Neocortical networks entrain neuronal circuits in cerebellar cortex

Journal of Neuroscience

Volumn 29, Issue 33, 2009, Pages 10309-10320

  Roš, Hana ^a,b   Sachdev, Robert N S ^a   Yu, Yuguo ^a   Šestan, Nenad ^a   McCormick, David A ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR; CELL ACTIVATION; CEREBELLUM CORTEX; CONTROLLED STUDY; ELECTRIC POTENTIAL; GOLGI COMPLEX; GRANULE CELL; MALE; MOUSE; NEOCORTEX; NERVE CELL; NERVE CELL NETWORK; NERVE CONDUCTION; NONHUMAN; OSCILLATION; PRIORITY JOURNAL; PURKINJE CELL; RAT; SPIKE; STIMULUS;

ACTION POTENTIALS; ANIMALS; CEREBELLAR CORTEX; MALE; MICE; NEOCORTEX; NERVE NET; NEURONS; RATS; RATS, LONG-EVANS; RATS, SPRAGUE-DAWLEY;

EID: 69049085617     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2327-09.2009     Document Type: Article

References (102)

1. Aizenman CD, Linden DJ (1999) Regulation of the rebound depolarization and spontaneous firing patterns of deep nuclear neurons in slices of rat cerebellum. J Neurophysiol 82:1697-1709.
2. Albus J (1971) A theory of cerebellar function. Math Biosci 10:25-61.
3. Armstrong DM, Rawson JA (1979) Activity patterns of cerebellar cortical neurones and climbing fibre afferents in the awake cat. J Physiol 289:425-448.
4. Armstrong DM, Cogdell B, Harvey RJ (1979) Discharge patterns of Purkinje cells in cats anaesthetized with alpha-chloralose. J Physiol 291:351-366.
5. Ba AM, Guiou M, Pouratian N, Muthialu A, Rex DE, Cannestra AF, Chen JW, Toga AW (2002) Multiwavelength optical intrinsic signal imaging of cortical spreading depression. J Neurophysiol 88:2726-2735.
6. Baker SN, Pinches EM, Lemon RN (2003) Synchronization in monkey motor cortex during a precision grip task. II. Effect of oscillatory activity on corticospinal output. J Neurophysiol 89:1941-1953.
7. Barmack NH, Yakhnitsa V (2008) Functions of interneurons in mouse cerebellum. J Neurosci 28:1140-1152.
8. Bell CC, Grimm RJ (1969) Discharge properties of Purkinje cells recorded on single and double microelectrodes. J Neurophysiol 32:1044-1055.
9. Bengtsson F, Jörntell H (2007) Ketamine and xylazine depress sensory-evoked parallel fiber and climbing fiber responses. J Neurophysiol 98:1697-1705.
10. Bloedel JR, Roberts WJ (1971) Action of climbing fibers in cerebellar cortex of the cat. J Neurophysiol 34:17-31.
11. Bower JM, Beermann DH, Gibson JM, Shambes GM, Welker W (1981) Principles of organization of a cerebro-cerebellar circuit. Micromapping the projections from cerebral (SI) to cerebellar (granule cell layer) tactile areas of rats. Brain Behav Evol 18:1-18.
12. Brown IE, Bower JM (2002) The influence of somatosensory cortex on climbing fiber responses in the lateral hemispheres of the rat cerebellum after peripheral tactile stimulation. J Neurosci 22:6819-6829.
13. Buzsaki G (2006) Rhythms of the brain. New York: Oxford.
14. Chadderton P, Margrie TW, Häusser M (2004) Integration of quanta in cerebellar granule cells during sensory processing. Nature 428:856-860.
15. Chen G, Hanson CL, Ebner TJ (1996) Functional parasagittal compartments in the rat cerebellar cortex: an in vivo optical imaging study using neutral red. J Neurophysiol 76:4169-4174.
16. Contreras D, Steriade M (1995) Cellular basis of EEG slow rhythms: a study of dynamic corticothalamic relationships. J Neurosci 15:604-622.
