Diurnal influences on electrophysiological oscillations and coupling in the dorsal striatum and Cerebellar cortex of the anesthetized rat

Frontiers in Systems Neuroscience

Volumn 8, Issue , 2014, Pages

  Frederick, Ariana ^a,b   Bourget Murray, Jonathan ^a,c   Andrew Chapman, C ^a,b   Amir, Shimon ^a,b   Courtemanche, Richard ^a,b  

^a and Applied Physiology   (Canada)

^b Gina Cody School of Engineering and Computer Science   (Canada)

^c MCGILL UNIVERSITY   (Canada)

Author keywords

Circadian; Coherence; Dopamine; Local field potential oscillation; Urethane

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR CHANGE; CEREBELLUM CORTEX; CIRCADIAN RHYTHM; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINE METABOLISM; ELECTRIC POTENTIAL; ELECTROPHYSIOLOGICAL PROCEDURES; ELECTROPHYSIOLOGY; GENETIC TRANSCRIPTION; IN VIVO STUDY; LIGHT DARK CYCLE; MALE; NEOCORTEX; NONHUMAN; OSCILLATION; RAT;

EID: 84907291026     PISSN: 16625137     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnsys.2014.00145     Document Type: Article

References (104)

1. Ahissar, E., Haidarliu, S., and Zacksenhouse, M. (1997). Decoding temporally encoded sensory input by cortical oscillations and thalamic phase comparators. Proc. Natl. Acad. Sci. U S A 94, 11633-11638. doi: 10.1073/pnas.94.21.11633
2. Albrecht, U., Bordon, A., Schmutz, I., and Ripperger, J. (2007). The multiple facets of Per2. Cold Spring Harb. Symp. Quant. Biol. 72, 95-104. doi: 10.1101/sqb.2007.72.001
3. Allen, G. I., and Tsukahara, N. (1974). Cerebrocerebellar communication systems. Physiol. Rev. 54, 957-1006.
4. Ballion, B., Frenois, F., Zold, C. L., Chetrit, J., Murer, M. G., and Gonon, F. (2009). D2 receptor stimulation, but not D1, restores striatal equilibrium in a rat model of Parkinsonism. Neurobiol. Dis. 35, 376-384. doi: 10.1016/j.nbd.2009.05.019
5. Baar, E., Baar-Eroglu, C., Karaka, S., and Schürmann, M. (2001). Gamma, alpha, delta and theta oscillations govern cognitive processes. Int. J. Psychophysiol. 39, 241-248. doi: 10.1016/s0167-8760(00)00145-8
6. Berke, J. D., Okatan, M., Skurski, J., and Eichenbaum, H. B. (2004). Oscillatory entrainment of striatal neurons in freely moving rats. Neuron 43, 883-896. doi: 10.1016/j.neuron.2004.08.035
7. Bostan, A. C., Dum, R. P., and Strick, P. L. (2010). The basal ganglia communicate with the cerebellum. Proc. Natl. Acad. Sci. U S A 107, 8452-8456. doi: 10.1073/pnas.1000496107
8. Bostan, A. C., and Strick, P. L. (2010). The cerebellum and basal ganglia are interconnected. Neuropsychol. Rev. 20, 261-270. doi: 10.1007/s11065-010-9143-9
9. Bouthenet, M. L., Martres, M. P., Sales, N., and Schwartz, J. C. (1987). A detailed mapping of dopamine D-2 receptors in rat central nervous system by autoradiography with [125I]iodosulpride. Neuroscience 20, 117-155. doi: 10.1016/0306-4522(87)90008-x
10. Brown, P., Oliviero, A., Mazzone, P., Insola, A., Tonali, P., and Di Lazzaro, V. (2001). Dopamine dependency of oscillations between subthalamic nucleus and pallidum in Parkinson’s disease. J. Neurosci. 21, 1033-1038.
