An excitatory GABA loop operating in vivo

Frontiers in Cellular Neuroscience

Volumn 9, Issue JULY, 2015, Pages

  Astorga, Guadalupe ^a,e   Bao, Jin ^a,f   Marty, Alain ^a   Augustine, George J ^b,c,d   Franconville, Romain ^a,g   Jalil, Abdelali ^a   Bradley, Jonathan ^a   Llano, Isabel ^a  

^a CNRS   (France)

^b NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^c INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

^d Korea Institute of Science and Technology   (South Korea)

^e ROCKEFELLER UNIVERSITY   (United States)

^f UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^g Janelia Research Campus ^*  (China)

Author keywords

Calcium; Cerebellum; GABA; Interneurons; Parallel fibers

Indexed keywords

3 AMINO 2 (3 CARBOXYPROPYL) 6 (4 METHOXYPHENYL)PYRIDAZINIUM BROMIDE; 4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; 5, 7 DICHLOROKYNURENIC ACID; CHLORIDE; CYCLIC AMP; NEURONAL NITRIC OXIDE SYNTHASE; RHODOPSIN; TETRODOTOXIN; UNCLASSIFIED DRUG;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DEPTH STIMULATION; BRAIN ELECTROPHYSIOLOGY; CEREBELLUM CORTEX; CONTROLLED STUDY; CRANIOTOMY; EVOKED SOMATOSENSORY RESPONSE; EXCITATORY JUNCTION POTENTIAL; FLUORESCENCE MICROSCOPY; GABAERGIC TRANSMISSION; IMMUNOCYTOCHEMISTRY; INTERNEURON; IONTOPHORESIS; MOUSE; NONHUMAN; PHOTOSTIMULATION; PROTEIN EXPRESSION; SPIKE WAVE; STIMULUS RESPONSE;

EID: 84937414444     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2015.00275     Document Type: Article

References (52)

