Optogenetic Mapping of Cerebellar Inhibitory Circuitry Reveals Spatially Biased Coordination of Interneurons via Electrical Synapses

Cell Reports

Volumn 7, Issue 5, 2014, Pages 1601-1613

  Kim, Jinsook ^a,b,c,d,e   Lee, Soojung ^b,c,f,g   Tsuda, Sachiko ^a,b,c,d,e   Zhang, Xuying ^h   Asrican, Brent ^h   Gloss, Bernd ^h   Feng, Guoping ^h,i   Augustine, George J ^{a,b,c,d,e,f,j}  

^a NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^b DUKE NUS MEDICAL SCHOOL   (Singapore)

^c AGENCY FOR SCIENCE   (Singapore)

^d INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

^e MARINE BIOLOGICAL LABORATORY   (United States)

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

^g Kyung Hee University   (South Korea)

^h DUKE UNIVERSITY MEDICAL CENTER   (United States)

ⁱ MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^j NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

more..

Author keywords

[No Author keywords available]

Indexed keywords

RHODOPSIN; CHANNELRHODOPSIN 2, MOUSE; RHODOPSIN 2; UNCLASSIFIED DRUG;

ADULT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CEREBELLUM CORTEX; CONTROLLED STUDY; ELECTRICAL SYNAPSE; EVOKED RESPONSE; GAP JUNCTION; GENE MAPPING; INHIBITORY POSTSYNAPTIC POTENTIAL; INTERNEURON; MOUSE; NONHUMAN; OPTOGENETICS; PHOTOSTIMULATION; PRIORITY JOURNAL; PURKINJE CELL; SYNAPTIC TRANSMISSION; ANIMAL; BRAIN MAPPING; GENETICS; METABOLISM; PHYSIOLOGY; BRAIN REGION; CELL COUNT; CELLULAR DISTRIBUTION; CEREBELLUM; NERVE CELL NETWORK; NERVE CELL STIMULATION; POSTSYNAPTIC POTENTIAL; PROTEIN EXPRESSION;

ANIMALS; BRAIN MAPPING; ELECTRICAL SYNAPSES; INTERNEURONS; MICE; OPTOGENETICS; PURKINJE CELLS; RHODOPSIN;

MUS MUSCULUS;

EID: 84902267189     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.04.047     Document Type: Article

References (46)

