Neural circuits underlying the generation of theta oscillations

Journal of Physiology Paris

Volumn 106, Issue 3-4, 2012, Pages 81-92

  Pignatelli, Michele ^a   Beyeler, Anna ^a   Leinekugel, Xavier ^a  

^a INSTITUT DES MALADIES NEURODÉGÉNÉRATIVES   (France)

Author keywords

Brainstem; Cholinergic system; Hippocampus; Limbic system; Neuronal networks; Oscillations; Theta

Indexed keywords

ARTICLE; ENTORHINAL CORTEX; FOREBRAIN; HIPPOCAMPUS; HUMAN; MEDIAL SEPTUM; NERVE CELL; NERVE CELL NETWORK; NEURAL CIRCUIT; NONHUMAN; OSCILLATION; PEDUNCULOPONTINE TEGMENTAL NUCLEUS; REM SLEEP; THETA RHYTHM; WAKEFULNESS;

AMYGDALA; ANIMALS; BRAIN STEM; ELECTROENCEPHALOGRAPHY; ENTORHINAL CORTEX; HIPPOCAMPUS; HUMANS; MICE; MIDLINE THALAMIC NUCLEI; NERVE NET; NEURAL PATHWAYS; PREFRONTAL CORTEX; RATS; SEPTAL NUCLEI; THETA RHYTHM; WAKEFULNESS;

EID: 84862212803     PISSN: 09284257     EISSN: 17697115     Source Type: Journal    
DOI: 10.1016/j.jphysparis.2011.09.007     Document Type: Article

References (211)

1. Allen-Brain-Atlas.
2. Allen G.V., Hopkins D.A. Topography and synaptology of mamillary body projections to the mesencephalon and pons in the rat. J. Comp. Neurol. 1990, 301(2):214-231.
3. +-dependent theta-like rhythmicity in stellate cells of entorhinal cortex layer II. Nature 1989, 342(6246):175-177.
4. Amaral D.G., Witter M.P. The three-dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience 1989, 31(3):571-591.
5. Anderson M.I., O'Mara S.M. Analysis of recordings of single-unit firing and population activity in the dorsal subiculum of unrestrained, freely moving rats. J. Neurophysiol. 2003, 90(2):655-665.
6. Apergis-Schoute J., Pinto A., Paré D. Ultrastructural organization of medial prefrontal inputs to the rhinal cortices. Eur. J. Neurosci. 2006, 24(1):135-144.
7. Bassant M.H., Poindessous-Jazat F. Ventral tegmental nucleus of Gudden: a pontine hippocampal theta generator?. Hippocampus 2001, 11(6):809-813.
8. Benchenane K., Peyrache A., Khamassi M., Tierney P.L., Gioanni Y., Battaglia F.P., Wiener S.I. Coherent theta oscillations and reorganization of spike timing in the hippocampal-prefrontal network upon learning. Neuron 2010, 66(6):921-936.
9. Bernard J.F., Alden M., Besson J.M. The organization of the efferent projections from the pontine parabrachial area to the amygdaloid complex: a Phaseolus vulgaris leucoagglutinin (PHA-L) study in the rat. J. Comp. Neurol. 1993, 329(2):201-229.
10. Berridge C.W., Foote S.L. Effects of locus coeruleus activation on electroencephalographic activity in neocortex and hippocampus. J. Neurosci. 1991, 11(10):3135-3145.
11. Bland B.H. The physiology and pharmacology of hippocampal formation theta rhythms. Prog. Neurobiol. 1986, 26(1):1-54.
12. Bland B.H., Colom L.V., Konopacki J., Roth S.H. Intracellular records of carbachol-induced theta rhythm in hippocampal slices. Brain Res. 1988, 447(2):364-368.
13. Bland B.H., Konopacki J., Kirk I.J., Oddie S.D., Dickson C.T. Discharge patterns of hippocampal theta-related cells in the caudal diencephalon of the urethan-anesthetized rat. J. Neurophysiol. 1995, 74(1):322-333.
14. Bland B.H., Oddie S.D. Anatomical, electrophysiological and pharmacological studies of ascending brainstem hippocampal synchronizing pathways. Neurosci. Biobehav. Rev. 1998, 22(2):259-273.
15. Bland B.H., Trepel C., Oddie S.D., Kirk I.J. Intraseptal microinfusion of muscimol: effects on hippocampal formation theta field activity and phasic theta-ON cell discharges. Exp. Neurol. 1996, 138(2):286-297.
16. Boccara C.N., Sargolini F., Thoresen V.H., Solstad T., Witter M.P., Moser E.I., Moser M.-B. Grid cells in pre- and parasubiculum. Nat. Neurosci. 2010, 13(8):987-994.
17. Bocian R., Konopacki J. Posterior hypothalamic GABAergic mediation of hippocampal theta in the cat. Brain Res. Bull. 2007, 73(4-6):289-300.
18. Bokor H., Csáki A., Kocsis K., Kiss J. Cellular architecture of the nucleus reuniens thalami and its putative aspartatergic/glutamatergic projection to the hippocampus and medial septum in the rat. Eur. J. Neurosci. 2002, 16(7):1227-1239.
19. Borhegyi Z., Freund T.F. Dual projection from the medial septum to the supramammillary nucleus in the rat. Brain Res. Bull. 1998, 46(5):453-459.
20. Borhegyi Z., Maglóczky Z., Acsády L., Freund T.F. The supramammillary nucleus innervates cholinergic and GABAergic neurons in the medial septum-diagonal band of Broca complex. Neuroscience 1998, 82(4):1053-1065.
21. Bradley P.B., Nicholson A.N. The effect of some drugs on hippocampal arousal. Electroencephalogr. Clin. Neurophysiol. 1962, 14:824-834.
22. Brandon M.P., Bogaard A.R., Libby C.P., Connerney M.A., Gupta K., Hasselmo M.E. Reduction of theta rhythm dissociates grid cell spatial periodicity from directional tuning. Science 2011, 332(6029):595-599.
