The roles of GABA B receptors in cortical network activity

Advances in Pharmacology

Volumn 58, Issue C, 2010, Pages 205-229

  Kohl, Michael M ^a   Paulsen, Ole ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Epilepsy; Inhibition; Network activity; Oscillations; Persistent activity

Indexed keywords

4 AMINOBUTYRIC ACID B RECEPTOR; AMPA RECEPTOR; KAINIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ARTICLE; BRAIN CORTEX; CORTICAL SYNCHRONIZATION; EPILEPSY; HIPPOCAMPUS; HUMAN; INHIBITORY POSTSYNAPTIC POTENTIAL; NEOCORTEX; NERVE CELL NETWORK; NEUROPATHOLOGY; NONHUMAN; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SCHIZOPHRENIA; SPIKE WAVE; THALAMUS; THETA RHYTHM; ANIMAL; METABOLISM; PATHOLOGY; REVIEW;

ANIMALS; CEREBRAL CORTEX; HIPPOCAMPUS; HUMANS; NERVE NET; RECEPTORS, GABA-B;

EID: 77955040003     PISSN: 10543589     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S1054-3589(10)58009-8     Document Type: Chapter

References (145)

1. Agnati L.F., Ferr S., Lluis C., Franco R., Fuxe K. Molecular mechanisms and therapeutical implications of intramembrane receptor/receptor interactions among heptahelical receptors with examples from the striatopallidal gaba neurons. Pharmacological Reviews 2003, 55:509-550.
2. Atencio C.A., Schreiner C.E. Spectrotemporal processing differences between auditory cortical fast-spiking and regular-spiking neurons. Journal of Neuroscience 2008, 28:3897-3910.
3. Bal T., von Krosigk M., McCormick D.A. Role of the ferret perigeniculate nucleus in the generation of synchronized oscillations in vitro. Journal of Physiology 1995, 483:665-685.
4. Bal T., von Krosigk M., McCormick D.A. Synaptic and membrane mechanisms underlying synchronized oscillations in the ferret lateral geniculate nucleus in vitro. Journal of Physiology 1995, 483:641-663.
5. B receptor trafficking. Journal of Biological Chemistry 2004, 279:18840-18850.
6. Bauer E.P., Paz R., Par D. Gamma oscillations coordinate amygdalo-rhinal interactions during learning. Journal of Neuroscience 2007, 27:9369-9379.
7. Bazhenov M., Timofeev I., Steriade M., Sejnowski T.J. Model of thalamocortical slow-wave sleep oscillations and transitions to activated states. Journal of Neuroscience 2002, 22:8691-8704.
8. Beierlein M., Gibson J.R., Connors B.W. Two dynamically distinct inhibitory networks in layer 4 of the neocortex. Journal of Neurophysiology 2003, 90:2987-3000.
9. Bland B.H. The physiology and pharmacology of hippocampal formation theta rhythms. Progress in Neurobiology 1986, 26:1-54.
10. Börgers C., Epstein S., Kopell N.J. Background gamma rhythmicity and attention in cortical local circuits: A computational study. Proceedings of the National Academy of Sciences of the United States of America 2005, 102:7002-7007.
11. B receptor pharmacology. Annual Review of Pharmacology and Toxicology 1993, 33:109-147.
12. Bowery N.G., Bettler B., Froestl W., Gallagher J.P., Marshall F., Raiteri M., et al. International Union of Pharmacology. XXXIII. Mammalian γ-aminobutyric acid(B) receptors: structure and function. Pharmacological Reviews 2002, 54:247-264.
13. Bowery N.G., Doble A., Hill D.R., Hudson A.L., Shaw J.S., Turnbull M.J., et al. Bicuculline-insensitive GABA receptors on peripheral autonomic nerve terminals. European Journal of Pharmacology 1981, 71:53-70.
14. Bowery N.G., Doble A., Hill D.R., Hudson A.L., Turnbull M.J., Warrington R. Structure/activity studies at a baclofen-sensitive, bicuculline-insensitive GABA receptor. Advances in Biochemical Psychopharmacology 1981, 29:333-341.
15. A receptors. Neuropharmacology 1982, 21:391-395.
16. B receptor binding sites on rat whole brain synaptic membranes. British Journal of Pharmacology 1983, 78:191-206.
17. Bowery N.G., Hill D.R., Hudson A.L., Doble A., Middlemiss D.N., Shaw J., et al. (-)Baclofen decreases neurotransmitter release in the mammalian CNS by an action at a novel GABA receptor. Nature 1980, 283:92-94.
