Activity-Dependent Myelination of Parvalbumin Interneurons Mediated by Axonal Morphological Plasticity

Stedehouder, Jeffrey; Brizee, Demi; Shpak, Guy; Kushner, Steven A.

doi:10.1523/jneurosci.0074-18.2018

Cited by 89 publications

(100 citation statements)

References 21 publications

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“…However, myelin is also present within the cortical grey matter, where it is heterogeneous and patchy along projection neurons 10,11 . Moreover, a large fraction of the parvalbumin-positive interneuron axons are myelinated 12–14 , even though their typical short distance to their target cells has been estimated to cause insignificant conduction delay times 13 . Oligodendrocyte lineage cells can myelinate axons in an activity dependent manner and influence their conduction velocity properties 15–19 .…”

Section: Introductionmentioning

confidence: 99%

A role of oligodendrocytes in information processing independent of conduction velocity

Moore

Meschkat

Ruhwedel

et al. 2019

Preprint

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41Myelinating oligodendrocytes enable fast impulse propagation along axons as revealed 42 through studies of homogeneously myelinated white matter tracts. However, gray matter 43 myelination patterns are different, with sparsely myelinated sections leaving large 44 portions of the axons naked. The consequences of this patchy myelination for 45 oligodendrocyte function are not understood but suggest other roles in information 46 processing beyond the regulation of axonal conduction velocity. Here, we analyzed the 47 contribution of myelin to auditory information processing using paradigms that are good 48 predictors of speech understanding in humans. We compared mice with different degrees 49 of dysmyelination using acute cortical multiunit recordings in combination with behavioral 50 readouts. We identified complex alterations of neuronal responses that reflect fatigue and 51 temporal acuity deficits. Partially discriminable but overall similar deficits were observed 52 in mice with oligodendrocytes that can myelinate but cannot fully support axons 53 metabolically. Thus, myelination contributes to sustained stimulus perception in 54 temporally complex paradigms, revealing a role of oligodendrocytes in the CNS beyond 55 the increase of axonal conduction velocity. 56 65 66Importantly, at the network level, the contribution of CNS myelination to information 67 processing remains poorly understood, in part because suitable phenotyping instruments 68 have been lacking. Yet, there is an increasing awareness that myelination is required for 69 higher-order brain functions. Subtle defects of the white matter have been associated with 70 various psychiatric diseases 6 . Moreover, in the aging brain, the physiological decline of 71 function is associated with subtle but widespread structural deterioration of myelin 7,8 . 72Functional studies of myelin have largely been restricted to motor behavior, which is 73 under control of myelinated axons in white matter tracts, and to the fast impulse 74 propagation and millisecond precision required for sound location in a highly specialized 75 circuit of the brain stem 9 . However, myelin is also present within the cortical grey matter, 76 where it is heterogeneous and patchy along projection neurons 10,11 . Moreover, a large 77 fraction of the parvalbumin-positive interneuron axons are myelinated 12-14 , even though 78 their typical short distance to their target cells has been estimated to cause insignificant 79 conduction delay times 13 . Oligodendrocyte lineage cells can myelinate axons in an 80 activity dependent manner and influence their conduction velocity properties [15][16][17][18][19] . Mature 81 oligodendrocytes respond to glutamatergic signals with enhanced glycolytic support of 82 the axonal energy metabolism 4,5 . These data are compatible with the idea that myelin 83 function in the CNS that go beyond regulating conduction velocity. 85Indeed, there is still a major conceptual gap between the role of myelin in saltatory 86 impulse propagation and its function ...

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Section: Introductionmentioning

confidence: 99%

A role of oligodendrocytes in information processing independent of conduction velocity

Moore

Meschkat

Ruhwedel

et al. 2019

Preprint

View full text Add to dashboard Cite

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“…Furthermore, the myelin remodeling observed on PV + axons after activity seems to mainly depend on changes in axon morphology rather than a released molecule. Indeed, axonal morphology predicts the myelin changes induced by activity (Stedehouder et al, ). This observation is in agreement with recent experiments showing that increasing the caliber of normally unmyelinated axons induces their myelination (Goebbels et al, ; Mayoral, Etxeberria, Shen, & Chan, ).…”

Section: Gaba In Neuron–oligodendroglia Communicationmentioning

confidence: 99%

“…While the implication of PV + interneuron activity on their own myelination has been confirmed (Stedehouder, Brizee, Shpak, & Kushner, 2018), the role of GABA receptors is uncertain. In a recent study, Stedehouder et al (2018) showed that the specific chemogenetic stimulation of PV + interneurons modifies the morphology and myelination of PV + axons without changing the total myelin content or the OL cell density. The activity of PV + interneurons seems therefore to specifically control the myelination of PV + axons.…”