23. Buzsáki G. Theta oscillations in the hippocampus. Neuron 2002.
24. Buzsáki G., Buhl D.L., Harris K.D., Csicsvari J., Czéh B., Morozov A. Hippocampal network patterns of activity in the mouse. Neuroscience 2003, 116(1):201-211.
25. Cacucci F., Lever C., Wills T.J., Burgess N., O'Keefe J. Theta-modulated place-by-direction cells in the hippocampal formation in the rat. J. Neurosci. 2004, 24(38):8265-8277.
26. Canteras N.S., Simerly R.B., Swanson L.W. Connections of the posterior nucleus of the amygdala. J. Comp. Neurol. 1992, 324(2):143-179.
27. Canteras N.S., Swanson L.W. Projections of the ventral subiculum to the amygdala, septum, and hypothalamus: a PHAL anterograde tract-tracing study in the rat. J. Comp. Neurol. 1992, 324(2):180-194.
28. Cantero J.L., Atienza M., Stickgold R., Kahana M.J., Madsen J.R., Kocsis B. Sleep-dependent theta oscillations in the human hippocampus and neocortex. J. Neurosci. 2003, 23(34):10897-10903.
29. Cassell M.D., Wright D.J. Topography of projections from the medial prefrontal cortex to the amygdala in the rat. Brain Res. Bull. 1986, 17(3):321-333.
30. Chrobak J.J., Buzsáki G. Selective activation of deep layer (V-VI) retrohippocampal cortical neurons during hippocampal sharp waves in the behaving rat. J. Neurosci. 1994, 14(10):6160-6170.
31. Cicchetti F., Lacroix S., Beach T.G., Parent A. Calretinin gene expression in the human thalamus. Brain Res. Mol. Brain Res. 1998, 54(1):1-12.
32. Clarke D.J. Cholinergic innervation of the rat dentate gyrus: an immunocytochemical and electron microscopical study. Brain Res. 1985, 360(1-2):349-354.
33. Clement E.A., Richard A., Thwaites M., Ailon J., Peters S., Dickson C.T. Cyclic and sleep-like spontaneous alternations of brain state under urethane anaesthesia. PLoS ONE 2008, 3(4):e2004.
34. Colom L.V., Bland B.H. State-dependent spike train dynamics of hippocampal formation neurons: evidence for theta-on and theta-off cells. Brain Res. 1987, 422(2):277-286.
35. Colom L.V., Castaneda M.T., Reyna T., Hernandez S., Garrido-Sanabria E. Characterization of medial septal glutamatergic neurons and their projection to the hippocampus. Synapse 2005, 58(3):151-164.
36. Condé F., Audinat E., Maire-Lepoivre E., Crépel F. Afferent connections of the medial frontal cortex of the rat. A study using retrograde transport of fluorescent dyes. I. Thalamic afferents. Brain Res. Bull. 1990, 24(3):341-354.
37. Condé F., Maire-Lepoivre E., Audinat E., Crépel F. Afferent connections of the medial frontal cortex of the rat. II. Cortical and subcortical afferents. J. Comp. Neurol. 1995, 352(4):567-593.
38. Crutcher K.A., Madison R., Davis J.N. A study of the rat septohippocampal pathway using anterograde transport of horseradish peroxidase. Neuroscience 1981, 6(10):1961-1973.
39. Csicsvari J., Henze D.A., Jamieson B., Harris K.D., Sirota A., Barthó P., Wise K.D., Buzsáki G. Massively parallel recording of unit and local field potentials with silicon-based electrodes. J. Neurophysiol. 2003, 90(2):1314-1323.
40. Csicsvari J., Hirase H., Mamiya A., Buzsáki G. Ensemble patterns of hippocampal CA3-CA1 neurons during sharp wave-associated population events. Neuron 2000, 28(2):585-594.
41. Datta S., Siwek D.F. Excitation of the brain stem pedunculopontine tegmentum cholinergic cells induces wakefulness and .... J. Neurophysiol. 1997.
42. Deshmukh S.S., Yoganarasimha D., Voicu H., Knierim J.J. Theta modulation in the medial and the lateral entorhinal cortices. J. Neurophysiol. 2010, 104(2):994-1006.
43. Dickson C.T., Kirk I.J., Oddie S.D., Bland B.H. Classification of theta-related cells in the entorhinal cortex: cell discharges are controlled by the ascending brainstem synchronizing pathway in parallel with hippocampal theta-related cells. Hippocampus 1995, 5(4):306-319.
44. Dickson C.T., Magistretti J., Shalinsky M.H., Fransén E., Hasselmo M.E., Alonso A. Properties and role of I(h) in the pacing of subthreshold oscillations in entorhinal cortex layer II neurons. J. Neurophysiol. 2000, 83(5):2562-2579.
45. Dolleman-Van der Weel M.J., Witter M.P. Projections from the nucleus reuniens thalami to the entorhinal cortex, hippocampal field CA1, and the subiculum in the rat arise from different populations of neurons. J. Comp. Neurol. 1996, 364(4):637-650.
46. Dolleman-Van der Weel M.J., Witter M.P. Nucleus reuniens thalami innervates gamma aminobutyric acid positive cells in hippocampal field CA1 of the rat. Neurosci. Lett. 2000, 278(3):145-148.
47. Dolorfo C.L., Amaral D.G. Entorhinal cortex of the rat: topographic organization of the cells of origin of the perforant path projection to the dentate gyrus. J. Comp. Neurol. 1998, 398(1):25-48.
48. Dougherty K.D., Milner T.A. Cholinergic septal afferent terminals preferentially contact neuropeptide Y-containing interneurons compared to parvalbumin-containing interneurons in the rat dentate gyrus. J. Neurosci. 1999, 19(22):10140-10152.