18. Bragin A., Jand G., Nádasdy Z., Hetke J., Wise K., Buzsáki G. Gamma (40-100hz) oscillation in the hippocampus of the behaving rat. Journal of Neuroscience 1995, 15:47-60.
19. Brown J.T., Davies C.H., Randall A.D. Synaptic activation of GABA(b) receptors regulates neuronal network activity and entrainment. European Journal of Neuroscience 2007, 25:2982-2990.
20. K5 -containing receptors in kainate-driven hippocampal gamma band oscillations. Neuropharmacology 2006, 50:47-56.
21. Brunel N., Wang X.-J. What determines the frequency of fast network oscillations with irregular neural discharges? I. Synaptic dynamics and excitation-inhibition balance. Journal of Neurophysiology 2003, 90:415-430.
22. Buhl E.H., Halasy K., Somogyi P. Diverse sources of hippocampal unitary inhibitory postsynaptic potentials and the number of synaptic release sites. Nature 1994, 368:823-828.
23. Buhl E.H., Tamás G., Fisahn A. Cholinergic activation and tonic excitation induce persistent gamma oscillations in mouse somatosensory cortex in vitro. Journal of Physiology 1998, 513:117-126.
24. Buzsáki G. Theta oscillations in the hippocampus. Neuron 2002, 33:325-340.
25. Cardin J., Carlén M., Meletis K., Knoblich U., Zhang F., Deisseroth K., et al. Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature 2009, 459:663-667.
26. B antagonist CGP36742 enhances spatial learning performance and antagonises baclofen-induced amnesia in mice. British Journal of Pharmacology Supplementum 1993, 109:74.
27. Chrobak J.J., Buzsáki G. Gamma oscillations in the entorhinal cortex of the freely behaving rat. Journal of Neuroscience 1998, 18:388-398.
28. Compte A., Sanchez-Vives M.V., McCormick D.A., Wang X.-J. Cellular and network mechanisms of slow oscillatory activity (<1hz) and wave propagations in a cortical network model. Journal of Neurophysiology 2003, 89:2707-2725.
29. B receptor-mediated responses in neocortex of rat and cat. Journal of Physiology (Paris) 1988, 406:443-468.
30. Crunelli V., Hughes S.W. The slow (<1hz) rhythm of non-rem sleep: A dialogue between three cardinal oscillators. Nature Neuroscience 2010, 13:9-17.
31. B receptors in excitation and inhibition of thalamocortical cells. Trends in Neurosciences 1991, 14:16-21.
32. Crunelli V., Leresche N. Childhood absence epilepsy: genes, channels, neurons and networks. Nature Reviews Neuroscience 2002, 3:371-382.
33. Csicsvari J., Hirase H., Czurk A., Mamiya A., Buzsáki G. Oscillatory coupling of hippocampal pyramidal cells and interneurons in the behaving rat. Journal of Neuroscience 1999, 19:274-287.
34. Csicsvari J., Jamieson B., Wise K.D., Buzsáki G. Mechanisms of gamma oscillations in the hippocampus of the behaving rat. Neuron 2003, 37:311-322.
35. Cunningham M.O., Davies C.H., Buhl E.H., Kopell N., Whittington M.A. Gamma oscillations induced by kainate receptor activation in the entorhinal cortex in vitro. Journal of Neuroscience 2003, 23:9761-9769.
36. Cunningham M.O., Halliday D.M., Davies C.H., Traub R.D., Buhl E.H., Whittington M.A. Coexistence of gamma and high-frequency oscillations in rat medial entorhinal cortex in vitro. Journal of Physiology 2004, 559:347-353.
37. Cunningham M.O., Pervouchine D.D., Racca C., Kopell N.J., Davies C.H., Jones R.S.G., et al. Neuronal metabolism governs cortical network response state. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:5597-5601.
38. Davies C.H., Davies S.N., Collingridge G.L. Paired-pulse depression of monosynaptic GABA-mediated inhibitory postsynaptic responses in rat hippocampus. Journal of Physiology 1990, 424:513-531.
39. B receptors in the ca1 region of rat hippocampus. Neuropharmacology 1993, 32:1071-1073.
40. B receptors. Journal of Neuroscience 1998, 18:9099-9111.
41. Diekelmann S., Born J. The memory function of sleep. Nature Reviews Neuroscience 2010, 11:114-126.
42. Dittman J.S., Regehr W.G. Contributions of calcium-dependent and calcium-independent mechanisms to presynaptic inhibition at a cerebellar synapse. Journal of Neuroscience 1996, 16:1623-1633.
