Postnatal Switch from Synaptic to Extrasynaptic Transmission between Interneurons and NG2 Cells

Vélez-Fort, Mateo; Maldonado, Paloma P.; Butt, Arthur M.; Audinat, Etienne; Angulo, Marı́a Cecilia

doi:10.1523/jneurosci.0238-10.2010

Cited by 96 publications

(187 citation statements)

References 40 publications

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“…OPCs form synapses with glutamatergic neurons in all gray and white matter regions that have been examined, including the hippocampus (Bergles et al 2000;Jabs et al 2005), cerebellum (Lin et al 2005), cortex (Chittajallu et al 2004), brainstem (Muller et al 2009), and white matter tracts (Káradó ttir et al 2005;Kukley et al 2007;Ziskin et al 2007). In gray matter, they also form synapses with GABAergic neurons (Lin and Bergles 2004;Jabs et al 2005;Mangin et al 2008;Tanaka et al 2009;Velez-Fort et al 2010), suggesting that synaptic signaling is an important and highly conserved property of OPCs. Glutamatergic axon-OPC synapses are formed early in development and become more robust (larger currents, more abundant inputs) with age, paralleling the normal development of synapses that occurs in surrounding neurons, whereas GABAergic signaling in the cortex changes from synaptic to extrasynaptic with age (Velez-Fort et al 2010).…”

Section: Axoglial Synaptic Signaling and Developmentmentioning

confidence: 99%

“…In gray matter, they also form synapses with GABAergic neurons (Lin and Bergles 2004;Jabs et al 2005;Mangin et al 2008;Tanaka et al 2009;Velez-Fort et al 2010), suggesting that synaptic signaling is an important and highly conserved property of OPCs. Glutamatergic axon-OPC synapses are formed early in development and become more robust (larger currents, more abundant inputs) with age, paralleling the normal development of synapses that occurs in surrounding neurons, whereas GABAergic signaling in the cortex changes from synaptic to extrasynaptic with age (Velez-Fort et al 2010). Unlike neurons, which participate in circuits as both presynaptic and postsynaptic partners, OPCs appear to be exclusively postsynaptic and receive input from neurons, rather than the reverse.…”

Section: Axoglial Synaptic Signaling and Developmentmentioning

confidence: 99%

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Oligodendrocyte Development and Plasticity

Bergles

Richardson

2015

Cold Spring Harb Perspect Biol

422

437

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Oligodendrocyte precursor cells (OPCs) originate in the ventricular zones (VZs) of the brain and spinal cord and migrate throughout the developing central nervous system (CNS) before differentiating into myelinating oligodendrocytes (OLs). It is not known whether OPCs or OLs from different parts of the VZ are functionally distinct. OPCs persist in the postnatal CNS, where they continue to divide and generate myelinating OLs at a decreasing rate throughout adult life in rodents. Adult OPCs respond to injury or disease by accelerating their cell cycle and increasing production of OLs to replace lost myelin. They also form synapses with unmyelinated axons and respond to electrical activity in those axons by generating more OLs and myelin locally. This experience-dependent "adaptive" myelination is important in some forms of plasticity and learning, for example, motor learning. We review the control of OL lineage development, including OL population dynamics and adaptive myelination in the adult CNS.

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Section: Axoglial Synaptic Signaling and Developmentmentioning

confidence: 99%

Section: Axoglial Synaptic Signaling and Developmentmentioning

confidence: 99%

Oligodendrocyte Development and Plasticity

Bergles

Richardson

2015

Cold Spring Harb Perspect Biol

422

437

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“…Glutamate promotes formation of myelin (241,428), while GABA stimulates OPC migration (407). GABA, like glutamate, may exert its effect extrasynaptically, through volume transmission (421). Glutamate receptor-mediated inhibition of OPC proliferation (131,455) may lead to enhanced conduction velocity due to increased internodal lengths when the axons must be covered by a reduced number of oligodendrocytes.…”

Section: A Glutamate and Gabamentioning

confidence: 99%

“…Microglial serotonin receptors have also been detected (5-HT 1a , 5-HT 1f , 5-HT 2a , 5-HT 7 serotonin receptors) (203,371), along with cholinergic receptors, of which the ␣7 nicotinic type seems to be most prevalent (89, 377), while the presence of muscarinic receptors in microglia has been suggested (165). Several studies have detected effects of stimulating adrenergic receptors on cultured microglia (127,337,422).…”