49. Dragoi G., Buzsaki G. Temporal encoding of place sequences by hippocampal cell assemblies. Neuron 2006, 50(1):145-157.
50. Dragoi G., Carpi D., Recce M., Csicsvari J., Buzsáki G. Interactions between hippocampus and medial septum during sharp waves and theta oscillation in the behaving rat. J. Neurosci. 1999, 19(14):6191-6199.
51. Egorov A.V., Hamam B.N., Fransén E., Hasselmo M.E., Alonso A.A. Graded persistent activity in entorhinal cortex neurons. Nature 2002, 420(6912):173-178.
52. Freund T.F. GABAergic septohippocampal neurons contain parvalbumin. Brain Res. 1989, 478(2):375-381.
53. Freund T.F., Antal M. GABA-containing neurons in the septum control inhibitory interneurons in the hippocampus. Nature 1988, 336(6195):170-173.
54. Frotscher M. Target cell specificity of synaptic connections in the hippocampus. Hippocampus 1991, 1(2):123-130.
55. Fuller P.M., Saper C.B., Lu J. The pontine REM switch: past and present. J. Physiol. (Lond.) 2007, 584(Pt. 3):735-741.
56. Gabbott P., Headlam A., Busby S. Morphological evidence that CA1 hippocampal afferents monosynaptically innervate PV-containing neurons and NADPH-diaphorase reactive cells in the medial prefrontal cortex (Areas 25/32) of the rat. Brain Res. 2002, 946(2):314-322.
57. Gabbott P.L.A., Warner T.A., Jays P.R.L., Salway P., Busby S.J. Prefrontal cortex in the rat: projections to subcortical autonomic, motor, and limbic centers. J. Comp. Neurol. 2005, 492(2):145-177.
58. Gaykema R.P., Luiten P.G., Nyakas C., Traber J. Cortical projection patterns of the medial septum-diagonal band complex. J. Comp. Neurol. 1990, 293(1):103-124.
59. Gaykema R.P., van Weeghel R., Hersh L.B., Luiten P.G. Prefrontal cortical projections to the cholinergic neurons in the basal forebrain. J. Comp. Neurol. 1991, 303(4):563-583.
60. Glasgow S.D., Chapman C.A. Local generation of theta-frequency EEG activity in the parasubiculum. J. Neurophysiol. 2007, 97(6):3868-3879.
61. Glasgow S.D., Chapman C.A. Conductances mediating intrinsic theta-frequency membrane potential oscillations in layer II parasubicular neurons. J. Neurophysiol. 2008, 100(5):2746-2756.
62. Gołebiewski H., Eckersdorf B., Błaszczyk M., Grabowski R., Konopacki J. Muscarinic (M1) mediation of carbachol-induced theta in the cat entorhinal cortex in vitro. Neuroreport 1994, 5(15):1989-1992.
63. Gonzalo-Ruiz A., Morte L., Flecha J.M., Sanz J.M. Neurotransmitter characteristics of neurons projecting to the supramammillary nucleus of the rat. Anat. Embryol. 1999, 200(4):377-392.
64. Goto M., Swanson L.W., Canteras N.S. Connections of the nucleus incertus. J. Comp. Neurol. 2001, 438(1):86-122.
65. Goutagny R., Jackson J., Williams S. Self-generated theta oscillations in the hippocampus. Nat. Neurosci. 2009, 12(12):1491-1493.
66. Gradinaru V., Zhang F., Ramakrishnan C., Mattis J., Prakash R., Diester I., Goshen I., Thompson K.R., Deisseroth K. Molecular and cellular approaches for diversifying and extending optogenetics. Cell 2010, 141(1):154-165.
67. Green J.D., Arduini A.A. Hippocampal electrical activity in arousal. J. Neurophysiol. 1954, 17(6):533-557.
68. Hafting T., Fyhn M., Bonnevie T., Moser M.-B., Moser E.I. Hippocampus-independent phase precession in entorhinal grid cells. Nature 2008, 453(7199):1248-1252.
69. Hafting T., Fyhn M., Molden S., Moser M.-B., Moser E.I. Microstructure of a spatial map in the entorhinal cortex. Nature 2005, 436(7052):801-806.
70. Hajszan T., Alreja M., Leranth C. Intrinsic vesicular glutamate transporter 2-immunoreactive input to septohippocampal parvalbumin-containing neurons: novel glutamatergic local circuit cells. Hippocampus 2004, 14(4):499-509.
71. Hallanger A.E., Levey A.I., Lee H.J., Rye D.B., Wainer B.H. The origins of cholinergic and other subcortical afferents to the thalamus in the rat. J. Comp. Neurol. 1987, 262(1):105-124.
72. Hallanger A.E., Wainer B.H. Ascending projections from the pedunculopontine tegmental nucleus and the adjacent mesopontine tegmentum in the rat. J. Comp. Neurol. 1988, 274(4):483-515.
73. Hangya B., Borhegyi Z., Szilágyi N., Freund T.F., Varga V. GABAergic neurons of the medial septum lead the hippocampal network during theta activity. J. Neurosci. 2009, 29(25):8094-8102.
74. Hartwich K., Pollak T., Klausberger T. Distinct firing patterns of identified basket and dendrite-targeting interneurons in the prefrontal cortex during hippocampal theta and local spindle oscillations. J. Neurosci. 2009, 29(30):9563-9574.
75. Hinman J.R., Penley S.C., Long L.L., Escabí M.A., Chrobak J.J. Septotemporal variation in dynamics of theta: speed and habituation. J. Neurophysiol. 2011, 105(6):2675-2686.
76. Huh C.Y.L., Goutagny R., Williams S. Glutamatergic neurons of the mouse medial septum and diagonal band of Broca synaptically drive hippocampal pyramidal cells: relevance for hippocampal theta rhythm. J. Neurosci. 2010, 30(47):15951-15961.