43. B receptors in the central nervous system. Nature 1988, 332:156-158.
44. Dvorak-Carbone H., Schuman E.M. Long-term depression of temporoammonic-ca1 hippocampal synaptic transmission. Journal of Neurophysiology 1999, 81:1036-1044.
45. B receptor cell surface stability. Journal of Biological Chemistry 2004, 279:12565-12573.
46. Fell J., Klaver P., Lehnertz K., Grunwald T., Schaller C., Elger C.E., et al. Human memory formation is accompanied by rhinal-hippocampal coupling and decoupling. Nature Neuroscience 2001, 4:1259-1264.
47. Fisahn A., Contractor A., Traub R.D., Buhl E.H., Heinemann S.F., McBain C.J. Distinct roles for the kainate receptor subunits GluR5 and GluR6 in kainate-induced hippocampal gamma oscillations. Journal of Neuroscience 2004, 24:9658-9668.
48. Fisahn A., Pike F.G., Buhl E.H., Paulsen O. Cholinergic induction of network oscillations at 40hz in the hippocampus in vitro. Nature 1998, 394:186-189.
49. Fischer Y., Wittner L., Freund T.F., Gähwiler B.H. Simultaneous activation of gamma and theta network oscillations in rat hippocampal slice cultures. Journal of Physiology 2002, 539:857-868.
50. Fries P., Reynolds J.H., Rorie A.E., Desimone R. Modulation of oscillatory neuronal synchronization by selective visual attention. Science 2001, 291:1560-1563.
51. B receptor function. EMBO Journal 2001, 20:2152-2159.
52. B receptor antagonists in an active avoidance learning paradigm in rats. Psychopharmacology 1998, 137:369-373.
53. A receptor function in developing rat thalamic reticular neurons: whole cell recordings of GABA-mediated currents and modulation by clonazepam. Journal of Neurophysiology 1996, 76:2568-2579.
54. Gonchar Y., Burkhalter A. Differential subcellular localization of forward and feedback interareal inputs to parvalbumin expressing GABAergic neurons in rat visual cortex. Journal of Comparative Neurology 1999, 406:346-360.
55. Goutagny R., Jackson J., Williams S. Self-generated theta oscillations in the hippocampus. Nature Neuroscience 2009, 12:1491-1493.
56. Gray J.A. A general model of the limbic system and basal ganglia: applications to schizophrenia and compulsive behavior of the obsessive type. Revue Neurologique 1994, 150:605-613.
57. Hájos N., Katona I., Naiem S.S., MacKie K., Ledent C., Mody I., et al. Cannabinoids inhibit hippocampal GABAergic transmission and network oscillations. European Journal of Neuroscience 2000, 12:3239-3249.
58. Hasselmo M.E. What is the function of hippocampal theta rhythm?-Linking behavioral data to phasic properties of field potential and unit recording data. Hippocampus 2005, 15:936-949.
59. Hasselmo M.E., Wyble B.P., Wallenstein G.V. Encoding and retrieval of episodic memories: role of cholinergic and GABAergic modulation in the hippocampus. Hippocampus 1996, 6:693-708.
60. Hill S., Tononi G. Modeling sleep and wakefulness in the thalamocortical system. Journal of Neurophysiology 2005, 93:1671-1698.
61. Holmgren C., Harkany T., Svennenfors B., Zilberter Y. Pyramidal cell communication within local networks in layer 2/3 of rat neocortex. Journal of Physiology 2003, 551:139-153.
62. Hormuzdi S.G., Pais I., LeBeau F.E., Towers S.K., Rozov A., Buhl E.H., et al. Impaired electrical signaling disrupts gamma frequency oscillations in connexin 36-deficient mice. Neuron 2001, 31:487-495.
63. B receptor activation in absence seizures of lethargic (lh/lh) mice. Science 1992, 257:398-401.
64. Huguenard J.R., Prince D.A. Intrathalamic rhythmicity studied in vitro: nominal t-current modulation causes robust antioscillatory effects. Journal of Neuroscience 1994, 14:5485-5502.
65. Isaacson J.S., Solís J.M., Nicoll R.A. Local and diffuse synaptic actions of GABA in the hippocampus. Neuron 1993, 10:165-175.
