The Contribution of Extrasynaptic Signaling to Cerebellar Information Processing

Overview

Journal Cerebellum

Publisher Springer

Specialty Neurology

Date 2014 Mar 5

PMID 24590660

Citations 5

Authors

Luke T Coddington

Angela K Nietz

Jacques I Wadiche

Affiliations

Soon will be listed here.

Abstract

The diversity of synapses within the simple modular structure of the cerebellum has been crucial for study of the phasic extrasynaptic signaling by fast neurotransmitters collectively referred to as "spillover." Additionally, the accessibility of cerebellar components for in vivo recordings and their recruitment by simple behaviors or sensory stimuli has allowed for both direct and indirect demonstrations of the effects of transmitter spillover in the intact brain. The continued study of spillover in the cerebellum not only promotes our understanding of information transfer through cerebellar structures but also how extrasynaptic signaling may be regulated and interpreted throughout the CNS.

Citing Articles

Climbing Fiber-Mediated Spillover Transmission to Interneurons Is Regulated by EAAT4.

Malhotra S, Banumurthy G, Pennock R, Vaden J, Sugihara I, Overstreet-Wadiche L J Neurosci. 2021; 41(39):8126-8133.

PMID: 34400517 PMC: 8482868. DOI: 10.1523/JNEUROSCI.0616-21.2021.

Parvalbumin interneurons provide spillover to newborn and mature dentate granule cells.

Vaden R, Gonzalez J, Tsai M, Niver A, Fusilier A, Griffith C Elife. 2020; 9.

PMID: 32602839 PMC: 7326496. DOI: 10.7554/eLife.54125.

Multifaceted circuit functions of adult-born neurons.

Dieni C, Gonzalez J, Overstreet-Wadiche L F1000Res. 2019; 8.

PMID: 31824650 PMC: 6880266. DOI: 10.12688/f1000research.20642.1.

Photolysis of a Caged, Fast-Equilibrating Glutamate Receptor Antagonist, MNI-Caged -D-Glutamyl-Glycine, to Investigate Transmitter Dynamics and Receptor Properties at Glutamatergic Synapses.

Palma-Cerda F, Papageorgiou G, Barbour B, Auger C, Ogden D Front Cell Neurosci. 2019; 12:465.

PMID: 30618624 PMC: 6300705. DOI: 10.3389/fncel.2018.00465.

Non-synaptic signaling from cerebellar climbing fibers modulates Golgi cell activity.

Nietz A, Vaden J, Coddington L, Overstreet-Wadiche L, Wadiche J Elife. 2017; 6.

PMID: 29028183 PMC: 5640426. DOI: 10.7554/eLife.29215.

References

Buckingham S, Campbell S, Haas B, Montana V, Robel S, Ogunrinu T . Glutamate release by primary brain tumors induces epileptic activity. Nat Med. 2011; 17(10):1269-74. PMC: 3192231. DOI: 10.1038/nm.2453. View

Szapiro G, Barbour B . Multiple climbing fibers signal to molecular layer interneurons exclusively via glutamate spillover. Nat Neurosci. 2007; 10(6):735-42. DOI: 10.1038/nn1907. View

Wadiche J, Tzingounis A, Jahr C . Intrinsic kinetics determine the time course of neuronal synaptic transporter currents. Proc Natl Acad Sci U S A. 2006; 103(4):1083-7. PMC: 1348018. DOI: 10.1073/pnas.0510476103. View

Hansel C, Linden D, DAngelo E . Beyond parallel fiber LTD: the diversity of synaptic and non-synaptic plasticity in the cerebellum. Nat Neurosci. 2001; 4(5):467-75. DOI: 10.1038/87419. View

Sah P, HESTRIN S, Nicoll R . Tonic activation of NMDA receptors by ambient glutamate enhances excitability of neurons. Science. 1989; 246(4931):815-8. DOI: 10.1126/science.2573153. View

Mathews P, Lee K, Peng Z, Houser C, Otis T . Effects of climbing fiber driven inhibition on Purkinje neuron spiking. J Neurosci. 2012; 32(50):17988-97. PMC: 3532857. DOI: 10.1523/JNEUROSCI.3916-12.2012. View