1. Alcami P., Marty A. Estimating functional connectivity in an electrically coupled interneuron network. Proc. Natl. Acad. Sci. USA 2013, 110:E4798-E4807.
2. Beierlein M., Gibson J.R., Connors B.W. A network of electrically coupled interneurons drives synchronized inhibition in neocortex. Nat. Neurosci. 2000, 3:904-910.
3. Bloomfield S.A., Völgyi B. The diverse functional roles and regulation of neuronal gap junctions in the retina. Nat. Rev. Neurosci. 2009, 10:495-506.
4. Bower J.M. Model-founded explorations of the roles of molecular layer inhibition in regulating purkinje cell responses in cerebellar cortex: more trouble for the beam hypothesis. Front. Cell. Neurosci. 2010, 4:1-16.
5. Callaway E.M., Katz L.C. Photostimulation using caged glutamate reveals functional circuitry in living brain slices. Proc. Natl. Acad. Sci. USA 1993, 90:7661-7665.
6. Cohen D., Yarom Y. Cerebellar on-beam and lateral inhibition: two functionally distinct circuits. J.Neurophysiol. 2000, 83:1932-1940.
7. Connors B.W., Long M.A. Electrical synapses in the mammalian brain. Annu. Rev. Neurosci. 2004, 27:393-418.
8. Cruikshank S.J., Hopperstad M., Younger M., Connors B.W., Spray D.C., Srinivas M. Potent block of Cx36 and Cx50 gap junction channels by mefloquine. Proc. Natl. Acad. Sci. USA 2004, 101:12364-12369.
9. Cruikshank S.J., Urabe H., Nurmikko A.V., Connors B.W. Pathway-specific feedforward circuits between thalamus and neocortex revealed by selective optical stimulation of axons. Neuron 2010, 65:230-245.
10. Dizon M.J., Khodakhah K. The role of interneurons in shaping Purkinje cell responses in the cerebellar cortex. J.Neurosci. 2011, 31:10463-10473.
11. Dunbar R.L., Chen G., Gao W., Reinert K.C., Feddersen R., Ebner T.J. Imaging parallel fiber and climbing fiber responses and their short-terminteractions in the mouse cerebellar cortex invivo. Neuroscience 2004, 126:213-227.
12. Eccles J.C., Ito M., Szentágothai J. The Cerebellum as a Neuronal Machine 1967, Springer, Heidelberg.
13. Galarreta M., Hestrin S. Electrical synapses between GABA-releasing interneurons. Nat. Rev. Neurosci. 2001, 2:425-433.
14. Gao W., Chen G., Reinert K.C., Ebner T.J. Cerebellar cortical molecular layer inhibition is organized in parasagittal zones. J.Neurosci. 2006, 26:8377-8387.
15. Hatton G.I. Synaptic modulation of neuronal coupling. Cell Biol. Int. 1998, 22:765-780.
16. Häusser M., Clark B.A. Tonic synaptic inhibition modulates neuronal output pattern and spatiotemporal synaptic integration. Neuron 1997, 19:665-678.
17. Heiney S.A., Kim J., Augustine G.J., Medina J.F. Precise control of movement kinematics by optogenetic inhibition of Purkinje cell activity. J.Neurosci. 2014, 34:2321-2330.
18. Helbig I., Sammler E., Eliava M., Bolshakov A.P., Rozov A., Bruzzone R., Monyer H., Hormuzdi S.G. Invivo evidence for the involvement of the carboxy terminal domain in assembling connexin 36 at the electrical synapse. Mol. Cell. Neurosci. 2010, 45:47-58.
19. Hormuzdi S.G., Filippov M.A., Mitropoulou G., Monyer H., Bruzzone R. Electrical synapses: a dynamic signaling system that shapes the activity of neuronal networks. Biochim. Biophys. Acta 2004, 1662:113-137.
20. King J.S., Chen Y.F., Bishop G.A. An analysis of HRP-filled basket cell axons in the cat's cerebellum. II. Axonal distribution. Anat. Embryol. (Berl.) 1993, 188:299-305.
21. Korbo L., Andersen B.B., Ladefoged O., Møller A. Total numbers of various cell types in rat cerebellar cortex estimated using an unbiased stereological method. Brain Res. 1993, 609:262-268.
22. Lee S., Yoon B.E., Berglund K., Oh S.J., Park H., Shin H.S., Augustine G.J., Lee C.J. Channel-mediated tonic GABA release from glia. Science 2010, 330:790-796.
23. Long M.A., Landisman C.E., Connors B.W. Small clusters of electrically coupled neurons generate synchronous rhythms in the thalamic reticular nucleus. J.Neurosci. 2004, 24:341-349.
24. Mann-Metzer P., Yarom Y. Electrotonic coupling interacts with intrinsic properties to generate synchronized activity in cerebellar networks of inhibitory interneurons. J.Neurosci. 1999, 19:3298-3306.
25. McCracken C.B., Roberts D.C. Neuronal gap junctions: expression, function, and implications for behavior. Int. Rev. Neurobiol. 2006, 73:125-151.
26. Medina J.F., Mauk M.D. Computer simulation of cerebellar information processing. Nat. Neurosci. 2000, 3(Suppl):1205-1211.
27. Mittmann W., Koch U., Häusser M. Feed-forward inhibition shapes the spike output of cerebellar Purkinje cells. J.Physiol. 2005, 563:369-378.
28. Palay S.L., Chan-Palay V. Cerebellar Cortex; Cytology and Organization 1974, Springer, Berlin.
29. Pan F., Mills S.L., Massey S.C. Screening of gap junction antagonists on dye coupling in the rabbit retina. Vis. Neurosci. 2007, 24:609-618.
30. Park S.M., Tara E., Khodakhah K. Efficient generation of reciprocal signals by inhibition. J.Neurophysiol. 2012, 107:2453-2462.
31. Petreanu L., Huber D., Sobczyk A., Svoboda K. Channelrhodopsin-2-assisted circuit mapping of long-range callosal projections. Nat. Neurosci. 2007, 10:663-668.
32. Pouzat C., Hestrin S. Developmental regulation of basket/stellate cell-Purkinje cell synapses in the cerebellum. J.Neurosci. 1997, 17:9104-9112.
33. Rela L., Szczupak L. Gap junctions: their importance for the dynamics of neural circuits. Mol. Neurobiol. 2004, 30:341-357.
34. Rickgauer J.P., Tank D.W. Two-photon excitation of channelrhodopsin-2 at saturation. Proc. Natl. Acad. Sci. USA 2009, 106:15025-15030.
35. Rieubland S., Roth A., Häusser M. Structured connectivity in cerebellar inhibitory networks. Neuron 2014, 81:913-929.
36. Santamaria F., Tripp P.G., Bower J.M. Feedforward inhibition controls the spread of granule cell-induced Purkinje cell activity in the cerebellar cortex. J.Neurophysiol. 2007, 97:248-263.
37. Schoenenberger P., Grunditz A., Rose T., Oertner T.G. Optimizing the spatial resolution of Channelrhodopsin-2 activation. Brain Cell Biol. 2008, 36:119-127.
38. Somogyi P., Hámori J. A quantitative electron microscopic study of the Purkinje cell axon initial segment. Neuroscience 1976, 1:361-365.
39. Sotelo C., Llinás R. Specialized membrane junctions between neurons in the vertebrate cerebellar cortex. J.Cell Biol. 1972, 53:271-289.
40. Sultan F., Bower J.M. Quantitative Golgi study of the rat cerebellar molecular layer interneurons using principal component analysis. J.Comp. Neurol. 1998, 393:353-373.
41. Tovar K.R., Maher B.J., Westbrook G.L. Direct actions of carbenoxolone on synaptic transmission and neuronal membrane properties. J.Neurophysiol. 2009, 102:974-978.
42. Vervaeke K., Lorincz A., Nusser Z., Silver R.A. Gap junctions compensate for sublinear dendritic integration in an inhibitory network. Science 2012, 335:1624-1628.
43. Vincent P., Marty A. Fluctuations of inhibitory postsynaptic currents in Purkinje cells from rat cerebellar slices. J.Physiol. 1996, 494:183-199.
44. Vincent P., Armstrong C.M., Marty A. Inhibitory synaptic currents in rat cerebellar Purkinje cells: modulation by postsynaptic depolarization. J.Physiol. 1992, 456:453-471.
45. Wang H., Peca J., Matsuzaki M., Matsuzaki K., Noguchi J., Qiu L., Wang D., Zhang F., Boyden E., Deisseroth K., et al. High-speed mapping of synaptic connectivity using photostimulation in Channelrhodopsin-2 transgenic mice. Proc. Natl. Acad. Sci. USA 2007, 104:8143-8148.
46. Zhao S., Ting J.T., Atallah H.E., Qiu L., Tan J., Gloss B., Augustine G.J., Deisseroth K., Luo M., Graybiel A.M., Feng G. Cell type-specific channelrhodopsin-2 transgenic mice for optogenetic dissection of neural circuitry function. Nat. Methods 2011, 8:745-752.