Rola obszaru tylnego podwzgórza w generowaniu rytmu theta

ARTYKUŁ PRZEGLĄDOWY

Rola obszaru tylnego podwzgórza w generowaniu rytmu theta

Agata Staszelis 1 , Tomasz Kowalczyk 1

1. Katedra Neurobiologii, Wydział Biologii i Ochrony Środowiska, Uniwersytet Łódzki, Łódź

Opublikowany: 2021-06-15
DOI: 10.5604/01.3001.0014.9333
GICID: 01.3001.0014.9333
Dostępne wersje językowe: pl en
Wydanie: Postepy Hig Med Dosw 2021; 75 : 406-416

 

Abstrakt

Rytm theta jest jednym z najlepiej zsynchronizowanych wzorców aktywności oscylacyjnej rejestrowanych w mózgach ssaków. U ludzi, rytm ten obserwowany jest podczas snu REM, nawigacji przestrzennej, procesów pamięciowych, analitycznych oraz językowych. Może być również traktowany jako nieswoisty marker stanów patologicznych ośrodkowego układu nerwowego, takich jak choroba Alzheimera czy padaczka. Główną strukturą zaangażowaną w generowanie wzorca aktywności bioelektrycznej, zarówno u ludzi, jak i u gryzoni (najczęściej badanych zwierząt laboratoryjnych), jest formacja hipokampa. Jej funkcjonowanie zależy od współdziałania wielu innych struktur układu nerwowego. Jedną z nich jest obszar tylnego podwzgórza, który jest istotnym elementem układów neuronalnych modulujących zdolność formacji hipokampa do generowania rytmu theta. Przedstawione w artykule wyniki badań podkreślają rolę obszaru tylnego podwzgórza, jako modulatora hipokampalnego rytmu theta, ale wykazują również, że obszar ten jest zdolny do samodzielnego, niezależnego od wpływu innych struktur, generowania rytmicznej aktywności theta.

