Precise control of movement kinematics by optogenetic inhibition of Purkinje cell activity

Journal of Neuroscience

Volumn 34, Issue 6, 2014, Pages 2321-2330

  Heiney, Shane A ^a   Kim, Jinsook ^b   Augustine, George J ^b,c,d   Medina, Javier F ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

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

^d INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

Author keywords

Basket cells; Disinhibition; Eyeblink; Forward model; Inverse model; Molecular layer interneurons

Indexed keywords

MELOXICAM;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CEREBELLUM CORTEX; CONTROLLED STUDY; ELECTROSTIMULATION; EYELID REFLEX; FEMALE; HISTOLOGY; KINEMATICS; MALE; MOUSE; MOVEMENT (PHYSIOLOGY); NONHUMAN; OPTOGENETICS; PHOTOSTIMULATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PURKINJE CELL; SPIKE;

BASKET CELLS; DISINHIBITION; EYEBLINK; FORWARD MODEL; INVERSE MODEL; MOLECULAR LAYER INTERNEURONS;

ANIMALS; BIOMECHANICAL PHENOMENA; ELECTRIC STIMULATION; FEMALE; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MOVEMENT; NEURAL INHIBITION; OPTOGENETICS; PHOTIC STIMULATION; PURKINJE CELLS;

EID: 84893474439     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4547-13.2014     Document Type: Article

References (67)