77. Hyman J.M., Zilli E.A., Paley A.M., Hasselmo M.E. Medial prefrontal cortex cells show dynamic modulation with the hippocampal theta rhythm dependent on behavior. Hippocampus 2005, 15(6):739-749.
78. Inglis W.L., Winn P. The pedunculopontine tegmental nucleus: where the striatum meets the reticular formation. Prog. Neurobiol. 1995, 47(1):1-29.
79. Irle E., Sarter M., Guldin W.O., Markowitsch H.J. Afferents to the ventral tegmental nucleus of Gudden in the mouse, rat, and cat. J. Comp. Neurol. 1984, 228(4):509-541.
80. Jackson J., Dickson C.T., Bland B.H. Median raphe stimulation disrupts hippocampal theta via rapid inhibition and state-dependent phase reset of theta-related neural circuitry. J. Neurophysiol. 2008, 99(6):3009-3026.
81. Jasper H.H., Tessier J. Acetylcholine liberation from cerebral cortex during paradoxical (REM) sleep. Science 1971, 172(983):601-602.
82. Jeffery K.J., Donnett J.G., O'Keefe J. Medial septal control of theta-correlated unit firing in the entorhinal cortex of awake rats. Neuroreport 1995, 6(16):2166-2170.
83. Jensen O. Reading the hippocampal code by theta phase-locking. Trends Cogn. Sci. (Regul. Ed.) 2005, 9(12):551-553.
84. Jolkkonen E., Miettinen R., Pikkarainen M., Pitkänen A. Projections from the amygdaloid complex to the magnocellular cholinergic basal forebrain in rat. Neuroscience 2002, 111(1):133-149.
85. Jones M.W., Wilson M.A. Phase precession of medial prefrontal cortical activity relative to the hippocampal theta rhythm. Hippocampus 2005, 15(7):867-873.
86. Jones M.W., Wilson M.A. Theta rhythms coordinate hippocampal-prefrontal interactions in a spatial memory task. PLoS Biol 2005, 3(12):e402.
87. Kahana M.J., Seelig D., Madsen J.R. Theta returns. Curr. Opin. Neurobiol. 2001, 11(6):739-744.
88. Kahana M.J., Sekuler R., Caplan J.B., Kirschen M., Madsen J.R. Human theta oscillations exhibit task dependence during virtual maze navigation. Nature 1999, 399(6738):781-784.
89. Kamondi A., Acsády L., Wang X.J., Buzsáki G. Theta oscillations in somata and dendrites of hippocampal pyramidal cells in vivo: activity-dependent phase-precession of action potentials. Hippocampus 1998, 8(3):244-261.
90. Karashima A., Nakao M., Honda K., Iwasaki N., Katayama N., Yamamoto M. Theta wave amplitude and frequency are differentially correlated with pontine waves and rapid eye movements during REM sleep in rats. Neurosci. Res. 2004, 50(3):283-289.
91. Karashima A., Nakao M., Katayama N., Honda K. Instantaneous acceleration and amplification of hippocampal theta wave coincident with phasic pontine activities during REM sleep. Brain Res. 2005, 1051(1-2):50-56.
92. Kemppainen S., Jolkkonen E., Pitkänen A. Projections from the posterior cortical nucleus of the amygdala to the hippocampal formation and parahippocampal region in rat. Hippocampus 2002, 12(6):735-755.
93. Kinney G.G., Kocsis B., Vertes R.P. Injections of muscimol into the median raphe nucleus produce hippocampal theta rhythm in the urethane anesthetized rat. Psychopharmacology (Berl.) 1995, 120(3):244-248.
94. Kirk I.J., McNaughton N. Supramammillary cell firing and hippocampal rhythmical slow activity. Neuroreport 1991, 2(11):723-725.
95. Kirk I.J., McNaughton N. Mapping the differential effects of procaine on frequency and amplitude of reticularly elicited hippocampal rhythmical slow activity. Hippocampus 1993, 3(4):517-525.
96. Kirk I.J., Oddie S.D., Konopacki J., Bland B.H. Evidence for differential control of posterior hypothalamic, supramammillary, and medial mammillary theta-related cellular discharge by ascending and descending pathways. J. Neurosci. 1996, 16(17):5547-5554.
97. Kishi T., Tsumori T., Yokota S., Yasui Y. Topographical projection from the hippocampal formation to the amygdala: a combined anterograde and retrograde tracing study in the rat. J. Comp. Neurol. 2006, 496(3):349-368.
98. Kiss J., Csáki A., Bokor H., Kocsis K., Kocsis B. Possible glutamatergic/aspartatergic projections to the supramammillary nucleus and their origins in the rat studied by selective [(3)H]d-aspartate labelling and immunocytochemistry. Neuroscience 2002, 111(3):671-691.
99. Kiss J., Patel A.J., Baimbridge K.G., Freund T.F. Topographical localization of neurons containing parvalbumin and choline acetyltransferase in the medial septum-diagonal band region of the rat. Neuroscience 1990, 36(1):61-72.
100. Klausberger T., Magill P.J., Márton L.F., Roberts J.D.B., Cobden P.M., Buzsáki G., Somogyi P. Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo. Nature 2003, 421(6925):844-848.
101. Kocsis B. The effect of descending theta rhythmic input from the septohippocampal system on firing in the supramammillary nucleus. Brain Res. 2006, 1086(1):92-97.
102. Kocsis B., Di Prisco G.V., Vertes R.P. Theta synchronization in the limbic system: the role of Gudden's tegmental nuclei. Eur. J. Neurosci. 2001, 13(2):381-388.
103. Kocsis B., Vertes R.P. Dorsal raphe neurons: synchronous discharge with the theta rhythm of the hippocampus in the freely behaving rat. J. Neurophysiol. 1992, 68(4):1463-1467.
104. Kocsis B., Vertes R.P. Characterization of neurons of the supramammillary nucleus and mammillary body that discharge rhythmically with the hippocampal theta rhythm in the rat. J. Neurosci. 1994, 14(11 Pt. 2):7040-7052.