11. Bruguerolle, B., and Simon, N. (2002). Biologic rhythms and Parkinson’s disease: a chronopharmacologic approach to considering fluctuations in function. Clin. Neuropharmacol. 25, 194-201. doi: 10.1097/00002826-200207000-00002
12. Buehlmann, A., and Deco, G. (2010). Optimal information transfer in the cortex through synchronization. PLoS Comput. Biol. 6:e1000934. doi: 10.1371/journal.pcbi.1000934
13. Buzsáki, G. (2006). Rhythms of the Brain. New York: Oxford University Press.
14. Buzsáki, G., and Draguhn, A. (2004). Neuronal oscillations in cortical networks. Science 304, 1926-1929. doi: 10.1126/science.1099745
15. Buzsáki, G., and Moser, E. I. (2013). Memory, navigation and theta rhythm in the hippocampal-entorhinal system. Nat. Neurosci. 16, 130-138. doi: 10.1038/nn.3304
16. Calderon, D. P., Fremont, R., Kraenzlin, F., and Khodakhah, K. (2011). The neural substrates of rapid-onset Dystonia-Parkinsonism. Nat. Neurosci. 14, 357-365. doi: 10.1038/nn.2753
17. Chaudhury, D., Wang, L. M., and Colwell, C. S. (2005). Circadian regulation of hippocampal long-term potentiation. J. Biol. Rhythms 20, 225-236. doi: 10.1177/0748730405276352
18. Clement, E. A., Richard, A., Thwaites, M., Ailon, J., Peters, S., and Dickson, C. T. (2008). Cyclic and sleep-like spontaneous alternations of brain state under urethane anaesthesia. PLoS One 3:e2004. doi: 10.1371/journal.pone.0002004
19. Colwell, C. S. (2011). Linking neural activity and molecular oscillations in the SCN. Nat. Rev. Neurosci. 12, 553-569. doi: 10.1038/nrn3086
20. Costa, R. M., Lin, S. C., Sotnikova, T. D., Cyr, M., Gainetdinov, R. R., Caron, M. G., et al. (2006). Rapid alterations in corticostriatal ensemble coordination during acute dopamine-dependent motor dysfunction. Neuron 52, 359-369. doi: 10.1016/j.neuron.2006.07.030
21. Courtemanche, R., Chabaud, P., and Lamarre, Y. (2009). Synchronization in primate cerebellar granule cell layer local field potentials: basic anisotropy and dynamic changes during active expectancy. Front. Cell. Neurosci. 3:6. doi: 10.3389/neuro.03.006.2009
22. Courtemanche, R., Fujii, N., and Graybiel, A. M. (2003). Synchronous, focally modulated beta-band oscillations characterize local field potential activity in the striatum of awake behaving monkeys. J. Neurosci. 23, 11741-11752. doi: 10.3410/f.1002999.201447
23. Courtemanche, R., and Lamarre, Y. (2005). Local field potential oscillations in primate cerebellar cortex: synchronization with cerebral cortex during active and passive expectancy. J. Neurophysiol. 93, 2039-2052. doi: 10.1152/jn.00080.2004
24. Courtemanche, R., Pellerin, J. P., and Lamarre, Y. (2002). Local field potential oscillations in primate cerebellar cortex: modulation during active and passive expectancy. J. Neurophysiol. 88, 771-782. doi: 10.1152/jn.00718.2001
25. Courtemanche, R., Robinson, J. C., and Aponte, D. I. (2013). Linking oscillations in cerebellar circuits. Front. Neural Circuits 7:125. doi: 10.3389/fncir.2013.00125
26. Crittenden, J. R., and Graybiel, A. M. (2011). Basal ganglia disorders associated with imbalances in the striatal striosome and matrix compartments. Front. Neuroanat. 5:59. doi: 10.3389/fnana.2011.00059
27. Darna, M., Schmutz, I., Richter, K., Yelamanchili, S. V., Pendyala, G., Holtje, M., et al. (2009). Time of day-dependent sorting of the vesicular glutamate transporter to the plasma membrane. J. Biol. Chem. 284, 4300-4307. doi: 10.1074/jbc.m805480200
28. DeCoteau, W. E., Thorn, C., Gibson, D. J., Courtemanche, R., Mitra, P., Kubota, Y., et al. (2007a). Learning-related coordination of striatal and hippocampal theta rhythms during acquisition of a procedural maze task. Proc. Natl. Acad. Sci. U S A 104, 5644-5649. doi: 10.1073/pnas.0700818104
29. DeCoteau, W. E., Thorn, C., Gibson, D. J., Courtemanche, R., Mitra, P., Kubota, Y., et al. (2007b). Oscillations of local field potentials in the rat dorsal striatum during spontaneous and instructed behaviors. J. Neurophysiol. 97, 3800-3805. doi: 10.1152/jn.00108.2007
30. Dejean, C., Arbuthnott, G., Wickens, J. R., Le Moine, C., Boraud, T., and Hyland, B. I. (2011). Power fluctuations in beta and gamma frequencies in rat globus pallidus: association with specific phases of slow oscillations and differential modulation by dopamine D1 and D2 receptors. J. Neurosci. 31, 6098-6107. doi: 10.1523/JNEUROSCI.3311-09.2011
31. Delis, F., Mitsacos, A., and Giompres, P. (2004). Dopamine receptor and transporter levels are altered in the brain of Purkinje cell degeneration mutant mice. Neuroscience 125, 255-268. doi: 10.1016/j.neuroscience.2004.01.020
32. Destexhe, A., Contreras, D., and Steriade, M. (1999). Spatiotemporal analysis of local field potentials and unit discharges in cat cerebral cortex during natural wake and sleep states. J. Neurosci. 19, 4595-4608.