1. Aksenov D, Serdyukova N, Irwin K, Bracha V (2004) GABA neurotransmission in the cerebellar interposed nuclei: involvement in classically conditioned eyeblinks and neuronal activity. J Neurophysiol 91: 719-727. CrossRef Medline
2. Albus J (1971) A theory of cerebellar function. Math Biosci 10: 25-61. CrossRef
3. Alviña K, Walter JT, Kohn A, Ellis-Davies G, Khodakhah K (2008) Questioning the role of rebound firing in the cerebellum. Nat Neurosci 11: 1256-1258. CrossRef Medline
4. Antal M, Sholomenko GN, Moschovakis AK, Storm-Mathisen J, Heizmann CW, Hunziker W (1992) The termination pattern and postsynaptic targets of rubrospinal fibers in the rat spinal cord: a light and electron microscopic study. J Comp Neurol 325: 22-37. CrossRef Medline
5. Asrican B, Augustine GJ, Berglund K, Chen S, Chow N, Deisseroth K, Feng G, Gloss B, Hira R, Hoffmann C, Kasai H, Katarya M, Kim J, Kudolo J, Lee LM, Lo SQ, Mancuso J, Matsuzaki M, Nakajima R, Qiu L, et al. (2013) Next-generation transgenic mice for optogenetic analysis of neural circuits. Front Neural Circuits 7: 160. CrossRef Medline
6. Bastian AJ, Martin TA, Keating JG, Thach WT (1996) Cerebellar ataxia: abnormal control of interaction torques across multiple joints. J Neurophysiol 76: 492-509. Medline
7. Blenkinsop TA, Lang EJ (2011) Synaptic action of the olivocerebellar system on cerebellar nuclear spike activity. J Neurosci 31: 14708-14720. CrossRef Medline
8. Boele H-J, Koekkoek SK, De Zeeuw CI, Ruigrok TJ (2013) Axonal sprouting and formation of terminals in the adult cerebellum during associative motor learning. J Neurosci 33: 17897-17907. CrossRef Medline
9. Büttner-Ennever JA, Cohen B, Pause M, Fries W (1988) Raphe nucleus of the pons containing omnipause neurons of the oculomotor system in the monkey, and its homologue in man. J Comp Neurol 267: 307-321. CrossRef Medline
10. Campolattaro MM, Kashef A, Lee I, Freeman JH (2011) Neuronal correlates of cross-modal transfer in the cerebellum and pontine nuclei. J Neurosci 31: 4051-4062. CrossRef Medline
11. Cao Y, Maran SK, Dhamala M, Jaeger D, Heck DH (2012) Behavior-related pauses in simple-spike activity of mouse Purkinje cells are linked to spike rate modulation. J Neurosci 32: 8678-8685. CrossRef Medline
12. Chen FP, Evinger C (2006) Cerebellar modulation of trigeminal reflex blinks: interpositus neurons. J Neurosci 26: 10569-10576. CrossRef Medline
13. Chettih SN, McDougle SD, Ruffolo LI, Medina JF (2011) Adaptive timing of motor output in the mouse: the role of movement oscillations in eyelid conditioning. Front Integr Neurosci 5: 72. CrossRef Medline
14. Chevalier G, Deniau JM (1990) Disinhibition as a basic process in the expression of striatal functions. Trends Neurosci 13: 277-280. CrossRef Medline
15. De Zeeuw CI, Hoebeek FE, Bosman LW, Schonewille M, Witter L, Koekkoek SK (2011) Spatiotemporal firing patterns in the cerebellum. Nat Rev Neurosci 12: 327-344. CrossRef Medline
16. Dow RS, Moruzzi G (1958) The physiology and pathology of the cerebellum. Minneapolis: University of Minnesota.
17. Gao W, Chen G, Reinert KC, Ebner TJ (2006) Cerebellar cortical molecular layer inhibition is organized in parasagittal zones. J Neurosci 26: 8377-8387. CrossRef Medline
18. Garcia KS, Steele PM, Mauk MD (1999) Cerebellar cortex lesions prevent acquisition of conditioned eyelid responses. J Neurosci 19: 10940-10947. Medline
19. Gauck V, Jaeger D (2000) The control of rate and timing of spikes in the deep cerebellar nuclei by inhibition. J Neurosci 20: 3006-3016. Medline
20. Hellman KM, Mason P (2012) Opioids disrupt pro-nociceptive modulation mediated by raphe magnus. J Neurosci 32: 13668-13678. CrossRef Medline
21. Hesslow G (1994) Correspondence between climbing fibre input and motor output in eyeblink-related areas in cat cerebellar cortex. J Physiol 476: 229-244. Medline
22. Hoebeek FE, Witter L, Ruigrok TJ, De Zeeuw CI (2010) Differential olivocerebellar cortical control of rebound activity in the cerebellar nuclei. Proc Natl Acad Sci U S A 107: 8410-8415. CrossRef Medline
23. Holdefer RN, Miller LE (2009) Dynamic correspondence between Purkinje cell discharge and forelimb muscle activity during reaching. Brain Res 1295: 67-75. CrossRef Medline
24. Houk JC, Buckingham JT, Barto AG (1996) Models of the cerebellum and motor learning. Behav Brain Sci 19: 368-383. CrossRef
25. Ito M (1984) The cerebellum and neural control. San Diego: Raven.
26. Ito M (2001) Cerebellar long-term depression: characterization, signal transduction, and functional roles. Physiol Rev 81: 1143-1195. Medline
27. Ivry RB, Keele SW (1989) Timing functions of the cerebellum. J Cogn Neurosci 1: 136-152. CrossRef Medline
28. Jirenhed DA, Bengtsson F, Hesslow G (2007) Acquisition, extinction, and reacquisition of a cerebellar cortical memory trace. J Neurosci 27: 2493-2502. CrossRef Medline
29. Johnson MD, Hyngstrom AS, Manuel M, Heckman CJ (2012) Push-pull control of motor output. J Neurosci 32: 4592-4599. CrossRef Medline
30. Jörntell H, Bengtsson F, Schonewille M, De Zeeuw CI (2010) Cerebellar molecular layer interneurons-computational properties and roles in learning. Trends Neurosci 33: 524-532. CrossRef Medline
31. Koekkoek SK, Hulscher HC, Dortland BR, Hensbroek RA, Elgersma Y, Ruigrok TJ, De Zeeuw CI (2003) Cerebellar LTD and learningdependent timing of conditioned eyelid responses. Science 301: 1736-1739. CrossRef Medline
32. Kojima Y, Soetedjo R, Fuchs AF (2010) Changes in simple spike activity of some Purkinje cells in the oculomotor vermis during saccade adaptation are appropriate to participate in motor learning. J Neurosci 30: 3715-3727. CrossRef Medline
33. Korn H, Axelrad H (1980) Electrical inhibition of Purkinje cells in the cerebellum of the rat. Proc Natl Acad Sci U S A 77: 6244-6247. CrossRef Medline
