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

Abstract

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.

The oligodendrocyte growth cone and its actin cytoskeleton: A fundamental element for progenitor cell migration and CNS myelination

“…Within the past few years, it has been recognized that myelination likely follows a basic intrinsic program that functions in the absence of extrinsic molecular instruction. This intrinsic program is thought to be modulated by a so‐called “adaptive program” initiated by extrinsic molecular signals and/or axonal electrical activity (Bechler, Byrne, & Ffrench‐Constant, ; Bechler, Swire, & Ffrench‐Constant, ; de Faria Jr., Pama, Evans, Luzhynskaya, & Karadottir, ; Foster, Bujalka, & Emery, ; Gibson, Geraghty, & Monje, ). Thus, the regulation of myelination via the action of extracellular factors, here referred to as “extrinsically modulated myelination,” could be considered a form of “adaptive” myelination.…”

Accelerated dystrophy and decay of oligodendrocyte precursor cells in the APP/PS1 model of Alzheimer’s-like pathology

“…We did not detect a decrease in GPR17+ or Olig2+ oligodendrocytes, suggesting the decrease in MBP immunostaining at 14-months in APP/PS1 mice is not due to a loss of oligodendrocytes per se, but may reflect a decrease in myelin production, which can involve changes in both the number and lengths of myelin sheaths (Hughes et al, 2018, Hill et al, 2018. Myelin remodelling is important for nervous system plasticity and repair (Ortiz et al, 2019, Chorghay et al, 2018, Williamson and Lyons, 2018, Foster et al, 2019, and the decline in myelination in APP/PS1 may be related to neuronal loss and learning dysfunction in these mice (Chao et al, 2018). The results provide evidence of OPC and myelin disruption in the hippocampus of APP/PS1 mice, suggesting key features of human AD are replicated in this mouse model.…”

Neuron-glia Integrity: Functional Assessment, Molecular Underpinnings, and Implication for Higher Brain Functions

“…OLs in the brain wrap neuronal axons and form the myelin sheath in the brain. The compacted myelin sheath provides high electrical resistance and low capacitance that is essential for saltatory impulse propagation (Foster et al, 2019). These knowledge supports a notion that astrocyte and neuron function as an integrative entity thereby signal transmission within CNS is adjusted (Murai and Pasquale, 2011;Schousboe et al, 2014) and that axonmyelin co-works as an integrative entity that ensures partly processed information can be properly synchronized at post-synaptic sites which is critical for information processing associated with perception, thought and action (Miller, 2002;Xiao et al, 2016).…”