Przypisy

  • 1. Anderson K.L., Rajagovindan R., Ghacibeh G.A., Meador K.J., DingM.: Theta oscillations mediate interaction between prefrontal cortexand medial temporal lobe in human memory. Cereb. Cortex, 2010;20: 1604-1612
    Google Scholar
  • 2. Bastiaansen M., Hagoort P.: Oscillatory neuronal dynamics duringlanguage comprehension. W: Progress in Brain Research. red.: C.Neuper, W. Klimesch. Elsevier, 2006; 179-196
    Google Scholar
  • 3. Bland B.H.: The physiology and pharmacology of hippocampalformation theta rhythms. Prog. Neurobiol., 1986; 26: 1-54
    Google Scholar
  • 4. Bland B.H., Declerck S., Jackson J., Glasgow S., Oddie S.: Septohippocampalproperties of N-methyl-D-aspartate-induced theta-bandoscillation and synchrony. Synapse, 2007; 61: 185-197
    Google Scholar
  • 5. Bland B.H., Colom L.V.: Extrinsic and intrinsic properties underlyingoscillation and synchrony in limbic cortex. Prog. Neurobiol.,1993; 41: 157-208
    Google Scholar
  • 6. Bland B.H., Colom L.V., Ford R.D.: Responses of septal θ-on and θ-offcells to activation of the dorsomedial-posterior hypothalamic region.Brain Res. Bull., 1990; 24: 71-79
    Google Scholar
  • 7. Bland B.H., Konopacki J., Kirk I.J., Oddie S.D., Dickson C.T.: Dischargepatterns of hippocampal theta-related cells in the caudal diencephalonof the urethan-anesthetized rat. J. Neurophysiol., 1995; 74: 322-333
    Google Scholar
  • 8. Bland B.H., Oddie S.D.: Theta band oscillation and synchrony inthe hippocampal formation and associated structures: The case for itsrole in sensorimotor integration. Behav. Brain Res., 2001; 127: 119-136
    Google Scholar
  • 9. Bland B.H., Oddie S.D.: Anatomical, electrophysiological and pharmacologicalstudies of ascending brainstem hippocampal synchronizingpathways. Neurosci. Biobehav. Rev., 1998; 22: 259-273
    Google Scholar
  • 10. Bland B.H., Oddie S.D., Colom L.V.: Mechanisms of neural synchronyin the septohippocampal pathways underlying hippocampaltheta generation. J. Neurosci., 1999; 19: 3223-3237
    Google Scholar
  • 11. Bland B.H., Trepel C., Oddie S.D., Kirk I.J.: Intraseptal microinfusionof muscimol: Effects on hippocampal formation theta field activityand phasic theta-ON cell discharges. Exp. Neurol., 1996; 138: 286-297
    Google Scholar
  • 12. Bland B.H., Vanderwolf C.H.: Diencephalic and hippocampal mechanismsof motor activity in the rat: Effects of posterior hypothalamicstimulation on behavior and hippocampal slow wave activity. BrainRes., 1972; 43: 67-88
    Google Scholar
  • 13. Bocian R., Caban B., Kłos-Wojtczak P., Konopacki J., Kowalczyk T.:Is electrical coupling involved in the generation of posterior hypothalamictheta rhythm? Eur. J. Neurosci., 2016; 44: 2324-2333
    Google Scholar
  • 14. Bocian R., Kłos-Wojtczak P., Caban B., Kowalczyk T., KaźmierskaP., Konopacki J.: Cell discharge correlates of posterior hypothalamictheta rhythm recorded in anesthetized rats and brain slices. Hippocampus,2016; 26: 1354-1369
    Google Scholar
  • 15. Borhegyi Z., Freund T.F.: Dual projection from the medial septumto the supramammillary nucleus in the rat. Brain Res. Bull., 1998;46: 453-459
    Google Scholar
  • 16. Borhegyi Z., Maglóczky Z., Acsády L., Freund T.F.: The supramammillarynucleus innervates cholinergic and GABAergic neurons inthe medial septum-diagonal band of Broca complex. Neuroscience,1998; 82: 1053-1065
    Google Scholar
  • 17. Bódizs R., Kántor S., Szabó G., Szûcs A., Erõss L., Halász P.: Rhythmichippocampal slow oscillation characterizes REM sleep in humans.Hippocampus, 2001; 11: 747-753
    Google Scholar
  • 18. Buzsáki G.: Theta oscillations in the hippocampus. Neuron, 2002;33: 325-340
    Google Scholar
  • 19. Caban B., Staszelis A., Kazmierska P., Kowalczyk T., Konopacki J.:Postnatal development of the posterior hypothalamic theta rhythmand local cell discharges in rat brain slices. Dev. Neurobiol., 2018; 78:1049-1063
    Google Scholar
  • 20. Carnes M., Lent S., Feyzi J., Hazel D.: Plasma adrenocorticotropichormone in the rat demonstrates three different rhythms within 24h. Neuroendocrinology, 1989; 50: 17-25