17. Courtemanche R, 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.
18. Courtemanche R, Pellerin JP, Lamarre Y (2002) Local field potential oscillations in primate cerebellar cortex: modulation during active and passive expectancy. J Neurophysiol 88:771-782.
19. Cowan RL, Wilson CJ (1994) Spontaneous firing patterns and axonal projections of single corticostriatal neurons in the rat medial agranular cortex. J Neurophysiol 71:17-32.
20. Crochet S, Petersen CC (2006) Correlating whisker behavior with membrane potential in barrel cortex of awake mice. Nat Neurosci 9:608-610.
21. de Solages C, Szapiro G, Brunel N, Hakim V, Isope P, Buisseret P, Rousseau C, Barbour B, Léna C (2008) High-frequency organization and synchrony of activity in the Purkinje cell layer of the cerebellum. Neuron 58:775-788.
22. De Zeeuw CI, Simpson JI, Hoogenraad CC, Galjart N, Koekkoek SK, Ruigrok TJ (1998) Microcircuitry and function of the inferior olive. Trends Neurosci 21:391-400.
23. De Zeeuw CI, Hoebeek FE, SchonewilleM (2008) Causes and consequences of oscillations in the cerebellar cortex. Neuron 58:655-658.
24. Dieudonne S (1998) Submillisecond kinetics and low efficacy of parallel fibre-Golgi cell synaptic currents in the rat cerebellum. J Physiol 510:845-866.
25. Douglas RJ, Koch C, Mahowald M, Martin KA, Suarez HH (1995) Recurrent excitation in neocortical circuits. Science 269:981-985.
26. Dugué GP, Brunel N, Hakim V, Schwartz E, Chat M, Lévesque M, Courtemanche R, Léna C, Dieudonné S (2009) Electrical coupling mediates tunable low-frequency oscillations and resonance in the cerebellar Golgi cell network. Neuron 61:126-139.
27. Eccles JC, Llinás R, Sasaki K (1966a) The mossy fibre-granule cell relay of the cerebellum and its inhibitory control by Golgi cells. Exp Brain Res 1:82-101.
28. Eccles JC, Llinás R, Sasaki K (1966b) The excitatory synaptic action of climbing fibres on the Purkinje cells of the cerebellum. J Physiol 182:268-296.
29. Eccles JC, Llinás R, Sasaki K (1966c) The inhibitory interneurones within the cerebellar cortex. Exp Brain Res 1:1-16.
30. Eccles JC, Llinás R, Sasaki K (1966d) Parallel fibre stimulation and the responses induced thereby in the Purkinje cells of the cerebellum. Exp Brain Res 1:17-39.
31. Eccles JC, Ito M, Szentágothai J (1967) The cerebellum as a neuronal machine. New York: Springer.
32. Eccles JC, Faber DS, Murphy JT, Sabah NH, Taborikova H (1971) Afferent volleys in limb nerves influencing impulse discharges in cerebellar cortex. I. In mossy fibres and granule cells. Exp Brain Res 13:15-35.
33. Ferezou I, Bolea S, Petersen CC (2006) Visualizing the cortical representation of whisker touch: voltage-sensitive dye imaging in freely moving mice. Neuron 50:617-629.
34. Fernandez FR, Engbers JD, Turner RW (2007) Firing dynamics of cerebellar Purkinje cells. J Neurophysiol 98:278-294.
35. Grafstein B (1956) Mechanism of spreading cortical depression. J Neurophysiol 19:154-171.
36. Granit R, Phillips CG (1956) Excitatory and inhibitory processes acting upon individual Purkinje cells of the cerebellum in cats. J Physiol 133:520-547.
37. Haider B, Duque A, Hasenstaub AR, McCormick DA (2006) Neocortical network activity in vivo is generated through a dynamic balance of excitation and inhibition. J Neurosci 26:4535-4545.
38. Haider B, Duque A, Hasenstaub AR, Yu Y, McCormick DA (2007) Enhancement of visual responsiveness by spontaneous local network activity in vivo. J Neurophysiol 97:4186-4202.
39. Hámori J, Szentágothai J (1966) Identification under the electron microscope of climbing fibers and their synaptic contacts. Exp Brain Res 1:65-81.