33. Doya, K. (2000). Complementary roles of basal ganglia and cerebellum in learning and motor control. Curr. Opin. Neurobiol. 10, 732-739. doi: 10.1016/s0959-4388(00)00153-7
34. Dugué, G. P., Brunel, N., Hakim, V., Schwartz, E. J., Chat, M., Lévesque, M., et al. (2009). Electrical coupling mediates tunable low-frequency oscillations and resonance in the cerebellar Golgi cell network. Neuron 61, 126-139. doi: 10.1016/j.neuron.2008.11.028
35. Ferris, M. J., Espana, R. A., Locke, J. L., Konstantopoulos, J. K., Rose, J. H., Chen, R., et al. (2014). Dopamine transporters govern diurnal variation in extracellular dopamine tone. Proc. Natl. Acad. Sci. U S A 111, E2751-E2759. doi: 10.1073/pnas.1407935111
36. Fowler, S. C., and Liou, J. R. (1998). Haloperidol, raclopride and eticlopride induce microcatalepsy during operant performance in rats, but clozapine and SCH 23390 do not. Psychopharmacology (Berl) 140, 81-90. doi: 10.1007/s002130050742
37. Frederick, A., Bourget-Murray, J., and Courtemanche, R. (2013). "Local field potential, synchrony of," in Encyclopedia of Computational Neuroscience: Springer Reference, eds D. Jaeger and R. Jung (Berlin Heidelberg: Springer-Verlag). Available online at: http://www.springerreference.com
38. Giompres, P., and Delis, F. (2005). Dopamine transporters in the cerebellum of mutant mice. Cerebellum 4, 105-111. doi: 10.1080/14734220510007851
39. Grasing, K., and Szeto, H. (1992). Diurnal variation in continuous measures of the rat EEG power spectra. Physiol. Behav. 51, 249-254. doi: 10.1016/0031-9384(92)90138-r
40. Gravotta, L., Gavrila, A. M., Hood, S., and Amir, S. (2011). Global depletion of dopamine using intracerebroventricular 6-hydroxydopamine injection disrupts normal circadian wheel-running patterns and PERIOD2 expression in the rat forebrain. J. Mol. Neurosci. 45, 162-171. doi: 10.1007/s12031-011-9520-8
41. Graybiel, A. M. (2008). Habits, rituals and the evaluative brain. Annu. Rev. Neurosci. 31, 359-387. doi: 10.1146/annurev.neuro.29.051605.112851
42. Graybiel, A. M. (2010). "Templates for neural dynamics in the striatum: striosomes and matrisomes," in Handbook of Brain Microcircuits, eds G. M. Shepherd and S. Grillner (New York, NY: Oxford University Press), 120-126.