    Google Scholar
  • 21. Coleman J.R., Lindsley D.B.: Behavioral and hippocampal electricalchanges during operant learning in cats and effects of stimulatingtwo hypothalamic-hippocampal systems. Electroencephalogr. Clin.Neurophysiol., 1977; 42: 309-331
    Google Scholar
  • 22. Colgin L.L.: Rhythms of the hippocampal network. Nat. Rev. Neurosci.,2016; 17: 239-249
    Google Scholar
  • 23. Colom L.V.: Septal networks: Relevance to theta rhythm, epilepsyand Alzheimer’s disease. J. Neurochem., 2006; 96: 609-623
    Google Scholar
  • 24. Colom L.V., Bland B.H.: State-dependent spike train dynamics ofhippocampal formation neurons: Evidence for theta-on and theta-offcells. Brain Res., 1987; 422: 277-286
    Google Scholar
  • 25. Datta S., Siwek D.F.: Excitation of the brain stem pedunculopontinetegmentum cholinergic cells induces wakefulness and REM sleep. J.Neurophysiol., 1997; 77: 2975-2988
    Google Scholar
  • 26. Dickson C.T., Kirk I.J., Oddie S.D., Bland B.H.: Classification of thetarelatedcells in the entorhinal cortex: Cell discharges are controlledby the ascending brainstem synchronizing pathway in parallel withhippocampal theta-related cells. Hippocampus, 1995; 5: 306-319
    Google Scholar
  • 27. Dickson C.T., Trepel C., Bland B.H.: Extrinsic modulation of thetafield activity in the entorhinal cortex of the anesthetized rat. Hippocampus,1994; 4: 37-51
    Google Scholar
  • 28. Dietl H., Prast H., Philippu A.: Pulsatile release of catecholaminesin the hypothalamus of conscious rats. Naunyn. Schmiedebergs Arch.Pharmacol., 1993; 347: 28-33
    Google Scholar
  • 29. Dunkley B.T., Sedge P.A., Doesburg S.M., Grodecki R.J., Jetly R.,Shek P.N., Taylor M.J., Pang E.W.: Theta, mental flexibility, and posttraumaticstress disorder: Connecting in the parietal cortex. PLoSOne, 2015; 10: e0123541
    Google Scholar
  • 30. Ekstrom A.D., Caplan J.B., Ho E., Shattuck K., Fried I., Kahana M.J.:Human hippocampal theta activity during virtual navigation. Hippocampus,2005; 15: 881-889
    Google Scholar
  • 31. Elazar Z., Adey W.R.: Electroencephalographic correlates of learningin subcortical and cortical structures. Electroencephalogr. Clin.Neurophysiol., 1967; 23: 306-319
    Google Scholar
  • 32. Gallego-Jutglà E., Solé-Casals J., Vialatte F.B., Dauwels J., CichockiA.: A theta-band EEG based index for early diagnosis of Alzheimer’sdisease. J. Alzheimers Dis., 2015; 43: 1175-1184
    Google Scholar
  • 33. Gärtner M., Rohde-Liebenau L., Grimm S., Bajbouj M.: Workingmemory-related frontal theta activity is decreased under acute stress.Psychoneuroendocrinology, 2014; 43: 105-113
    Google Scholar
  • 34. Glin L., Zernicki B., Gottesmann C.: Hippocampal and corticalEEG activity in rats with transected hypothalamus. Brain Res. Bull.,1991; 27: 637-640
    Google Scholar
  • 35. Gołebiewski H., Eckersdorf B., Konopacki J.: Cholinergic/GABAergicinteraction in the production of EEG theta oscillations in rat hippocampalformation in vitro. Acta Neurobiol. Exp., 1996; 56: 147-153
    Google Scholar
  • 36. Grass K., Prast H., Philippu A.: Ultradian rhythm in the delta andtheta frequency bands of the EEG in the posterior hypothalamus ofthe rat. Neurosci. Lett., 1995; 191: 161-164
    Google Scholar
  • 37. Gray J.A., McNaughton N.: The Neuropsychology of Anxiety: Anenquiry into the function of the septo-hippocampal system. OxfordUniversity Press, 2003
    Google Scholar
  • 38. Green J.D., Maxwell D.S., Schindler W.J., Stumpf C.: Rabbit eeg„theta” rhythm: Its anatomical source and relation to activity in singleneurons. J. Neurophysiol., 1960; 23: 403-420
    Google Scholar
  • 39. Hata T., Nishimura Y., Kita T., Kawabata A., Itoh E.: Electrocorticogramin rats loaded with SART stress (repeated cold stress). Jpn. J.Pharmacol., 1987; 45: 365-372
    Google Scholar
  • 40. Huerta P.T., Lisman J.E.: Bidirectional synaptic plasticity inducedby a single burst during cholinergic theta oscillation in CA1 in vitro.Neuron, 1995; 15: 1053-1063
    Google Scholar