105. Koenig J., Linder A.N., Leutgeb J.K., Leutgeb S. The spatial periodicity of grid cells is not sustained during reduced theta oscillations. Science 2011, 332(6029):592-595.
106. Konopacki J., Bland B.H., MacIver M.B., Roth S.H. Cholinergic theta rhythm in transected hippocampal slices: independent CA1 and dentate generators. Brain Res. 1987, 436(2):217-222.
107. Konopacki J., Gołebiewski H. Theta rhythms in the rat medial entorhinal cortex in vitro: evidence for involvement of muscarinic receptors. Neurosci. Lett. 1992, 141(1):93-96.
108. Konopacki J., MacIver M.B., Bland B.H., Roth S.H. Carbachol-induced EEG 'theta' activity in hippocampal brain slices. Brain Res. 1987, 405(1):196-198.
109. Kramis R., Vanderwolf C.H., Bland B.H. Two types of hippocampal rhythmical slow activity in both the rabbit and the rat: relations to behavior and effects of atropine, diethyl ether, urethane, and pentobarbital. Exp. Neurol. 1975, 49(1 Pt. 1):58-85.
110. Lee H.J., Rye D.B., Hallanger A.E., Levey A.I., Wainer B.H. Cholinergic vs. noncholinergic efferents from the mesopontine tegmentum to the extrapyramidal motor system nuclei. J. Comp. Neurol. 1988, 275(4):469-492.
111. Lee M.G., Chrobak J.J., Sik A., Wiley R.G., Buzsáki G. Hippocampal theta activity following selective lesion of the septal cholinergic system. Neuroscience 1994, 62(4):1033-1047.
112. Leranth C., Frotscher M. Organization of the septal region in the rat brain: cholinergic-GABAergic interconnections and the termination of hippocampo-septal fibers. J. Comp. Neurol. 1989, 289(2):304-314.
113. Lesting J., Narayanan R.T., Kluge C., Sangha S., Seidenbecher T., Pape H.-C. Patterns of coupled theta activity in amygdala-hippocampal-prefrontal cortical circuits during fear extinction. PLoS ONE 2011, 6(6):e21714.
114. Li S., Topchiy I., Kocsis B. The effect of atropine administered in the medial septum or hippocampus on high- and low-frequency theta rhythms in the hippocampus of urethane anesthetized rats. Synapse 2007, 61(6):412-419.
115. Lu J., Sherman D., Devor M., Saper C.B. A putative flip-flop switch for control of REM sleep. Nature 2006, 441(7093):589-594.
116. Lubenov E.V., Siapas A.G. Hippocampal theta oscillations are travelling waves. Nature 2009, 459(7246):534-539.
117. Maglóczky Z., Acsády L., Freund T.F. Principal cells are the postsynaptic targets of supramammillary afferents in the hippocampus of the rat. Hippocampus 1994, 4(3):322-334.
118. Manns I.D., Mainville L., Jones B.E. Evidence for glutamate, in addition to acetylcholine and GABA, neurotransmitter synthesis in basal forebrain neurons projecting to the entorhinal cortex. Neuroscience 2001, 107(2):249-263.
119. Markram H., Segal M. Electrophysiological characteristics of cholinergic and non-cholinergic neurons in the rat medial septum-diagonal band complex. Brain Res. 1990, 513(1):171-174.
120. McDonald A.J. Cortical pathways to the mammalian amygdala. Prog. Neurobiol. 1998, 55(3):257-332.
121. McDonald A.J., Mascagni F. Projections of the lateral entorhinal cortex to the amygdala: a Phaseolus vulgaris leucoagglutinin study in the rat. Neuroscience 1997, 77(2):445-459.
122. McDonald A.J., Mascagni F., Guo L. Projections of the medial and lateral prefrontal cortices to the amygdala: a Phaseolus vulgaris leucoagglutinin study in the rat. Neuroscience 1996, 71(1):55-75.
123. McKenna J.T., Vertes R.P. Afferent projections to nucleus reuniens of the thalamus. J. Comp. Neurol. 2004, 480(2):115-142.
124. Meibach R.C., Siegel A. The origin of fornix fibers which project to the mammillary bodies in the rat: a horseradish peroxidase study. Brain Res. 1975, 88(3):508-512.
125. Meibach R.C., Siegel A. Efferent connections of the septal area in the rat: an analysis utilizing retrograde and anterograde transport methods. Brain Res. 1977, 119(1):1-20.
126. Mesulam M.M., Mufson E.J., Wainer B.H., Levey A.I. Central cholinergic pathways in the rat: an overview based on an alternative nomenclature (Ch1-Ch6). Neuroscience 1983, 10(4):1185-1201.
127. Milner K.L., Mogenson G.J. Electrical and chemical activation of the mesencephalic and subthalamic locomotor regions in freely moving rats. Brain Res. 1988, 452(1-2):273-285.
128. Mitani A., Ito K., Hallanger A.E., Wainer B.H., Kataoka K., McCarley R.W. Cholinergic projections from the laterodorsal and pedunculopontine tegmental nuclei to the pontine gigantocellular tegmental field in the cat. Brain Res. 1988, 451(1-2):397-402.
129. Mitchell S.J., Ranck J.B. Generation of theta rhythm in medial entorhinal cortex of freely moving rats. Brain Res. 1980, 189(1):49-66.
130. Mitchell S.J., Rawlins J.N., Steward O., Olton D.S. Medial septal area lesions disrupt theta rhythm and cholinergic staining in medial entorhinal cortex and produce impaired radial arm maze behavior in rats. J. Neurosci. 1982, 2(3):292-302.
131. Mizumori S.J., Perez G.M., Alvarado M.C., Barnes C.A., McNaughton B.L. Reversible inactivation of the medial septum differentially affects two forms of learning in rats. Brain Res. 1990, 528(1):12-20.