40. Hartmann MJ, Bower JM (1998) Oscillatory activity in the cerebellar hemispheres of unrestrained rats. J Neurophysiol 80:1598-1604.
41. Hasenstaub A, Sachdev RN, McCormick DA (2007) State changes rapidly modulate cortical neuronal responsiveness. J Neurosci 27:9607-9622.
42. Haslinger R, Ulbert I, Moore CI, Brown EN, Devor A (2006) Analysis of LFP phase predicts sensory response of barrel cortex. J Neurophysiol 96:1658-1663.
43. Häusser M, Clark BA (1997) Tonic synaptic inhibition modulates neuronal output pattern and spatiotemporal synaptic integration. Neuron 19:665-678.
44. Hurlock EC, McMahon A, Joho RH (2008) Purkinje-cell-restricted restoration of Kv3.3 function restores complex spikes and rescues motor coordination in Kcnc3 mutants. J Neurosci 28:4640-4648.
45. Isope P, Barbour B (2002) Properties of unitary granule cell→Purkinje cell synapses in adult rat cerebellar slices. J Neurosci 22:9668-9678.
46. Ito M (1984) The cerebellum and neural control. New York: Raven.
47. Jaeger D (2003) No parallel fiber volleys in the cerebellar cortex: evidence from cross-correlation analysis between Purkinje cells in a computer model and in recordings from anesthetized rats. J Comput Neurosci 14:311-327.
48. Jaeger D, De Schutter E, Bower JM (1997) The role of synaptic and voltage-gated currents in the control of Purkinje cell spiking: a modeling study. J Neurosci 17:91-106.
49. Jörntell H, Ekerot CF (2002) Reciprocal bidirectional plasticity of parallel fiber receptive fields in cerebellar Purkinje cells and their afferent interneurons. Neuron 34:797-806.
50. Jörntell H, Ekerot CF (2006) Properties of somatosensory synaptic integration in cerebellar granule cells in vivo. J Neurosci 26:11786-11797.
51. Khaliq ZM, Gouwens NW, Raman IM (2003) The contribution of resurgent sodium current to high-frequency firing in Purkinje neurons: an experimental and modeling study. J Neurosci 23:4899-4912.
52. Leao AP (1944) Spreading depression of activity in the cerebral cortex. J Neurophysiol 7:359-390.
53. LeVay S, Gilbert CD (1976) Laminar patterns of geniculocortical projection in the cat. Brain Res 113:1-19.
54. Llinás R, Sugimori M (1980) Electrophysiological properties of in vitro Purkinje cell dendrites in mammalian cerebellar slices. J Physiol 305:197-213.
55. Llinás R, Nicholson C, Freeman JA, Hillman DE (1968) Dendritic spikes and their inhibition in alligator Purkinje cells. Science 160:1132-1135.
56. Loewenstein Y, Mahon S, Chadderton P, Kitamura K, Sompolinsky H, Yarom Y, Häusser M (2005) Bistability of cerebellar Purkinje cells modulated by sensory stimulation. Nat Neurosci 8:202-211.
57. Lu H, Hartmann MJ, Bower JM (2005) Correlations between Purkinje cell single-unit activity and simultaneously recorded field potentials in the immediately underlying granule cell layer. J Neurophysiol 94:1849-1860.
58. Maex R, De Schutter E (1998) Synchronization of golgi and granule cell firing in a detailed network model of the cerebellar granule cell layer. J Neurophysiol 80:2521-2537.
59. Magill PJ, Bolam JP, Bevan MD (2000) Relationship of activity in the subthalamic nucleus-globus pallidus network to cortical electroencephalogram. J Neurosci 20:820-833.
60. Marr D (1969) A theory of cerebellar cortex. J Physiol 202:437-470.
61. Marshall SP, Lang EJ (2004) Inferior olive oscillations gate transmission of motor cortical activity to the cerebellum. J Neurosci 24:11356-11367.
62. McKay BE, Engbers JD, Mehaffey WH, Gordon GR, Molineux ML, Bains JS, Turner RW (2007) Climbing fiber discharge regulates cerebellar functions by controlling the intrinsic characteristics of Purkinje cell output. J Neurophysiol 97:2590-2604.