  • 41. Huerta P.T., Lisman J.E.: Synaptic plasticity during the cholinergictheta-frequency oscillation in vitro. Hippocampus, 1996; 6: 58-61
    Google Scholar
  • 42. Jellinck P.H., Monder C., McEwen B.S., Sakai R.R.: Differential inhibitionof 11 beta-hydroxysteroid dehydrogenase by carbenoxolonein rat brain regions and peripheral tissues. J. Steroid Biochem. Mol.Biol., 1993; 46: 209-213
    Google Scholar
  • 43. Kawakami M., Kimura F., Tsai C.W.: Relationship between thethree-hour-period sleep-wakefulness cycle and growth hormone secretionin the immature rat. J. Physiol., 1984; 348: 271-283
    Google Scholar
  • 44. Kawamura H., Domino E.F.: Hippocampal slow („arousal”) waveactivation in the rostral midbrain transected cat. Electroencephalogr.Clin. Neurophysiol., 1968; 25: 471-480
    Google Scholar
  • 45. Kawamura H., Nakamura Y., Tokizane T.: Effect of acute brain stemlesions on the electrical activities of the limbic system and neocortex.Jpn. J. Physiol., 1961; 11: 564-575
    Google Scholar
  • 46. Kirk I.J.: Supramammillary neural discharge patterns and hippocampalEEG. Brain Res. Bull., 1997; 42: 23-26
    Google Scholar
  • 47. Kirk I.J.: Frequency modulation of hippocampal theta by the supramammillarynucleus, and other hypothalamo–hippocampal interactions:Mechanisms and functional implications. Neurosci. Biobehav.Rev., 1998; 22: 291-302
    Google Scholar
  • 48. Kirk I.J., McNaughton N.: Mapping the differential effects of procaineon frequency and amplitude of reticularly elicited hippocampalrhythmical slow activity. Hippocampus, 1993; 3: 517-525
    Google Scholar
  • 49. Kirk I.J., McNaughton N.: Supramammillary cell firing and hippocampalrhythmical slow activity. Neuroreport, 1991; 2: 723-725
    Google Scholar
  • 50. Kirk I.J., Oddie S.D., Konopacki J., Bland B.H.: Evidence for differentialcontrol of posterior hypothalamic, supramammillary, andmedial mammillary theta-related cellular discharge by ascending anddescending pathways. J. Neurosci., 1996; 16: 5547-5554
    Google Scholar
  • 51. Kiss J., Csáki A., Bokor H., Kocsis K., Kocsis B.: Possible glutamatergic/aspartatergic projections to the supramammillary nucleus andtheir origins in the rat studied by selective [(3)H]D-aspartate labellingand immunocytochemistry. Neuroscience, 2002; 111: 671-691
    Google Scholar
  • 52. Kiss J., Csáki A., Bokor H., Shanabrough M., Leranth C.: The supramammillo-hippocampal and supramammillo-septal glutamatergic/aspartatergic projections in the rat: A combined [3H]D-aspartateautoradiographic and immunohistochemical study. Neuroscience,2000; 97: 657-669
    Google Scholar
  • 53. Kocsis B.: The effect of descending theta rhythmic input from theseptohippocampal system on firing in the supramammillary nucleus.Brain Res., 2006; 1086: 92-97
    Google Scholar
  • 54. Kocsis B., Kaminski M.: Dynamic changes in the direction of thetheta rhythmic drive between supramammillary nucleus and the septohippocampalsystem. Hippocampus, 2006; 16: 531-540
    Google Scholar
  • 55. Kocsis B., Vertes R.P.: Characterization of neurons of the supramammillarynucleus and mammillary body that discharge rhythmicallywith the hippocampal theta rhythm in the rat. J. Neurosci.,1994; 14: 7040-7052
    Google Scholar
  • 56. Kocsis B., Vertes R.P.: Phase relations of rhythmic neuronal firingin the supramammillary nucleus and mammillary body to the hippocampaltheta activity in urethane anesthetized rats. Hippocampus,1997; 7: 204-214
    Google Scholar
  • 57. Komisaruk B.R.: Synchrony between limbic system theta activityand rhythmical behavior in rats. J. Comp. Physiol. Psychol., 1970;70: 482-492
    Google Scholar
  • 58. Konopacki J., Eckersdorf B., Kowalczyk T., Gołebiewski H.: Firingcell repertoire during carbachol-induced theta rhythm in rat hippocampalformation slices. Eur. J. Neurosci., 2006; 23: 1811-1818
    Google Scholar
  • 59. Konopacki J., MacIver M.B., Bland B.H., Roth S.H.: CarbacholinducedEEG „theta” activity in hippocampal brain slices. Brain Res.,1987; 405: 196-198
    Google Scholar
  • 60. Kowalczyk T., Bocian R., Caban B., Konopacki J.: Atropine-sensitivetheta rhythm in the posterior hypothalamic area: In vivo and in vitrostudies. Hippocampus, 2014; 24: 7-20