43. Guilding, C., and Piggins, H. D. (2007). Challenging the omnipotence of the suprachiasmatic timekeeper: are circadian oscillators present throughout the mammalian brain? Eur. J. Neurosci. 25, 3195-3216. doi: 10.1111/j.1460-9568.2007.05581.x
44. Harbour, V. L., Weigl, Y., Robinson, B., and Amir, S. (2013). Comprehensive mapping of regional expression of the clock protein PERIOD2 in rat forebrain across the 24-h day. PLoS One 8:e76391. doi: 10.1371/journal.pone.0076391
45. Herrera-Meza, G., Aguirre-Manzo, L., Coria-Avila, G. A., Lopez-Meraz, M. L., Toledo-Cárdenas, R., Manzo, J., et al. (2014). Beyond the basal ganglia: cFOS expression in the cerebellum in response to acute and chronic dopaminergic alterations. Neuroscience 267, 219-231. doi: 10.1016/j.neuroscience.2014.02.046
46. Herzog, E. D. (2007). Neurons and networks in daily rhythms. Nat. Rev. Neurosci. 8, 790-802. doi: 10.1038/nrn2215
47. Hood, S., Cassidy, P., Cossette, M. P., Weigl, Y., Verwey, M., Robinson, B., et al. (2010). Endogenous dopamine regulates the rhythm of expression of the clock protein PER2 in the rat dorsal striatum via daily activation of D2 dopamine receptors. J. Neurosci. 30, 14046-14058. doi: 10.1523/JNEUROSCI.2128-10.2010
48. Hoshi, E., Tremblay, L., Feger, J., Carras, P. L., and Strick, P. L. (2005). The cerebellum communicates with the basal ganglia. Nat. Neurosci. 8, 1491-1493. doi: 10.1038/nn1544
49. Hurley, M. J., Mash, D. C., and Jenner, P. (2003). Markers for dopaminergic neurotransmission in the cerebellum in normal individuals and patients with Parkinson’s disease examined by RT-PCR. Eur. J. Neurosci. 18, 2668-2672. doi: 10.1046/j.1460-9568.2003.02963.x
50. Hutcheon, B., and Yarom, Y. (2000). Resonance, oscillation and the intrinsic frequency preferences of neurons. Trends Neurosci. 23, 216-222. doi: 10.1016/s0166-2236(00)01547-2
51. Ichinohe, N., Mori, F., and Shoumura, K. (2000). A di-synaptic projection from the lateral cerebellar nucleus to the laterodorsal part of the striatum via the central lateral nucleus of the thalamus in the rat. Brain Res. 880, 191-197. doi: 10.1016/s0006-8993(00)02744-x
52. Ikai, Y., Takada, M., Shinonaga, Y., and Mizuno, N. (1992). Dopaminergic and non-dopaminergic neurons in the ventral tegmental area of the rat project, respectively, to the cerebellar cortex and deep cerebellar nuclei. Neuroscience 51, 719-728. doi: 10.1016/0306-4522(92)90310-x
53. Imbesi, M., Yildiz, S., Dirim Arslan, A., Sharma, R., Manev, H., and Uz, T. (2009). Dopamine receptor-mediated regulation of neuronal "clock" gene expression. Neuroscience 158, 537-544. doi: 10.1016/j.neuroscience.2008.10.044
54. Ito, M. (2006). Cerebellar circuitry as a neuronal machine. Prog. Neurobiol. 78, 272-303. doi: 10.1016/j.pneurobio.2006.02.006
55. Kiss, B., Horti, F., and Bobok, A. (2011). In vitro and in vivo comparison of [3H](+)-PHNO and [3H]raclopride binding to rat striatum and lobes 9 and 10 of the cerebellum: a method to distinguish dopamine D(3) from D(2) receptor sites. Synapse 65, 467-478. doi: 10.1002/syn.20867
56. Koch, G., Brusa, L., Carrillo, F., Lo Gerfo, E., Torriero, S., Oliveri, M., et al. (2009). Cerebellar magnetic stimulation decreases levodopa-induced dyskinesias in Parkinson disease. Neurology 73, 113-119. doi: 10.1212/WNL.0b013e3181ad5387
57. Lemaire, N., Hernandez, L. F., Hu, D., Kubota, Y., Howe, M. W., and Graybiel, A. M. (2012). Effects of dopamine depletion on LFP oscillations in striatum are taskand learning-dependent and selectively reversed by L-DOPA. Proc. Natl. Acad. Sci. U S A 109, 18126-18131. doi: 10.1073/pnas.1216403109
58. Li, C. L., and Parker, L. O. (1969). Effect of dentate stimulation on neuronal activity in the globus pallidus. Exp. Neurol. 24, 298-309. doi: 10.1016/0014-4886(69)90023-5