63. Medina JF, Lisberger SG (2008) Links from complex spikes to local plasticity and motor learning in the cerebellum of awake-behaving monkeys. Nat Neurosci 11:1185-1192.
64. Mena-Segovia J, Sims HM, Magill PJ, Bolam JP (2008) Cholinergic brainstem neurons modulate cortical gamma activity during slow oscillations. J Physiol 586:2947-2960.
65. Middleton SJ, Racca C, Cunningham MO, Traub RD, Monyer H, Knöpfel T, Schofield IS, Jenkins A, Whittington MA (2008) High-frequency network oscillations in cerebellar cortex. Neuron 58:763-774.
66. Morissette J, Bower JM (1996) Contribution of somatosensory cortex to responses in the rat cerebellar granule cell layer following peripheral tactile stimulation. Exp Brain Res 109:240-250.
67. Napper RM, Harvey RJ (1988) Number of parallel fiber synapses on an individual Purkinje cell in the cerebellum of the rat. J Comp Neurol 274:168-177.
68. O'Connor SM, Berg RW, Kleinfeld D (2002) Coherent electrical activity between vibrissa sensory areas of cerebellum and neocortex is enhanced during free whisking. J Neurophysiol 87:2137-2148.
69. Palay SL, Chan-Palay VC (1974) Cerebellar cortex: cytology and organization. New York: Springer.
70. Palkovits M, Magyar P, Szentágothai J (1972) Quantitative histological analysis of the cerebellar cortex in the cat. IV. Mossy fiber-Purkinje cell numerical transfer. Brain Res 45:15-29.
71. Paré D, Shink E, Gaudreau H, Destexhe A, Lang EJ (1998) Impact of spontaneous synaptic activity on the resting properties of cat neocortical pyramidal neurons in vivo. J Neurophysiol 79:1450-1460.
72. Pellerin JP, Lamarre Y (1997) Local field potential oscillations in primate cerebellar cortex during voluntary movement. J Neurophysiol 78:3502-3507.
73. Peters A, Payne BR (1993) Numerical relationships between geniculocortical afferents and pyramidal cell modules in cat primary visual cortex. Cereb Cortex 3:69-78.
74. Petersen CC, Hahn TT, Mehta M, Grinvald A, Sakmann B (2003) Interaction of sensory responses with spontaneous depolarization in layer 2/3 barrel cortex. Proc Natl Acad Sci U S A 100:13638-13643.
75. Pinault D (1996) A novel single-cell staining procedure performed in vivo under electrophysiological control: morpho-functional features of juxtacellularly labeled thalamic cells and other central neurons with biocytin or neurobiotin. J Neurosci Methods 65:113-136.
76. Provini L, Redman S, Strata P (1968) Mossy and climbing fibre organization on the anterior lobe of the cerebellum activated by forelimb and hindlimb areas of the sensorimotor cortex. Exp Brain Res 6:216-233.
77. Raman IM, Bean BP (1997) Resurgent sodium current and action potential formation in dissociated cerebellar Purkinje neurons. J Neurosci 17:4517-4526.
78. Ramon y Cajal S (1904) Textura del sistema nervioso del hombre y los vertebrados. Madrid: Moya.
79. Rancz EA, Ishikawa T, Duguid I, Chadderton P, Mahon S, Häusser M (2007) High-fidelity transmission of sensory information by single cerebellar mossy fibre boutons. Nature 450:1245-1248.
80. Sachdev RN, Sellien H, Ebner FF (2000) Direct inhibition evoked by whisker stimulation in somatic sensory (SI) barrel field cortex of the awake rat. J Neurophysiol 84:1497-1504.
81. Sachdev RN, Ebner FF, Wilson CJ (2004) Effect of subthreshold up and down states on the whisker-evoked response in somatosensory cortex. J Neurophysiol 92:3511-3521.
82. Sanchez-Vives MV, McCormick DA (2000) Cellular and network mechanisms of rhythmic recurrent activity in neocortex. Nat Neurosci 3:1027-1034.