Pugh J, Raman I . Potentiation of mossy fiber EPSCs in the cerebellar nuclei by NMDA receptor activation followed by postinhibitory rebound current. Neuron. 2006; 51(1):113-23. DOI: 10.1016/j.neuron.2006.05.021. View

Valera A, Doussau F, Poulain B, Barbour B, Isope P . Adaptation of granule cell to Purkinje cell synapses to high-frequency transmission. J Neurosci. 2012; 32(9):3267-80. PMC: 6622027. DOI: 10.1523/JNEUROSCI.3175-11.2012. View

Lin S, Huck J, Roberts J, Macklin W, Somogyi P, Bergles D . Climbing fiber innervation of NG2-expressing glia in the mammalian cerebellum. Neuron. 2005; 46(5):773-85. DOI: 10.1016/j.neuron.2005.04.025. View

10.

Rudolph S, Overstreet-Wadiche L, Wadiche J . Desynchronization of multivesicular release enhances Purkinje cell output. Neuron. 2011; 70(5):991-1004. PMC: 3148031. DOI: 10.1016/j.neuron.2011.03.029. View

11.

Tsai M, Tanaka K, Overstreet-Wadiche L, Wadiche J . Neuronal glutamate transporters regulate glial excitatory transmission. J Neurosci. 2012; 32(5):1528-35. PMC: 3532047. DOI: 10.1523/JNEUROSCI.5232-11.2012. View

12.

Harvey R, Napper R . Quantitative study of granule and Purkinje cells in the cerebellar cortex of the rat. J Comp Neurol. 1988; 274(2):151-7. DOI: 10.1002/cne.902740202. View

13.

Sargent P, Saviane C, Nielsen T, DiGregorio D, Silver R . Rapid vesicular release, quantal variability, and spillover contribute to the precision and reliability of transmission at a glomerular synapse. J Neurosci. 2005; 25(36):8173-87. PMC: 6725539. DOI: 10.1523/JNEUROSCI.2051-05.2005. View

14.

Zhang W, Linden D . Long-term depression at the mossy fiber-deep cerebellar nucleus synapse. J Neurosci. 2006; 26(26):6935-44. PMC: 6673927. DOI: 10.1523/JNEUROSCI.0784-06.2006. View

15.

Isaacson J . Glutamate spillover mediates excitatory transmission in the rat olfactory bulb. Neuron. 1999; 23(2):377-84. DOI: 10.1016/s0896-6273(00)80787-4. View

16.

Telgkamp P, Padgett D, Ledoux V, Woolley C, Raman I . Maintenance of high-frequency transmission at purkinje to cerebellar nuclear synapses by spillover from boutons with multiple release sites. Neuron. 2004; 41(1):113-26. DOI: 10.1016/s0896-6273(03)00802-x. View

17.

Bosman L, Koekkoek S, Shapiro J, Rijken B, Zandstra F, van der Ende B . Encoding of whisker input by cerebellar Purkinje cells. J Physiol. 2010; 588(Pt 19):3757-83. PMC: 2998225. DOI: 10.1113/jphysiol.2010.195180. View

18.

Schwarz C, Welsh J . Dynamic modulation of mossy fiber system throughput by inferior olive synchrony: a multielectrode study of cerebellar cortex activated by motor cortex. J Neurophysiol. 2001; 86(5):2489-504. DOI: 10.1152/jn.2001.86.5.2489. View

19.

Dittman J, Regehr W . Mechanism and kinetics of heterosynaptic depression at a cerebellar synapse. J Neurosci. 1997; 17(23):9048-59. PMC: 6573588. View

20.

Collin T, Franconville R, Ehrlich B, Llano I . Activation of metabotropic glutamate receptors induces periodic burst firing and concomitant cytosolic Ca2+ oscillations in cerebellar interneurons. J Neurosci. 2009; 29(29):9281-91. PMC: 6665558. DOI: 10.1523/JNEUROSCI.1865-09.2009. View