132. Mizumori S.J., Ward K.E., Lavoie A.M. Medial septal modulation of entorhinal single unit activity in anesthetized and freely moving rats. Brain Res. 1992, 570(1-2):188-197.
133. Mizuseki K., Diba K., Pastalkova E., Buzsaki G. Hippocampal CA1 pyramidal cells form functionally distinct sublayers. Nat. Neurosci. 2011, 14(9):1174-1181.
134. Mizuseki K., Sirota A., Pastalkova E., Buzsáki G. Theta oscillations provide temporal windows for local circuit computation in the entorhinal-hippocampal loop. Neuron 2009, 64(2):267-280.
135. Montgomery S.M., Sirota A., Buzsáki G. Theta and gamma coordination of hippocampal networks during waking and rapid eye movement sleep. J. Neurosci. 2008, 28(26):6731-6741.
136. Montoya C.P., Sainsbury R.S. The effects of entorhinal cortex lesions on type 1 and type 2 theta. Physiol. Behav. 1985, 35(1):121-126.
137. Morales, G.J., Ramcharan, E.J., Sundararaman, N., Morgera, S.D., Vertes, R.P., 2007. Analysis of the actions of nucleus reuniens and the entorhinal cortex on EEG and evoked population behavior of the hippocampus. In: Conference Proceedings: Annual International Conference of the IEEE Engineering in Medicine and Biology Society IEEE Engineering in Medicine and Biology Society Conference 2007, pp. 2480-2484.
138. Moruzzi G., Magoun H.W. Brain stem reticular formation and activation of the EEG. Electroencephalogr. Clin. Neurophysiol. 1949, 1(4):455-473.
139. Muñoz M.D., Núñez A., García-Austt E. In vivo intracellular analysis of rat dentate granule cells. Brain Res. 1990, 509(1):91-98.
140. Newman D.B., Ginsberg C.Y. Brainstem reticular nuclei that project to the thalamus in rats: a retrograde tracer study. Brain Behav. Evol. 1994, 44(1):1-39.
141. Nowacka A., Jurkowlaniec E., Trojniar W. Microinjection of procaine into the pedunculopontine tegmental nucleus suppresses hippocampal theta rhythm in urethane-anesthetized rats. Brain Res. Bull. 2002, 58(4):377-384.
142. Nuñez A., Cervera-Ferri A., Olucha-Bordonau F., Ruiz-Torner A., Teruel V. Nucleus incertus contribution to hippocampal theta rhythm generation. Eur. J. Neurosci. 2006, 23(10):2731-2738.
143. Oddie S.D., Bland B.H., Colom L.V., Vertes R.P. The midline posterior hypothalamic region comprises a critical part of the ascending brainstem hippocampal synchronizing pathway. Hippocampus 1994, 4(4):454-473.
144. Otake K., Reis D.J., Ruggiero D.A. Afferents to the midline thalamus issue collaterals to the nucleus tractus solitarii: an anatomical basis for thalamic and visceral reflex integration. J. Neurosci. 1994, 14(9):5694-5707.
145. Paré D., Gaudreau H. Projection cells and interneurons of the lateral and basolateral amygdala: distinct firing patterns and differential relation to theta and delta rhythms in conscious cats. J. Neurosci. 1996, 16(10):3334-3350.
146. Paz R., Bauer E.P., Paré D. Theta synchronizes the activity of medial prefrontal neurons during learning. Learn Mem. 2008, 15(7):524-531.
147. Peck B.K., Vanderwolf C.H. Effects of raphe stimulation on hippocampal and neocortical activity and behaviour. Brain Res. 1991, 568(1-2):244-252.
148. Petrovich G.D., Risold P.Y., Swanson L.W. Organization of projections from the basomedial nucleus of the amygdala: a PHAL study in the rat. J. Comp. Neurol. 1996, 374(3):387-420.
149. 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. Electroencephalogr. Clin. Neurophysiol. 1962, 14:202-211.
150. Peyron C., Petit J.M., Rampon C., Jouvet M., Luppi P.H. Forebrain afferents to the rat dorsal raphe nucleus demonstrated by retrograde and anterograde tracing methods. Neuroscience 1998, 82(2):443-468.
151. Pikkarainen M., Rönkkö S., Savander V., Insausti R., Pitkänen A. Projections from the lateral, basal, and accessory basal nuclei of the amygdala to the hippocampal formation in rat. J. Comp. Neurol. 1999, 403(2):229-260.
152. Popa D., Duvarci S., Popescu A.T., Léna C., Paré D. Coherent amygdalocortical theta promotes fear memory consolidation during paradoxical sleep. Proc. Natl. Acad. Sci. USA 2010, 107(14):6516-6519.
153. Poulet J., Petersen C. Internal brain state regulates membrane potential synchrony in barrel cortex of behaving mice. Nature 2008.
154. Robinson T.E., Vanderwolf C.H. Electrical stimulation of the brain stem in freely moving rats: II. Effects on hippocampal and neocortical electrical activity, and relations to behavior. Exp. Neurol. 1978, 61(3):485-515.
155. Royer S., Sirota A., Patel J., Buzsáki G. Distinct representations and theta dynamics in dorsal and ventral hippocampus. J. Neurosci. 2010, 30(5):1777-1787.
156. Ryan P.J., Ma S., Olucha-Bordonau F.E., Gundlach A.L. Nucleus incertus - an emerging modulatory role in arousal, stress and memory. Neurosci. Biobehav. Rev. 2011, 35(6):1326-1341.
157. Rye D.B., Lee H.J., Saper C.B., Wainer B.H. Medullary and spinal efferents of the pedunculopontine tegmental nucleus and adjacent mesopontine tegmentum in the rat. J. Comp. Neurol. 1988, 269(3):315-341.