83. Santamaria F, Tripp PG, Bower JM (2007) Feedforward inhibition controls the spread of granule cell-induced Purkinje cell activity in the cerebellar cortex. J Neurophysiol 97:248-263.
84. Schonewille M, Khosrovani S, Winkelman BH, Hoebeek FE, De Jeu MT, Larsen IM, Van der Burg J, Schmolesky MT, Frens MA, De Zeeuw CI (2006) Purkinje cells in awake behaving animals operate at the upstate membrane potential. Nat Neurosci 9:459-461; author reply 461.
85. Shambes GM, Gibson JM, Welker W (1978) Fractured somatotopy in granule cell tactile areas of rat cerebellar hemispheres revealed by micromapping. Brain Behav Evol 15:94-140.
86. Shu Y, Hasenstaub A, McCormick DA (2003) Turning on and off recurrent balanced cortical activity. Nature 423:288-293.
87. Simpson JI, Hulscher HC, Sabel-Goedknegt E, Ruigrok TJ (2005) Between in and out: linking morphology and physiology of cerebellar cortical interneurons. Prog Brain Res 148:329-340.
88. Soteropoulos DS, Baker SN (2006) Cortico-cerebellar coherence during a precision grip task in the monkey. J Neurophysiol 95:1194-1206.
89. Steriade M, Contreras D, Curró Dossi R, Nuñez A (1993a) The slow (<1 Hz) oscillation in reticular thalamic and thalamocortical neurons: scenario of sleep rhythm generation in interacting thalamic and neocortical networks. J Neurosci 13:3284-3299.
90. Steriade M, Nuñez A, Amzica F (1993b) Intracellular analysis of relations between the slow (<1 Hz) neocortical oscillation and other sleep rhythms of the electroencephalogram. J Neurosci 13:3266-3283.
91. Steriade M, Nuñez A, Amzica F (1993c) A novel slow (<1 Hz) oscillation of neocortical neurons in vivo: depolarizing and hyperpolarizing components. J Neurosci 13:3252-3265.
92. Steriade M, Timofeev I, Grenier F (2001) Natural waking and sleep states: a view from inside neocortical neurons. J Neurophysiol 85:1969-1985.
93. Stern EA, Kincaid AE, Wilson CJ (1997) Spontaneous subthreshold membrane potential fluctuations and action potential variability of rat corticostriatal and striatal neurons in vivo. J Neurophysiol 77:1697-1715.
94. Thach WT Jr (1967) Somatosensory receptive fields of single units in cat cerebellar cortex. J Neurophysiol 30:675-696.
95. Timofeev I, Steriade M (1996) Low-frequency rhythms in the thalamus of intact-cortex and decorticated cats. J Neurophysiol 76:4152-4168.
96. Timofeev I, Contreras D, Steriade M (1996) Synaptic responsiveness of cortical and thalamic neurones during various phases of slow sleep oscillation in cat. J Physiol 494:265-278.
97. Timofeev I, Grenier F, Steriade M (2001) Disfacilitation and active inhibition in the neocortex during the natural sleep-wake cycle: an intracellular study. Proc Natl Acad Sci U S A 98:1924-1929.
98. Walsh JV, Houk JC, Mugnaini E (1974) Identification of unitary potentials in turtle cerebellum and correlations with structures in granular layer. J Neurophysiol 37:30-47.
99. Wilson CJ, Kawaguchi Y (1996) The origins of two-state spontaneous membrane potential fluctuations of neostriatal spiny neurons. J Neurosci 16:2397-2410.
100. Wilson CJ, Sachdev RN (2004) Intracellular and juxtacellular staining with biocytin. Curr Protoc Neurosci Chapter 1:Unit 1.12.
101. Witham CL, Baker SN (2007) Network oscillations and intrinsic spiking rhythmicity do not co-vary in monkey sensorimotor areas. J Physiol 580:801-814.
102. Yartsev MM, Givon-Mayo R, Maller M, Donchin O (2009) Pausing Purkinje cells in the cerebellum of the awake cat. Front Syst Neurosci 3:2.