66. B R2. Nature 1998, 396:674-679.
67. Jouvet M. Biogenic amines and the states of sleep. Science 1969, 163:32-41.
68. B receptors, schizophrenia and sleep dysfunction: A review of the relationship and its potential clinical and therapeutic implications. CNS Drugs 2009, 23:681-691.
69. B -receptor subtypes assemble into functional heteromeric complexes. Nature 1998, 396:683-687.
70. Kim U., Sanchez-Vives M.V., McCormick D.A. Functional dynamics of gabaergic inhibition in the thalamus. Science 1997, 278:130-134.
71. B receptors. Brain Research 1997, 775:91-98.
72. Kwag J., Paulsen O. The timing of external input controls the sign of plasticity at local synapses. Nature Neuroscience 2009, 12:1219-1221.
73. Lambert N.A., Wilson W.A. Temporally distinct mechanisms of use-dependent depression at inhibitory synapses in the rat hippocampus in vitro. Journal of Neurophysiology 1994, 72:121-130.
74. Lebeau F.E.N., Towers S.K., Traub R.D., Whittington M.A., Buhl E.H. Fast network oscillations induced by potassium transients in the rat hippocampus in vitro. Journal of Physiology 2002, 542:167-179.
75. B receptor modulation of excitatory and inhibitory synaptic transmission onto rat CA3 hippocampal interneurons. Journal of Physiology (Paris) 2003, 546:439-453.
76. B -receptor blockade in the freely moving rat. Epilepsia 2005, 46:203-216.
77. B receptor blockade enhances theta and gamma rhythms in the hippocampus of behaving rats. Hippocampus 2007, 17:281-291.
78. Lisman J., Buzsáki G. A neural coding scheme formed by the combined function of gamma and theta oscillations. Schizophrenia Bulletin 2008, 34:974-980.
79. B neurotransmission in the control of absence seizures in the rat. Neuroscience 1992, 48:87-93.
80. Llinás R., Ribary U., Contreras D., Pedroarena C. The neuronal basis for consciousness. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 1998, 353:1841-1849.
81. B R2 during rat neocortical development. European Journal of Neuroscience 2002, 15:1766-1778.
82. B2 in the rat hippocampus during prenatal and postnatal development. Hippocampus 2004, 14:836-848.
83. + channels (GIRKS) mediate postsynaptic but not presynaptic transmitter actions in hippocampal neurons. Neuron 1997, 19:687-695.
84. MacLean J.N., Watson B.O., Aaron G.B., Yuste R. Internal dynamics determine the cortical response to thalamic stimulation. Neuron 2005, 48:811-823.
85. B receptors in balancing and terminating persistent cortical activity. Journal of Neuroscience 2009, 29:7513-7518.
86. Mann E.O., Paulsen O. Mechanisms underlying gamma ("40hz") network oscillations in the hippocampus - a mini-review. Progress in Biophysics and Molecular Biology 2005, 87:67-76.
87. B receptor antagonists: potential new anti-absence drugs. Journal of Neural Transmission. Supplementum 1992, 35:179-188.
88. Meeren H., van Luijtelaar G., Lopes da Silva F., Coenen A. Evolving concepts on the pathophysiology of absence seizures: the cortical focus theory. Archives of Neurology 2005, 62:371-376.
89. Milojkovic B.A., Radojicic M.S., Antic S.D. A strict correlation between dendritic and somatic plateau depolarizations in the rat prefrontal cortex pyramidal neurons. Journal of Neuroscience 2005, 25:3940-3951.
90. 2+ channels in central neurons. Neuron 1993, 10:889-898.
91. Mody I., De Koninck Y., Otis T.S., Soltesz I. Bridging the cleft at GABA synapses in the brain. Trends in Neurosciences 1994, 17:517-525.
92. B blocker improves the cognitive performance of mice, rats, and rhesus monkeys. Behavioral and Neural Biology 1993, 60:62-68.
93. Montgomery S.M., Buzsáki G. Gamma oscillations dynamically couple hippocampal CA3 and CA1 regions during memory task performance. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:14495-14500.
94. Oláh S., Füle M., Komlósi G., Varga C., Báldi R., Barz P., et al. Regulation of cortical microcircuits by unitary GABA-mediated volume transmission. Nature 2009, 461:1278-1281.
95. B modulate oscillatory activity in auditory cortex. Journal of Neuroscience 2009, 29:10321-10334.
96. B to synaptically induced afterhyperpolarizations in CA1: A brake on the NMDA response. Journal of Neurophysiology 2004, 92:2027-2039.