59. Lim, C., and Allada, R. (2013). ATAXIN-2 activates PERIOD translation to sustain circadian rhythms in Drosophila. Science 340, 875-879. doi: 10.1126/science.1234785
60. Maggi, C. A., and Meli, A. (1986). Suitability of urethane anesthesia for physiopharmacological investigations in various systems. Part 1: general considerations. Experientia 42, 109-114. doi: 10.1007/bf01952426
61. Magill, P. J., Sharott, A., Bolam, J. P., and Brown, P. (2004). Brain state-dependency of coherent oscillatory activity in the cerebral cortex and basal ganglia of the rat. J. Neurophysiol. 92, 2122-2136. doi: 10.1152/jn.00333.2004
62. Mallet, N., Le Moine, C., Charpier, S., and Gonon, F. (2005). Feedforward inhibition of projection neurons by fast-spiking GABA interneurons in the rat striatum in vivo. J. Neurosci. 25, 3857-3869. doi: 10.1523/jneurosci.5027-04.2005
63. Masubuchi, S., Honma, S., Abe, H., Ishizaki, K., Namihira, M., Ikeda, M., et al. (2000). Clock genes outside the suprachiasmatic nucleus involved in manifestation of locomotor activity rhythm in rats. Eur. J. Neurosci. 12, 4206-4214. doi: 10.1111/j.1460-9568.2000.01313.x
64. Mayne, E. W., Craig, M. T., McBain, C. J., and Paulsen, O. (2013). Dopamine suppresses persistent network activity via D(1) -like dopamine receptors in rat medial entorhinal cortex. Eur. J. Neurosci. 37, 1242-1247. doi: 10.1111/ejn.12125
65. McCormick, D. A. (2004). "Membrane properties and neurotransmitter actions," in The Synaptic Organization of the Brain, ed G. M. Shepherd (New York, NY: Oxford University Press), 39-77.
66. Mendoza, J., Pevet, P., Felder-Schmittbuhl, M. P., Bailly, Y., and Challet, E. (2010). The cerebellum harbors a circadian oscillator involved in food anticipation. J. Neurosci. 30, 1894-1904. doi: 10.1523/JNEUROSCI.5855-09.2010
67. Middleton, F. A., and Strick, P. L. (2000). Basal ganglia and cerebellar loops: motor and cognitive circuits. Brain Res. Brain Res. Rev. 31, 236-250. doi: 10.1016/s0165-0173(99)00040-5
68. Moers-Hornikx, V. M., Vles, J. S., Tan, S. K., Cox, K., Hoogland, G., Steinbusch, W. M., et al. (2011). Cerebellar nuclei are activated by high-frequency stimulation of the subthalamic nucleus. Neurosci. Lett. 496, 111-115. doi: 10.1016/j.neulet.2011.03.094
69. Monti, J. M., and Monti, D. (2007). The involvement of dopamine in the modulation of sleep and waking. Sleep Med. Rev. 11, 113-133. doi: 10.1016/j.smrv.2006.08.003
70. Mordel, J., Karnas, D., Pevet, P., Isope, P., Challet, E., and Meissl, H. (2013). The output signal of Purkinje cells of the cerebellum and circadian rhythmicity. PLoS One 8:e58457. doi: 10.1371/journal.pone.0058457
71. Morissette, J., and Bower, J. M. (1996). Contribution of somatosensory cortex to responses in the rat cerebellar granule cell layer following peripheral tactile stimulation. Exp. Brain Res. 109, 240-250. doi: 10.1007/bf00231784
72. Namihira, M., Honma, S., Abe, H., Tanahashi, Y., Ikeda, M., and Honma, K. (1999). Daily variation and light responsiveness of mammalian clock gene, Clock and BMAL1, transcripts in the pineal body and different areas of brain in rats. Neurosci. Lett. 267, 69-72. doi: 10.1016/s0304-3940(99)00324-9
73. Nicolelis, M. A. L., Baccala, L. A., Lin, R. C. S., and Chapin, J. K. (1995). Sensorimotor encoding by synchronous neural ensemble activity at multiple levels of the somatosensory system. Science 268, 1353-1358. doi: 10.1126/science.7761855
74. Nutt, J. G., Carter, J. H., Lea, E. S., and Woodward, W. R. (1997). Motor fluctuations during continuous levodopa infusions in patients with Parkinson’s disease. Mov. Disord. 12, 285-292. doi: 10.1002/mds.870120304
75. Owasoyo, J. O., Walker, C. A., and Whitworth, U. G. (1979). Diurnal variation in the dopamine level of rat brain areas: effect of sodium phenobarbital. Life Sci. 25, 119-122. doi: 10.1016/0024-3205(79)90382-5