1. Alger, B. E., and Nicoll, R. A. (1979). GABA-mediated biphasic inhibitory responses in hippocampus. Nature 281, 315-317. doi: 10.1038/281315a0
2. Ben-Ari, Y. (2002). Excitatory actions of gaba during development: the nature of the nurture. Nat. Rev. Neurosci. 3, 728-739. doi: 10.1038/nrn920
3. Ben-Ari, Y., Cherubini, E., Corradetti, R., and Gaiarsa, J. L. (1989). Giant synaptic potentials in immature rat CA3 hippocampal neurones. J. Physiol. 416, 303-325.
4. Bregestovski, P., and Bernard, C. (2012). Excitatory GABA: how a correct observation may turn out to be an experimental artifact. Front. Pharmacol. 3:65. doi: 10.3389/fphar.2012.00065
5. Brenowitz, S. D., and Regehr, W. G. (2007). Reliability and heterogeneity of calcium signaling at single presynaptic boutons of cerebellar granule cells. J. Neurosci. 27, 7888-7898. doi: 10.1523/jneurosci.1064-07.2007
6. Chadderton, P., Margrie, T. W., and Häusser, M. (2004). Integration of quanta in cerebellar granule cells during sensory processing. Nature 428, 856-860. doi: 10.1038/nature02442
7. Chan-Palay, V., and Palay, S. L. (1978). Ultrastructural localization of gamma-aminobutyric acid receptors in the mammalian central nervous system by means of [3H]muscimol binding. Proc. Natl. Acad. Sci. U S A 75, 2977-2980. doi: 10.1073/pnas.75.6.2977
8. Chavas, J., Forero, M. E., Collin, T., Llano, I., and Marty, A. (2004). Osmotic tension as a possible link between GABA(A) receptor activation and intracellular calcium elevation. Neuron 44, 701-713. doi: 10.1016/j.neuron.2004.11.002
9. Collin, T., Chat, M., Lucas, M. G., Moreno, H., Racay, P., Schwaller, B., et al. (2005). Developmental changes in parvalbumin regulate presynaptic Ca2+ signaling. J. Neurosci. 25, 96-107. doi: 10.1523/jneurosci.3748-04.2005
10. Cramer, S. W., Gao, W., Chen, G., and Ebner, T. J. (2013). Reevaluation of the beam and radial hypotheses of parallel fiber action in the cerebellar cortex. J. Neurosci. 33, 11412-11424. doi: 10.1523/jneurosci.0711-13.2013
11. Dellal, S. S., Luo, R., and Otis, T. S. (2012). GABAA receptors increase excitability and conduction velocity of cerebellar parallel fiber axons. J. Neurophysiol. 107, 2958-2970. doi: 10.1152/jn.01028.2011
12. Duguid, I., Branco, T., London, M., Chadderton, P., and Häusser, M. (2012). Tonic inhibition enhances fidelity of sensory information transmission in the cerebellar cortex. J. Neurosci. 32, 11132-11143. doi: 10.1523/jneurosci.0460-12.2012
13. Dzhala, V., Valeeva, G., Glykys, J., Khazipov, R., and Staley, K. (2012). Traumatic alterations in GABA signaling disrupt hippocampal network activity in the developing brain. J. Neurosci. 32, 4017-4031. doi: 10.1523/jneurosci.5139-11.2012
14. Eccles, J. C., Llinás, R., and Sasaki, K. (1966). Parallel fibre stimulation and the responses induced thereby in the Purkinje cells of the cerebellum. Exp. Brain Res. 1, 17-39. doi: 10.1007/bf00235207
15. Edelstein, A., Amodaj, N., Hoover, K., Vale, R., and Stuurman, N. (2010). Computer control of microscopes using µManager. Curr. Protoc. Mol. Biol. 14, 20.1-20.17. doi: 10.1002/0471142727.mb1420s92
16. Eilers, J., Plant, T. D., Marandi, N., and Konnerth, A. (2001). GABA-mediated Ca2+ signalling in developing rat cerebellar Purkinje neurones. J. Physiol. 536, 429-437. doi: 10.1111/j.1469-7793.2001.0429c.xd
17. Farrant, M., and Nusser, Z. (2005). Variations on an inhibitory theme: phasic and tonic activation of GABA(A) receptors. Nat. Rev. Neurosci. 6, 215-229. doi: 10.1038/nrn1625
18. Franconville, R., Revet, G., Astorga, G., Schwaller, B., and Llano, I. (2011). Somatic calcium level reports integrated spiking activity of cerebellar interneurons in vitro and in vivo. J. Neurophysiol. 106, 1793-1805. doi: 10.1152/jn.00133.2011