158. Rye D.B., Saper C.B., Lee H.J., Wainer B.H. Pedunculopontine tegmental nucleus of the rat: cytoarchitecture, cytochemistry, and some extrapyramidal connections of the mesopontine tegmentum. J. Comp. Neurol. 1987, 259(4):483-528.
159. Sabolek H.R., Penley S.C., Hinman J.R., Bunce J.G., Markus E.J., Escabi M., Chrobak J.J. Theta and gamma coherence along the septotemporal axis of the hippocampus. J. Neurophysiol. 2009, 101(3):1192-1200.
160. Saper C.B., Fuller P.M., Pedersen N.P., Lu J., Scammell T.E. Sleep state switching. Neuron 2010, 68(6):1023-1042.
161. Satoh K., Fibiger H.C. Cholinergic neurons of the laterodorsal tegmental nucleus: efferent and afferent connections. J. Comp. Neurol. 1986, 253(3):277-302.
162. Schmitz D., Gloveli T., Behr J., Dugladze T., Heinemann U. Subthreshold membrane potential oscillations in neurons of deep layers of the entorhinal cortex. Neuroscience 1998, 85(4):999-1004.
163. Seidenbecher T., Laxmi T.R., Stork O., Pape H.-C. Amygdalar and hippocampal theta rhythm synchronization during fear memory retrieval. Science 2003, 301(5634):846-850.
164. Semba K., Fibiger H.C. Afferent connections of the laterodorsal and the pedunculopontine tegmental nuclei in the rat: a retro- and antero-grade transport and immunohistochemical study. J. Comp. Neurol. 1992, 323(3):387-410.
165. Semba K., Reiner P.B., Fibiger H.C. Single cholinergic mesopontine tegmental neurons project to both the pontine reticular formation and the thalamus in the rat. Neuroscience 1990, 38(3):643-654.
166. Sesack S.R., Deutch A.Y., Roth R.H., Bunney B.S. Topographical organization of the efferent projections of the medial prefrontal cortex in the rat: an anterograde tract-tracing study with Phaseolus vulgaris leucoagglutinin. J. Comp. Neurol. 1989, 290(2):213-242.
167. Sesack S.R., Hawrylak V.A., Matus C., Guido M.A., Levey A.I. Dopamine axon varicosities in the prelimbic division of the rat prefrontal cortex exhibit sparse immunoreactivity for the dopamine transporter. J. Neurosci. 1998, 18(7):2697-2708.
168. Shiromani P.J., Armstrong D.M., Gillin J.C. Cholinergic neurons from the dorsolateral pons project to the medial pons: a WGA-HRP and choline acetyltransferase immunohistochemical study. Neurosci. Lett. 1988, 95(1-3):19-23.
169. Siapas A.G., Lubenov E.V., Wilson M.A. Prefrontal phase locking to hippocampal theta oscillations. Neuron 2005, 46(1):141-151.
170. Sik A., Penttonen M., Buzsáki G. Interneurons in the hippocampal dentate gyrus: an in vivo intracellular study. Eur. J. Neurosci. 1997, 9(3):573-588.
171. Sirota A., Montgomery S., Fujisawa S., Isomura Y., Zugaro M., Buzsáki G. Entrainment of neocortical neurons and gamma oscillations by the hippocampal theta rhythm. Neuron 2008, 60(4):683-697.
172. Skinner R.D., Garcia-Rill E. The mesencephalic locomotor region (MLR) in the rat. Brain Res. 1984, 323(2):385-389.
173. Sparks P.D., LeDoux J.E. Septal lesions potentiate freezing behavior to contextual but not to phasic conditioned stimuli in rats. Behav. Neurosci. 1995, 109(1):184-188.
174. Steinbusch H.W., Nieuwenhuys R. Localization of serotonin-like immunoreactivity in the central nervous system and pituitary of the rat, with special references to the innervation of the hypothalamus. Adv. Exp. Med. Biol. 1981, 133:7-35.
175. Steininger T.L., Rye D.B., Wainer B.H. Afferent projections to the cholinergic pedunculopontine tegmental nucleus and adjacent midbrain extrapyramidal area in the albino rat. I. Retrograde tracing studies. J. Comp. Neurol. 1992, 321(4):515-543.
176. Steriade M., Datta S., Paré D., Oakson G., Curró Dossi R.C. Neuronal activities in brain-stem cholinergic nuclei related to tonic activation processes in thalamocortical systems. J. Neurosci. 1990, 10(8):2541-2559.
177. Stewart M., Quirk G.J., Barry M., Fox S.E. Firing relations of medial entorhinal neurons to the hippocampal theta rhythm in urethane anesthetized and walking rats. Exp. Brain Res. Experimentelle Hirnforschung Expérimentation cérébrale 1992, 90(1):21-28.
178. Su H.S., Bentivoglio M. Thalamic midline cell populations projecting to the nucleus accumbens, amygdala, and hippocampus in the rat. J. Comp. Neurol. 1990, 297(4):582-593.
179. Swanson L.W. A direct projection from Ammon's horn to prefrontal cortex in the rat. Brain Res. 1981, 217(1):150-154.
180. Thinschmidt J.S., Kinney G.G., Kocsis B. The supramammillary nucleus: is it necessary for the mediation of hippocampal theta rhythm?. Neuroscience 1995, 67(2):301-312.
181. Tóth K., Borhegyi Z., Freund T.F. Postsynaptic targets of GABAergic hippocampal neurons in the medial septum-diagonal band of broca complex. J. Neurosci. 1993, 13(9):3712-3724.
182. Tóth K., Freund T.F., Miles R. Disinhibition of rat hippocampal pyramidal cells by GABAergic afferents from the septum. J. Physiol. (Lond.) 1997, 500(Pt. 2):463-474.
183. Tsujimoto T., Shimazu H., Isomura Y. Direct recording of theta oscillations in primate prefrontal and anterior cingulate cortices. J. Neurophysiol. 2006, 95(5):2987-3000.