76. Paxinos, G., and Watson, C. (1998). The Rat Brain in Stereotaxic Coordinates. SanDiego, CA: Academic Press.
77. Pellerin, J. P., and Lamarre, Y. (1997). Local field potential oscillations in primate cerebellar cortex during voluntary movement. J. Neurophysiol. 78, 3502-3507.
78. Ratcheson, R. A., and Li, C. L. (1969). Effect of dentate stimulation on neuronal activity in the caudate nucleus. Exp. Neurol. 25, 268-281. doi: 10.1016/0014-4886(69)90050-8
79. Rath, M. F., Rohde, K., and Moller, M. (2012). Circadian oscillations of molecular clock components in the cerebellar cortex of the rat. Chronobiol. Int. 29, 1289-1299. doi: 10.3109/07420528.2012.728660
80. Rivlin-Etzion, M., Marmor, O., Heimer, G., Raz, A., Nini, A., and Bergman, H. (2006). Basal ganglia oscillations and pathophysiology of movement disorders. Curr. Opin. Neurobiol. 16, 629-637. doi: 10.1016/j.conb.2006.10.002
81. Roopun, A. K., Lebeau, F. E., Rammell, J., Cunningham, M. O., Traub, R. D., and Whittington, M. A. (2010). Cholinergic neuromodulation controls directed temporal communication in neocortex in vitro. Front. Neural Circuits 4:8. doi: 10.3389/fncir.2010.00008
82. Ros, H., Sachdev, R. N., Yu, Y., Sestan, N., and McCormick, D. A. (2009). Neocortical networks entrain neuronal circuits in cerebellar cortex. J. Neurosci. 29, 10309-10320. doi: 10.1523/JNEUROSCI.2327-09.2009
83. Sanchez-Vives, M. V., and McCormick, D. A. (2000). Cellular and network mechanisms of rhythmic recurrent activity in neocortex. Nat. Neurosci. 3, 1027-1034. doi: 10.1038/79848
84. Schnitzler, A., and Gross, J. (2005). Normal and pathological oscillatory communication in the brain. Nat. Rev. Neurosci. 6, 285-296. doi: 10.1038/nrn1650
85. Schweighofer, N., Doya, K., and Kuroda, S. (2004). Cerebellar aminergic neuromodulation: towards a functional understanding. Brain Res. Brain Res. Rev. 44, 103-116. doi: 10.1016/j.brainresrev.2003.10.004
86. Sharma, A. V., Wolansky, T., and Dickson, C. T. (2010). A comparison of sleeplike slow oscillations in the hippocampus under ketamine and urethane anesthesia. J. Neurophysiol. 104, 932-939. doi: 10.1152/jn.01065.2009
87. Sharott, A., Doig, N. M., Mallet, N., and Magill, P. J. (2012). Relationships between the firing of identified striatal interneurons and spontaneous and driven cortical activities in vivo. J. Neurosci. 32, 13221-13236. doi: 10.1523/jneurosci.2440-12.2012
88. Sharott, A., Magill, P. J., Harnack, D., Kupsch, A., Meissner, W., and Brown, P. (2005). Dopamine depletion increases the power and coherence of betaoscillations in the cerebral cortex and subthalamic nucleus of the awake rat. Eur. J. Neurosci. 21, 1413-1422. doi: 10.1111/j.1460-9568.2005.03973.x
89. Shieh, K. R. (2003). Distribution of the rhythm-related genes rPERIOD1, rPE-RIOD2 and rCLOCK, in the rat brain. Neuroscience 118, 831-843. doi: 10.1016/s0306-4522(03)00004-6