34. Krause M, German PW, Taha SA, Fields HL (2010) A pause in nucleus accumbens neuron firing is required to initiate and maintain feeding. J Neurosci 30: 4746-4756. CrossRef Medline
35. Lev-Ram V, Mehta SB, Kleinfeld D, Tsien RY (2003) Reversing cerebellar long-term depression. Proc Natl Acad Sci U S A 100: 15989-15993. CrossRef Medline
36. Manni E, Petrosini L (2004) A century of cerebellar somatotopy: a debated representation. Nat Rev Neurosci 5: 241-249. CrossRef Medline
37. Manto M-U, Pandolfo M (2002) The cerebellum and its disorders. Cambridge: Cambridge UP.
38. Mauk MD, Ruiz BP (1992) Learning-dependent timing of Pavlovian eyelid responses: differential conditioning using multiple interstimulus intervals. Behav Neurosci 106: 666-681. CrossRef Medline
39. Mauk MD, Medina JF, Nores WL, Ohyama T (2000) Cerebellar function: coordination, learning or timing? Curr Biol 10: R522-5. CrossRef Medline
40. McCormick DA, Thompson RF (1984) Neuronal responses of the rabbit cerebellum during acquisition and performance of a classically conditioned nictitating membrane-eyelid response. J Neurosci 4: 2811-2822. Medline
41. Medina JF (2011) The multiple roles of Purkinje cells in sensori-motor calibration: to predict, teach and command. Curr Opin Neurobiol 21: 616-622. CrossRef Medline
42. Medina JF, Lisberger SG (2009) Encoding and decoding of learned smoothpursuit eye movements in the floccular complex of the monkey cerebellum. J Neurophysiol 102: 2039-2054. CrossRef Medline
43. Medina JF, Mauk MD (2000) Computer simulation of cerebellar information processing. Nat Neurosci 3: 1205-1211. CrossRef Medline
44. Medina JF, Nores WL, Ohyama T, Mauk MD (2000) Mechanisms of cerebellar learning suggested by eyelid conditioning. Curr Opin Neurobiol 10: 717-724. CrossRef Medline
45. Miall RC, Christensen LO, Cain O, Stanley J (2007) Disruption of state estimation in the human lateral cerebellum. PLoS Biol 5: e316. CrossRef Medline
46. Mittmann W, Häusser M (2007) Linking synaptic plasticity and spike output at excitatory and inhibitory synapses onto cerebellar Purkinje cells. J Neurosci 27: 5559-5570. CrossRef Medline
47. Mittmann W, Koch U, Häusser M (2005) Feed-forward inhibition shapes the spike output of cerebellar Purkinje cells. J Physiol 563: 369-378. CrossRef Medline
48. Mostofi A, Holtzman T, Grout AS, Yeo CH, Edgley SA (2010) Electrophysiological localization of eyeblink-related microzones in rabbit cerebellar cortex. J Neurosci 30: 8920-8934. CrossRef Medline
49. Noda H, Suzuki DA (1979) The role of the flocculus of the monkey in saccadic eye movements. J Physiol 294: 317-334. Medline
50. Ohyama T, Nores WL, Medina JF, Riusech FA, Mauk MD (2006) Learninginduced plasticity in deep cerebellar nucleus. J Neurosci 26: 12656-12663. CrossRef Medline
51. Otis TS, Mathews PJ, Lee KH, Maiz J (2012) How do climbing fibers teach? Front Neural Circuits 6: 1-3. CrossRef Medline
52. Park SM, Tara E, Khodakhah K (2012) Efficient generation of reciprocal signals by inhibition. J Neurophysiol 107: 2453-2462. CrossRef Medline
53. Pasalar S, Roitman AV, Durfee WK, Ebner TJ (2006) Force field effects on cerebellar Purkinje cell discharge with implications for internal models. Nat Neurosci 9: 1404-1411. CrossRef Medline
54. Perrett SP, Ruiz BP, Mauk MD (1993) Cerebellar cortex lesions disrupt learning-dependent timing of conditioned eyelid responses. J Neurosci 13: 1708-1718. Medline
55. Person AL, Raman IM (2012) Purkinje neuron synchrony elicits timelocked spiking in the cerebellar nuclei. Nature 481: 502-505. CrossRef Medline
56. Pugh JR, Raman IM (2006) Potentiation of mossy fiber EPSCs in the cerebellar nuclei by NMDA receptor activation followed by postinhibitory rebound current. Neuron 51: 113-123. CrossRef Medline
57. Roitman AV, Pasalar S, Johnson MT, Ebner TJ (2005) Position, direction of movement, and speed tuning of cerebellar Purkinje cells during circular manual tracking in monkey. J Neurosci 25: 9244-9257. CrossRef Medline
58. Shidara M, Kawano K, Gomi H, Kawato M (1993) Inverse-dynamics model eye movement control by Purkinje cells in the cerebellum. Nature 365: 50-52. CrossRef Medline
59. Shin SL, De Schutter E (2006) Dynamic synchronization of Purkinje cell simple spikes. J Neurophysiol 96: 3485-3491. CrossRef Medline
60. Spencer RM, Zelaznik HN, Diedrichsen J, Ivry RB (2003) Disrupted timing of discontinuous but not continuous movements by cerebellar lesions. Science 300: 1437-1439. CrossRef Medline
61. Steuber V, Mittmann W, Hoebeek FE, Silver RA, De Zeeuw CI, Häusser M, De Schutter E (2007) Cerebellar LTD and pattern recognition by Purkinje cells. Neuron 54: 121-136. CrossRef Medline
62. Thach WT (1968) Discharge of Purkinje and cerebellar nuclear neurons during rapidly alternating arm movements in the monkey. J Neurophysiol 31: 785-797. Medline
63. Thach WT, Goodkin HP, Keating JG (1992) The cerebellum and the adaptive coordination of movement. Annu Rev Neurosci 15: 403-442. CrossRef Medline
64. Thier P, Dicke PW, Haas R, Barash S (2000) Encoding of movement time by populations of cerebellar Purkinje cells. Nature 405: 72-76. CrossRef Medline
65. Tsuda S, Kee MZ, Cunha C, Kim J, Yan P, Loew LM, Augustine GJ (2013) Probing the function of neuronal populations: combining micromirrorbased optogenetic photostimulation with voltage-sensitive dye imaging. Neurosci Res 75: 76-81. CrossRef Medline
66. Walter JT, Alviña K, Womack MD, Chevez C, Khodakhah K (2006) Decreases in the precision of Purkinje cell pacemaking cause cerebellar dysfunction and ataxia. Nat Neurosci 9: 389-397. CrossRef Medline
67. Witter L, Canto CB, Hoogland TM, de Gruijl JR, De Zeeuw CI (2013) Strength and timing of motor responses mediated by rebound firing in the cerebellar nuclei after Purkinje cell activation. Front Neural Circuits 7: 133. CrossRef Medline