myelin internodes along axons altering action potential conduction velocity. Such a mechanism would allow for variations in conduction velocities that provide a degree of plasticity in accordance to environmental needs. It will be important in future work to investigate how these changes in myelination and conduction velocity contribute to signal integration in postsynaptic neurons and circuit function.
ISSN:0270-6474
1529-2401
DOI:10.1523/jneurosci.0908-16.2016