Section: B Microglia Express Neurotransmitter Receptorsmentioning

confidence: 99%

Neuroglial Transmission

Gundersen

Storm‐Mathisen

Bergersen

2015

Physiological Reviews

146

113

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Neuroglia, the "glue" that fills the space between neurons in the central nervous system, takes active part in nerve cell signaling. Neuroglial cells, astroglia, oligodendroglia, and microglia, are together about as numerous as neurons in the brain as a whole, and in the cerebral cortex grey matter, but the proportion varies widely among brain regions. Glial volume, however, is less than one-fifth of the tissue volume in grey matter. When stimulated by neurons or other cells, neuroglial cells release gliotransmitters by exocytosis, similar to neurotransmitter release from nerve endings, or by carrier-mediated transport or channel flux through the plasma membrane. Gliotransmitters include the common neurotransmitters glutamate and GABA, the nonstandard amino acid d-serine, the high-energy phosphate ATP, and l-lactate. The latter molecule is a "buffer" between glycolytic and oxidative metabolism as well as a signaling substance recently shown to act on specific lactate receptors in the brain. Complementing neurotransmission at a synapse, neuroglial transmission often implies diffusion of the transmitter over a longer distance and concurs with the concept of volume transmission. Transmission from glia modulates synaptic neurotransmission based on energetic and other local conditions in a volume of tissue surrounding the individual synapse. Neuroglial transmission appears to contribute significantly to brain functions such as memory, as well as to prevalent neuropathologies.

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“…Patch-clamp studies have identified two classes of OLP in white matter - those with synaptic input and voltage-gated Na + currents and others that have undetectable Na + currents (Karadottir et al, 2008). Some of this variation might reflect developmental stage (De Biase et al, 2010; Etxeberria et al, 2010; Kukley et al, 2010; Velez-Fort et al, 2010), although a fraction of NG2-expressing OLPs lack detectable Na + currents (Karadottir et al, 2008; Clarke et al, 2011). …”

Section: Introductionmentioning

confidence: 99%

Dorsally and Ventrally Derived Oligodendrocytes Have Similar Electrical Properties but Myelinate Preferred Tracts

Tripathi¹,

Clarke²,

Burzomato³

et al. 2011

J. Neurosci.

159

167

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In the developing spinal cord most oligodendrocyte precursors (OLPs) arise from the ventral ventricular zone (VZ) under the influence of Sonic Hedgehog but a minority is generated from the dorsal VZ in a Hedgehog-independent manner. In the developing forebrain too, OLPs arise from both the ventral and the dorsal VZ. It is not known whether dorsally- and ventrally- derived oligodendrocyte (OL) lineage cells have different properties. We generated a dual reporter mouse line to color code ventrally- and dorsally-derived OLPs (vOLPs and dOLPs) and their differentiated oligodendrocyte progeny (vOLs and dOLs) for functional studies. We found that ~80% of OL lineage cells in the postnatal spinal cord and ~20% in the corpus callosum are ventrally-derived. In both spinal cord and corpus callosum, vOLPs and dOLPs had indistinguishable electrical properties, as did vOLs and dOLs. However, vOLPs and dOLPs had different migration and settling patterns. In the spinal cord, vOLPs appeared early and spread uniformly throughout the cord whereas dOLPs arrived later and remained mainly in the dorsal and dorsolateral funiculi. During adulthood, corticospinal and rubrospinal tracts became myelinated mainly by dOLs, even though vOLs dominated these tracts during early postnatal life. Thus, dOLPs are electrically similar to vOLPs but appear to out-compete them for dorsal axons.

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Postnatal Switch from Synaptic to Extrasynaptic Transmission between Interneurons and NG2 Cells

Cited by 96 publications

References 40 publications

Oligodendrocyte Development and Plasticity

Oligodendrocyte Development and Plasticity

Neuroglial Transmission

Dorsally and Ventrally Derived Oligodendrocytes Have Similar Electrical Properties but Myelinate Preferred Tracts

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