19. Gandolfi, D., Pozzi, P., Tognolina, M., Chirico, G., Mapelli, J., and D’Angelo, E. (2014). The spatiotemporal organization of cerebellar network activity resolved by two-photon imaging of multiple single neurons. Front. Cell. Neurosci. 8:92. doi: 10.3389/fncel.2014.00092
20. Gao, W., Chen, G., Reinert, K. C., and Ebner, T. J. (2006). Cerebellar cortical molecular layer inhibition is organized in parasagittal zones. J. Neurosci. 26, 8377-8387. doi: 10.1523/jneurosci.2434-06.2006
21. Glykys, J., Dzhala, V., Egawa, K., Balena, T., Saponjian, Y., Kuchibhotla, K. V., et al. (2014). Local impermeant anions establish the neuronal chloride concentration. Science 343, 670-675. doi: 10.1126/science.1245423
22. Heiney, S. A., Kim, J., Augustine, G. J., and Medina, J. F. (2014). Precise control of movement kinematics by optogenetic inhibition of Purkinje cell activity. J. Neurosci. 34, 2321-2330. doi: 10.1523/jneurosci.4547-13.2014
23. Hippenmeyer, S., Vrieseling, E., Sigrist, M., Portmann, T., Laengle, C., Ladle, D. R., et al. (2005). A developmental switch in the response of DRG neurons to ETS transcription factor signaling. PLoS Biol. 3:e159. doi: 10.1371/journal.pbio.0030159
24. Jackson, M. B., and Zhang, S. J. (1995). Action potential propagation and propagation block by GABA in rat posterior pituitary nerve terminals. J. Physiol. 483(Pt. 3), 597-611. doi: 10.1113/jphysiol.1995.sp020609
25. Jörntell, H., Bengtsson, F., Schonewille, M., and De Zeeuw, C. I. (2010). Cerebellar molecular layer interneurons - computational properties and roles in learning. Trends Neurosci. 33, 524-532. doi: 10.1016/j.tins.2010.08.004
26. Junek, S., Chen, T.-W., Alevra, M., and Schild, D. (2009). Activity correlation imaging: visualizing function and structure of neuronal populations. Biophys. J. 96, 3801-3809. doi: 10.1016/j.bpj.2008.12.3962
27. Kim, J., Lee, S., Tsuda, S., Zhang, X., Asrican, B., Gloss, B., et al. (2014). Optogenetic mapping of cerebellar inhibitory circuitry reveals spatially biased coordination of interneurons via electrical synapses. Cell Rep. 7, 1601-1613. doi: 10.1016/j.celrep.2014.04.047
28. Kuhn, B., Ozden, I., Lampi, Y., Hasan, M. T., and Wang, S.S.-H. (2012). An amplified promoter system for targeted expression of calcium indicator proteins in the cerebellar cortex. Front. Neural Circuits 6:49. doi: 10.3389/fncir.2012.00049
29. Lee, S., Yoon, B.-E., Berglund, K., Oh, S.-J., Park, H., Shin, H.-S., et al. (2010). Channel-mediated tonic GABA release from glia. Science 330, 790-796. doi: 10.1126/science.1184334
30. Mapelli, J., Gandolfi, D., and D’Angelo, E. (2010). High-pass filtering and dynamic gain regulation enhance vertical bursts transmission along the mossy fiber pathway of cerebellum. Front. Cell. Neurosci. 4:14. doi: 10.3389/fncel.2010.00014
31. Mapelli, L., Solinas, S., and D’Angelo, E. (2014). Integration and regulation of glomerular inhibition in the cerebellar granular layer circuit. Front. Cell. Neurosci. 8:55. doi: 10.3389/fncel.2014.00055
32. Nicholson, C., and Phillips, J. M. (1981). Ion diffusion modified by tortuosity and volume fraction in the extracellular microenvironment of the rat cerebellum. J. Physiol. 321, 225-257. doi: 10.1113/jphysiol.1981.sp013981
33. Ozden, I., Dombeck, D. A., Hoogland, T. M., Tank, D. W., and Wang, S.S.-H. (2012). Widespread state-dependent shifts in cerebellar activity in locomoting mice. PLoS One 7:e42650. doi: 10.1371/journal.pone.0042650
34. Price, G. D., and Trussell, L. O. (2006). Estimate of the chloride concentration in a central glutamatergic terminal: a gramicidin perforated-patch study on the calyx of Held. J. Neurosci. 26, 11432-11436. doi: 10.1523/jneurosci.1660-06.2006