97. Palhalmi J., Paulsen O., Freund T.F., Hajos N. Distinct properties of carbachol- and DHPG-induced network oscillations in hippocampal slices. Neuropharmacology 2004, 47:381-389.
98. 2+ spikes in layer 5 somatosensory pyramidal neurons. Neuron 2006, 50:603-616.
99. Petsche H., Stumpf C., Gogolak G. The significance of the rabbit's septum as a relay station between the midbrain and the hippocampus. I. The control of hippocampus arousal activity by the septum cells. Electroencephalography and Clinical Neurophysiology 1962, 14:202-211.
100. Price C.J., Cauli B., Kovacs E.R., Kulik A., Lambolez B., Shigemoto R., et al. Neurogliaform neurons form a novel inhibitory network in the hippocampal CA1 area. Journal of Neuroscience 2005, 25:6775-6786.
101. B receptor modulation of feedforward inhibition through hippocampal neurogliaform cells. Journal of Neuroscience 2008, 28:6974-6982.
102. B1 -deficient mice. Molecular and Cellular Neuroscience 2001, 17:1059-1070.
103. Rigas P., Castro-Alamancos M.A. Thalamocortical Up states: differential effects of intrinsic and extrinsic cortical inputs on persistent activity. Journal of Neuroscience 2007, 27:4261-4272.
104. B receptor heterodimer. Journal of Neuroscience 2001, 21:8043-8052.
105. Roy J.P., Clercq M., Steriade M., Deschĉnes M. Electrophysiology of neurons of lateral thalamic nuclei in cat: mechanisms of long-lasting hyperpolarizations. Journal of Neurophysiology 1984, 51:1220-1235.
106. B receptor activation at a glutamatergic synapse. Nature 2003, 424:775-778.
107. Sanchez-Vives M.V., McCormick D.A. Cellular and network mechanisms of rhythmic recurrent activity in neocortex. Nature Neuroscience 2000, 3:1027-1034.
108. B receptors to control rhythmic hippocampal activity. Neuron 2000, 25:673-681.
109. B(1) . Neuron 2001, 31:47-58.
110. Sederberg P.B., Schulze-Bonhage A., Madsen J.R., Bromfield E.B., McCarthy D.C., Brandt A., et al. Hippocampal and neocortical gamma oscillations predict memory formation in humans. Cerebral Cortex 2007, 17:1190-1196.
111. Shu Y., Hasenstaub A., McCormick D.A. Turning on and off recurrent balanced cortical activity. Nature 2003, 423:288-293.
112. Singer W. Synchronization of cortical activity and its putative role in information processing and learning. Annual Review of Physiology 1993, 55:349-374.
113. Sohal V., Zhang F., Yizhar O., Deisseroth K. Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature 2009, 459:698-702.
114. Soltesz I., Deschĉnes M. Low- and high-frequency membrane potential oscillations during theta activity in CA1 and CA3 pyramidal neurons of the rat hippocampus under ketamine-xylazine anesthesia. Journal of Neurophysiology 1993, 70:97-116.
115. Song C., Murray T.A., Kimura R., Wakui M., Ellsworth K., Javedan S.P., et al. Role of α7-nicotinic acetylcholine receptors in tetanic stimulation-induced γ oscillations in rat hippocampal slices. Neuropharmacology 2005, 48:869-880.
116. B receptor antagonism: facilitatory effects on memory parallel those on LTP induced by TBS but not HFS. Journal of Neuroscience 1999, 19:4609-4615.
117. Steriade M., Contreras D., Amzica F., Timofeev I. Synchronization of fast (30-40hz) spontaneous oscillations in intrathalamic and thalamocortical networks. Journal of Neuroscience 1996, 16:2788-2808.
118. Steriade M., Contreras D., Curró Dossi R., Nuñez A. The slow (<1hz) oscillation in reticular thalamic and thalamocortical neurons: Scenario of sleep rhythm generation in interacting thalamic and neocortical networks. Journal of Neuroscience 1993, 13:3284-3299.
119. Steriade M., McCormick D.A., Sejnowski T.J. Thalamocortical oscillations in the sleeping and aroused brain. Science 1993, 262:679-685.
120. Steriade M., Nuñez A., Amzica F. Intracellular analysis of relations between the slow (<1hz) neocortical oscillation and other sleep rhythms of the electroencephalogram. Journal of Neuroscience 1993, 13:3266-3283.