184. van der Meer M.A.A., Redish A.D. Theta phase precession in rat ventral striatum links place and reward information. J. Neurosci. 2011, 31(8):2843-2854.
185. Van der Werf Y.D., Witter M.P., Groenewegen H.J. The intralaminar and midline nuclei of the thalamus. Anatomical and functional evidence for participation in processes of arousal and awareness. Brain Res. Brain Res. Rev. 2002, 39(2-3):107-140.
186. Van Groen T., Miettinen P., Kadish I. The entorhinal cortex of the mouse: organization of the projection to the hippocampal formation. Hippocampus 2003, 13(1):133-149.
187. Vanderwolf C.H. Hippocampal electrical activity and voluntary movement in the rat. Electroencephalogr. Clin. Neurophysiol. 1969, 26(4):407-418.
188. Vann S.D., Aggleton J.P. The mammillary bodies: two memory systems in one?. Nat. Rev. Neurosci. 2004, 5(1):35-44.
189. Varga V., Hangya B., Kránitz K., Ludányi A., Zemankovics R., Katona I., Shigemoto R., Freund T.F., Borhegyi Z. The presence of pacemaker HCN channels identifies theta rhythmic GABAergic neurons in the medial septum. J. Physiol. (Lond.) 2008, 586(16):3893-3915.
190. Vertes R.P. Selective firing of rat pontine gigantocellular neurons during movement and REM sleep. Brain Res. 1977, 128(1):146-152.
191. Vertes R.P. Brain stem gigantocellular neurons: patterns of activity during behavior and sleep in the freely moving rat. J. Neurophysiol. 1979, 42(1 Pt. 1):214-228.
192. Vertes R.P. A PHA-L analysis of ascending projections of the dorsal raphe nucleus in the rat. J. Comp. Neurol. 1991, 313(4):643-668.
193. Vertes R.P. PHA-L analysis of projections from the supramammillary nucleus in the rat. J. Comp. Neurol. 1992, 326(4):595-622.
194. Vertes R.P. Analysis of projections from the medial prefrontal cortex to the thalamus in the rat, with emphasis on nucleus reuniens. J. Comp. Neurol. 2002, 442(2):163-187.
195. Vertes R.P., Albo Z., Viana Di Prisco G. Theta-rhythmically firing neurons in the anterior thalamus: implications for mnemonic functions of Papez's circuit. Neuroscience 2001, 104(3):619-625.
196. Vertes R.P., Crane A.M., Colom L.V., Bland B.H. Ascending projections of the posterior nucleus of the hypothalamus: PHA-L analysis in the rat. J. Comp. Neurol. 1995, 359(1):90-116.
197. Vertes R.P., Hoover W.B., Do Valle A.C., Sherman A., Rodriguez J.J. Efferent projections of reuniens and rhomboid nuclei of the thalamus in the rat. J. Comp. Neurol. 2006, 499(5):768-796.
198. Vertes R.P., Hoover W.B., Szigeti-Buck K., Leranth C. Nucleus reuniens of the midline thalamus: link between the medial prefrontal cortex and the hippocampus. Brain Res. Bull. 2007, 71(6):601-609.
199. Vertes R.P., Kocsis B. Brainstem-diencephalo-septohippocampal systems controlling the theta rhythm of the hippocampus. Neuroscience 1997, 81(4):893-926.
200. Vertes R.P., Martin G.F., Waltzer R. An autoradiographic analysis of ascending projections from the medullary reticular formation in the rat. Neuroscience 1986, 19(3):873-898.
201. Wang W.-T., Wan Y.-H., Zhu J.-L., Lei G.-S., Wang Y.-Y., Zhang P., Hu S.-J. Theta-frequency membrane resonance and its ionic mechanisms in rat subicular pyramidal neurons. Neuroscience 2006, 140(1):45-55.
202. Winson J. Loss of hippocampal theta rhythm results in spatial memory deficit in the rat. Science 1978, 201(4351):160-163.
203. Woodnorth M.-A., Kyd R.J., Logan B.J., Long M.A., McNaughton N. Multiple hypothalamic sites control the frequency of hippocampal theta rhythm. Hippocampus 2003, 13(3):361-374.
204. Woolf N.J., Butcher L.L. Cholinergic systems in the rat brain: III. Projections from the pontomesencephalic tegmentum to the thalamus, tectum, basal ganglia, and basal forebrain. Brain Res. Bull. 1986, 16(5):603-637.
205. Wouterlood F.G., Aliane V., Boekel A.J., Hur E.E., Zaborszky L., Barroso-Chinea P., Härtig W., Lanciego J.L., Witter M.P. Origin of calretinin-containing, vesicular glutamate transporter 2-coexpressing fiber terminals in the entorhinal cortex of the rat. J. Comp. Neurol. 2008, 506(2):359-370.
206. Wyble B.P., Hyman J.M., Rossi C.A., Hasselmo M.E. Analysis of theta power in hippocampal EEG during bar pressing and running behavior in rats during distinct behavioral contexts. Hippocampus 2004, 14(5):662-674.
207. 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(1):78-90.
208. Yoder R.M., Pang K.C.H. Involvement of GABAergic and cholinergic medial septal neurons in hippocampal theta rhythm. Hippocampus 2005, 15(3):381-392.
209. Zaborszky L., Buhl D.L., Pobalashingham S., Bjaalie J.G., Nadasdy Z. Three-dimensional chemoarchitecture of the basal forebrain: spatially specific association of cholinergic and calcium binding protein-containing neurons. Neuroscience 2005, 136(3):697-713.
210. Zhang H., Lin S.-C., Nicolelis M.A.L. Spatiotemporal coupling between hippocampal acetylcholine release and theta oscillations in vivo. J. Neurosci. 2010, 30(40):13431-13440.
211. Ziegler D.R., Cullinan W.E., Herman J.P. Distribution of vesicular glutamate transporter mRNA in rat hypothalamus. J. Comp. Neurol. 2002, 448(3):217-229.