35. Pugh, J. R., and Jahr, C. E. (2011). Axonal GABAA receptors increase cerebellar granule cell excitability and synaptic activity. J. Neurosci. 31, 565-574. doi: 10.1523/jneurosci.4506-10.2011
36. Pugh, J. R., and Jahr, C. E. (2013). Activation of axonal receptors by GABA spillover increases somatic firing. J. Neurosci. 33, 16924-16929. doi: 10.1523/jneurosci.2796-13.2013
37. Rice, M. E., Okada, Y. C., and Nicholson, C. (1993). Anisotropic and heterogeneous diffusion in the turtle cerebellum: implications for volume transmission. J. Neurophysiol. 70, 2035-2044.
38. Rieubland, S., Roth, A., and Häusser, M. (2014). Structured connectivity in cerebellar inhibitory networks. Neuron 81, 913-929. doi: 10.1016/j.neuron.2013.12.029
39. Rossi, D. J., and Hamann, M. (1998). Spillover-mediated transmission at inhibitory synapses promoted by high affinity alpha6 subunit GABA(A) receptors and glomerular geometry. Neuron 20, 783-795. doi: 10.1016/s0896-6273(00)81016-8
40. Santamaria, F., Tripp, P. G., and Bower, J. M. (2007). Feedforward inhibition controls the spread of granule cell-induced Purkinje cell activity in the cerebellar cortex. J. Neurophysiol. 97, 248-263. doi: 10.1152/jn.01098.2005
41. Seja, P., Schonewille, M., Spitzmaul, G., Badura, A., Klein, I., Rudhard, Y., et al. (2012). Raising cytosolic Cl- in cerebellar granule cells affects their excitability and vestibulo-ocular learning. EMBO J. 31, 1217-1230. doi: 10.1038/emboj.2011.488
42. Staley, K. J., Soldo, B. L., and Proctor, W. R. (1995). Ionic mechanisms of neuronal excitation by inhibitory GABAA receptors. Science 269, 977-981. doi: 10.1126/science.7638623
43. Stell, B. M. (2011). Biphasic action of axonal GABA-A receptors on presynaptic calcium influx. J. Neurophysiol. 105, 2931-2936. doi: 10.1152/jn.01125.2010
44. Stell, B. M., Rostaing, P., Triller, A., and Marty, A. (2007). Activation of presynaptic GABA(A) receptors induces glutamate release from parallel fiber synapses. J. Neurosci. 27, 9022-9031. doi: 10.1523/jneurosci.1954-07.2007
45. Szabadics, J., Varga, C., Molnár, G., Oláh, S., Barzó, P., and Tamás, G. (2006). Excitatory effect of GABAergic axo-axonic cells in cortical microcircuits. Science 311, 233-235. doi: 10.1126/science.1121325
46. Thompson, S. M., and Gähwiler, B. H. (1989). Activity-dependent disinhibition. I. Repetitive stimulation reduces IPSP driving force and conductance in the hippocampus in vitro. J. Neurophysiol. 61, 501-511.
47. Tian, L., Hires, S. A., Mao, T., Huber, D., Chiappe, M. E., Chalasani, S. H., et al. (2009). Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators. Nat. Methods 6, 875-881. doi: 10.1038/nmeth.1398
48. Trigo, F. F., Marty, A., and Stell, B. M. (2008). Axonal GABAA receptors. Eur. J. Neurosci. 28, 841-848. doi: 10.1111/j.1460-9568.2008.06404.x
49. Vinueza Veloz, M. F., Zhou, K., Bosman, L. W. J., Potters, J.-W., Negrello, M., Seepers, R. M., et al. (2014). Cerebellar control of gait and interlimb coordination. Brain Struct. Funct. doi: 10.1007/s00429-014-0870-1 [Epub ahead of print].
50. Wang, X., Chen, G., Gao, W., and Ebner, T. J. (2011). Parasagittally aligned, mGluR1-dependent patches are evoked at long latencies by parallel fiber stimulation in the mouse cerebellar cortex in vivo. J. Neurophysiol. 105, 1732-1746. doi: 10.1152/jn.00717.2010
51. Wulff, P., Schonewille, M., Renzi, M., Viltono, L., Sassoè-Pognetto, M., Badura, A., et al. (2009). Synaptic inhibition of Purkinje cells mediates consolidation of vestibulo-cerebellar motor learning. Nat. Neurosci. 12, 1042-1049. doi: 10.1038/nn.2348
52. Zhao, S., Ting, J. T., Atallah, H. E., Qiu, L., Tan, J., Gloss, B., et al. (2011). Cell type-specific channelrhodopsin-2 transgenic mice for optogenetic dissection of neural circuitry function. Nat. Methods 8, 745-752. doi: 10.1038/nmeth.1668