Section: Gaba In Adaptive Myelinationmentioning

confidence: 99%

Glutamate versus GABA in neuron–oligodendroglia communication

Habermacher

Angulo

Benamer

2019

Glia

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In the central nervous system (CNS), myelin sheaths around axons are formed by glial cells named oligodendrocytes (OLs). In turn, OLs are generated by oligodendrocyte precursor cells (OPCs) during postnatal development and in adults, according to a process that depends on the proliferation and differentiation of these progenitors. The maturation of OL lineage cells as well as myelination by OLs are complex and highly regulated processes in the CNS. OPCs and OLs express an array of receptors for neurotransmitters, in particular for the two main CNS neurotransmitters glutamate and GABA, and are therefore endowed with the capacity to respond to neuronal activity. Initial studies in cell cultures demonstrated that both glutamate and GABA signaling mechanisms play important roles in OL lineage cell development and function. However, much remains to be learned about the communication of glutamatergic and GABAergic neurons with oligodendroglia in vivo. This review focuses on recent major advances in our understanding of the neuron–oligodendroglia communication mediated by glutamate and GABA in the CNS, and highlights the present controversies in the field. We discuss the expression, activation modes and potential roles of synaptic and extrasynaptic receptors along OL lineage progression. We review the properties of OPC synaptic connectivity with presynaptic glutamatergic and GABAergic neurons in the brain and consider the implication of glutamate and GABA signaling in activity‐driven adaptive myelination.

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“…Since these early studies in the visual system, a wide range of animal models have been used to investigate the responsiveness of myelination to either environmental input or neuronal activity. These diverse approaches include stimulating or blocking activity in myelinating co‐cultures (Demerens et al, ; Lundgaard et al, ; Stevens, Porta, Haak, Gallo, & Fields, ; Wake, Lee, & Fields, ), social isolation or environmental deprivation (Hughes, Orthmann‐Murphy, Langseth, & Bergles, ; Liu et al, ; Makinodan, Rosen, Ito, & Corfas, ; Narducci et al, ), motor training (McKenzie et al, ; Sampaio‐Baptista et al, ), optogenetic, electrophysiological, or chemogenetic stimulation of neurons in the mouse brain (Gibson et al, ; Li, Brus‐Ramer, Martin, & McDonald, ; Mitew et al, ; Stedehouder, Brizee, Shpak, & Kushner, ) or genetic modulation of neuronal firing and vesicular release in the zebrafish (Hines, Ravanelli, Schwindt, Scott, & Appel, ; Koudelka et al, ; Mensch et al, ).…”

Section: Introductionmentioning

confidence: 99%

“…Whether signaling from active axons to the mature myelin also results in active modification of the myelin sheath remains unclear. BDNF, brain-derived neurotropic factor; OPC, oligodendrocyte progenitor cell Makinodan, Rosen, Ito, & Corfas, 2012;Narducci et al, 2018), motor training (McKenzie et al, 2014Sampaio-Baptista et al, 2013), optogenetic, electrophysiological, or chemogenetic stimulation of neurons in the mouse brain (Gibson et al, 2014;Li, Brus-Ramer, Martin, & McDonald, 2010;Mitew et al, 2018;Stedehouder, Brizee, Shpak, & Kushner, 2018) or genetic modulation of neuronal firing and vesicular release in the zebrafish (Hines, Ravanelli, Schwindt, Scott, & Appel, 2015;Koudelka et al, 2016;Mensch et al, 2015).…”

Section: Introductionmentioning

confidence: 99%

Axoglial interactions in myelin plasticity: Evaluating the relationship between neuronal activity and oligodendrocyte dynamics

Foster

Bujalka

Emery

2019

Glia

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Myelin is a critical component of the vertebrate nervous system, both increasing the conduction velocity of myelinated axons and allowing for metabolic coupling between the myelinating cells and axons. An increasing number of studies demonstrate that myelination is not simply a developmentally hardwired program, but rather that new myelinating oligodendrocytes can be generated throughout life. The generation of these oligodendrocytes and the formation of myelin are influenced both during development and adulthood by experience and levels of neuronal activity. This led to the concept of adaptive myelination, where ongoing activity‐dependent changes to myelin represent a form of neural plasticity, refining neuronal functioning, and circuitry. Although human neuroimaging experiments support the concept of dynamic changes within specific white matter tracts relevant to individual tasks, animal studies have only just begun to probe the extent to which neuronal activity may alter myelination at the level of individual circuits and axons. Uncovering the role of adaptive myelination requires a detailed understanding of the localized interactions that occur between active axons and myelinating cells. In this review, we focus on recent animal studies that have begun to investigate the interactions between active axons and myelinating cells and review the evidence for—and against—the ability of neuronal activity to alter myelination at an axon‐specific level.

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Activity-Dependent Myelination of Parvalbumin Interneurons Mediated by Axonal Morphological Plasticity

Cited by 89 publications

References 21 publications

A role of oligodendrocytes in information processing independent of conduction velocity

A role of oligodendrocytes in information processing independent of conduction velocity

Glutamate versus GABA in neuron–oligodendroglia communication

Axoglial interactions in myelin plasticity: Evaluating the relationship between neuronal activity and oligodendrocyte dynamics

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