90. Steriade, M. (2003). Neuronal Substrates of Sleep and Epilepsy. Cambridge, UK: Cambridge University Press.
91. Stern, E. A., Jaeger, D., and Wilson, C. J. (1998). Membrane potential synchrony of simultaneously recorded striatal spiny neurons in vivo. Nature 394, 475-478. doi: 10.1038/28848
92. Takada, M., Sugimoto, T., and Hattori, T. (1993). MPTP neurotoxicity to cerebellar Purkinje cells in mice. Neurosci. Lett. 150, 49-52. doi: 10.1016/0304-3940(93)90105-t
93. Thorn, C. A., Atallah, H., Howe, M., and Graybiel, A. M. (2010). Differential dynamics of activity changes in dorsolateral and dorsomedial striatal loops during learning. Neuron 66, 781-795. doi: 10.1016/j.neuron.2010.04.036
94. Thorn, C. A., and Graybiel, A. M. (2014). Differential entrainment and learningrelated dynamics of spike and local field potential activity in the sensorimotor and associative striatum. J. Neurosci. 34, 2845-2859. doi: 10.1523/jneurosci.1782-13.2014
95. Tseng, K. Y., Kasanetz, F., Kargieman, L., Riquelme, L. A., and Murer, M. G. (2001). Cortical slow oscillatory activity is reflected in the membrane potential and spike trains of striatal neurons in rats with chronic nigrostriatal lesions. J. Neurosci. 21, 6430-6439.
96. Uhlhaas, P. J., Roux, F., Rodriguez, E., Rotarska-Jagiela, A., and Singer, W. (2010). Neural synchrony and the development of cortical networks. Trends Cogn. Sci. 14, 72-80. doi: 10.1016/j.tics.2009.12.002
97. Valencia, M., Artieda, J., Bolam, J. P., and Mena-Segovia, J. (2013). Dynamic interaction of spindles and gamma activity during cortical slow oscillations and its modulation by subcortical afferents. PLoS One 8:e67540. doi: 10.1371/journal.pone.0067540
98. Verwey, M., and Amir, S. (2012). Variable restricted feeding disrupts the daily oscillations of Period2 expression in the limbic forebrain and dorsal striatum in rats. J. Mol. Neurosci. 46, 258-264. doi: 10.1007/s12031-011ds-9529-z
99. Walters, J. R., Hu, D., Itoga, C. A., Parr-Brownlie, L. C., and Bergstrom, D. A. (2007). Phase relationships support a role for coordinated activity in the indirect pathway in organizing slow oscillations in basal ganglia output after loss of dopamine. Neuroscience 144, 762-776. doi: 10.1016/j.neuroscience.2006.10.006
100. Watson, T. C., Becker, N., Apps, R., and Jones, M. W. (2014). Back to front: cerebellar connections and interactions with the prefrontal cortex. Front. Syst. Neurosci. 8:4. doi: 10.3389/fnsys.2014.00004
101. Wilder-Smith, E., Tan, E. K., Law, H. Y., Zhao, Y., Ng, I., and Wong, M. C. (2003). Spinocerebellar ataxia type 3 presenting as an L-DOPA responsive dystonia phenotype in a Chinese family. J. Neurol. Sci. 213, 25-28. doi: 10.1016/s0022-510x(03)00129-1
102. Wilson, C. J., and Kawaguchi, Y. (1996). The origins of two-state spontaneous membrane potential fluctuations of neostriatal spiny neurons. J. Neurosci. 16, 2397-2410.
103. Zeitzer, J. M. (2013). Control of sleep and wakefulness in health and disease. Prog. Mol. Biol. Transl. Sci. 119, 137-154. doi: 10.1016/B978-0-12-396971-2.00006-3
104. Zhang, Y., Ling, J., Yuan, C., Dubruille, R., and Emery, P. (2013). A role for Drosophila ATX2 in activation of PER translation and circadian behavior. Science 340, 879-882. doi: 10.1126/science.1234746