121. Steriade M., Nuñez A., Amzica F. A novel slow (<1hz) oscillation of neocortical neurons in vivo: Depolarizing and hyperpolarizing components. Journal of Neuroscience 1993, 13:3252-3265.
122. B receptor. Journal of Neuroscience 1998, 18:3138-3146.
123. Tamás G., Lorincz A., Simon A., Szabadics J. Identified sources and targets of slow inhibition in the neocortex. Science 2003, 299:1902-1905.
124. Thompson S.M., Capogna M., Scanziani M. Presynaptic inhibition in the hippocampus. Trends in Neurosciences 1993, 16:222-227.
125. Thomson A.M., Destexhe A. Dual intracellular recordings and computational models of slow inhibitory postsynaptic potentials in rat neocortical and hippocampal slices. Neuroscience 1999, 92:1193-1215.
126. Thomson A.M., West D.C., Hahn J., Deuchars J. Single axon IPSPs elicited in pyramidal cells by three classes of interneurones in slices of rat neocortex. Journal of Physiology 1996, 496:81-102.
127. Timofeev I., Grenier F., Bazhenov M., Sejnowski T.J., Steriade M. Origin of slow cortical oscillations in deafferented cortical slabs. Cerebral Cortex 2000, 10:1185-1199.
128. Traub R.D., Bibbig A., Fisahn A., LeBeau F.E., Whittington M.A., Buhl E.H. A model of gamma-frequency network oscillations induced in the rat CA3 region by carbachol in vitro. European Journal of Neuroscience 2000, 12:4093-4106.
129. Traub R.D., Bibbig A., Lebeau F.E.N., Cunningham M.O., Whittington M.A. Persistent gamma oscillations in superficial layers of rat auditory neocortex: experiment and model. Journal of Physiology 2005, 562:3-8.
130. Traub R.D., Spruston N., Soltesz I., Konnerth A., Whittington M.A., Jefferys G.R. Gamma-frequency oscillations: A neuronal population phenomenon, regulated by synaptic and intrinsic cellular processes, and inducing synaptic plasticity. Progress in Neurobiology 1998, 55:563-575.
131. Uhlhaas P.J., Singer W. Abnormal neural oscillations and synchrony in schizophrenia. Nature Reviews Neuroscience 2010, 11:100-113.
132. Ulrich D., Bettler B. GABA(b) receptors: synaptic functions and mechanisms of diversity. Current Opinion in Neurobiology 2007, 17:298-303.
133. Ulrich D., Huguenard J.R. γ-aminobutyric acid type B receptor-dependent burst-firing in thalamic neurons: A dynamic clamp study. Proceedings of the National Academy of Sciences of the United States of America 1996, 93:13245-13249.
134. Vanderwolf C.H. Hippocampal electrical activity and voluntary movement in the rat. Electroencephalography and Clinical Neurophysiology 1969, 26:407-418.
135. Varela F., Lachaux J.P., Rodriguez E., Martinerie J. The brainweb: phase synchronization and large-scale integration. Nature Reviews Neuroscience 2001, 2:229-239.
136. B receptors is independent of γ-aminobutyric acid but controlled by glutamate in central neurons. Journal of Biological Chemistry 2008, 283:24641-24648.
137. B receptor antagonists on absences and convulsive seizures. European Journal of Pharmacology 1997, 332:245-255.
138. B receptor variants. Neuron 2006, 50:589-601.
139. Volgushev M., Chauvette S., Mukovski M., Timofeev I. Precise long-range synchronization of activity and silence in neocortical neurons during slow-wave oscillations. Journal of Neuroscience 2006, 26:5665-5672.
140. Wallenstein G.V., Hasselmo M.E. GABAergic modulation of hippocampal population activity: sequence learning, place field development, and the phase precession effect. Journal of Neurophysiology 1997, 78:393-408.
141. Wespatat V., Tennigkeit F., Singer W. Phase sensitivity of synaptic modifications in oscillating cells of rat visual cortex. Journal of Neuroscience 2004, 24:9067-9075.
142. B receptor. Nature 1998, 396:679-682.
143. Whittington M.A., Traub R.D., Jefferys J.G. Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation. Nature 1995, 373:612-615.
144. B receptors in rat cerebellum. Nature 1981, 294:584-587.
145. Ylinen A., Soltész I., Bragin A., Penttonen M., Sik A., Buzsáki G. Intracellular correlates of hippocampal theta rhythm in identified pyramidal cells, granule cells, and basket cells. Hippocampus 1995, 5:78-90.