    Google Scholar
  • 61. Kowalczyk T., Bocian R., Konopacki J.: The generation of thetarhythm in hippocampal formation maintained in vitro. Eur. J. Neurosci.,2013; 37: 679-699
    Google Scholar
  • 62. Kowalczyk T., Konopacki J.: Depth amplitude and phase profilesof carbachol-induced theta in hippocampal formation slices. BrainRes. Bull., 2002; 58: 569-574
    Google Scholar
  • 63. Kowalczyk T., Konopacki J., Bocian R., Caban B.: Theta-relatedgating cells in hippocampal formation: in vivo and in vitro study.Hippocampus, 2013; 23: 30-39
    Google Scholar
  • 64. Kramis R., Vanderwolf C.H., Bland B.H.: Two types of hippocampalrhythmical slow activity in both the rabbit and the rat: Relations tobehavior and effects of atropine, diethyl ether, urethane, and pentobarbital.Exp. Neurol., 1975; 49: 58-85
    Google Scholar
  • 65. Lega B.C., Jacobs J., Kahana M.: Human hippocampal theta oscillationsand the formation of episodic memories. Hippocampus,2012; 22: 748-761
    Google Scholar
  • 66. Leranth C., Carpi D., Buzsaki G., Kiss J.: The entorhino-septosupramammillarynucleus connection in the rat: Morphological basisof a feedback mechanism regulating hippocampal theta rhythm.Neuroscience, 1999; 88: 701-718
    Google Scholar
  • 67. Leung L.S.: Generation of theta and gamma rhythms in the hippocampus.Neurosci. Biobehav. Rev., 1998; 22: 275-290
    Google Scholar
  • 68. Maglóczky Z., Acsády L., Freund T.F.: Principal cells are the postsynaptictargets of supramammillary afferents in the hippocampusof the rat. Hippocampus, 1994; 4: 322-334
    Google Scholar
  • 69. McNaughton N., Logan B., Panickar K.S., Kirk I.J., Pan W.X., BrownN.T., Heenan A.: Contribution of synapses in the medial supramammillarynucleus to the frequency of hippocampal theta rhythm in freelymoving rats. Hippocampus, 1995; 5: 534-545
    Google Scholar
  • 70. Mitchell D.J., McNaughton N., Flanagan D., Kirk I.J.: Frontal-midlinetheta from the perspective of hippocampal „theta”. Prog. Neurobiol.,2008; 86: 156-185
    Google Scholar
  • 71. Nishida M., Pearsall J., Buckner R.L., Walker M.P.: REM sleep, prefrontaltheta, and the consolidation of human emotional memory.Cereb. Cortex, 2009; 19: 1158-1166
    Google Scholar
  • 72. Nuñez A., Cervera-Ferri A., Olucha-Bordonau F., Ruiz-Torner A.,Teruel V.: Nucleus incertus contribution to hippocampal theta rhythmgeneration. Eur. J. Neurosci., 2006; 23: 2731-2738
    Google Scholar
  • 73. Oddie S.D., Bland B.H., Colom L.V., Vertes R.P.: The midline posteriorhypothalamic region comprises a critical part of the ascendingbrainstem hippocampal synchronizing pathway. Hippocampus,1994; 4: 454-473
    Google Scholar
  • 74. Pan W.X., McNaughton N.: The medial supramammillary nucleus,spatial learning and the frequency of hippocampal theta activity. BrainRes., 1997; 764: 101-108
    Google Scholar
  • 75. Pan W.X., McNaughton N.: The supramammillary area: Its organization,functions and relationship to the hippocampus. Prog.Neurobiol., 2004; 74: 127-166
    Google Scholar
  • 76. Pan W.X., McNaughton N.: The role of the medial supramammillarynucleus in the control of hippocampal theta activity and behaviorin rats. Eur. J. Neurosci., 2002; 16: 1797-1809
    Google Scholar
  • 77. Parker S.M., Sinnamon H.M.: Forward locomotion elicited byelectrical stimulation in the diencephalon and mesencephalon of theawake rat. Physiol. Behav., 1983; 31: 581-587
    Google Scholar
  • 78. Pignatelli M., Beyeler A., Leinekugel X.: Neural circuits underlyingthe generation of theta oscillations. J. Physiol. Paris, 2012; 106: 81-92
    Google Scholar
  • 79. Plotsky P.M., Cunningham E.T.Jr., Widmaier E.P.: Catecholaminergicmodulation of corticotropin-releasing factor and adrenocorticotropinsecretion. Endocr. Rev., 1989; 10: 437-458
    Google Scholar
  • 80. Robinson T.E., Whishaw I.Q.: Effects of posterior hypothalamic lesionson voluntary behavior and hippocampal electroencephalogramsin the rat. J. Comp. Physiol. Psychol., 1974; 86: 768-786
    Google Scholar
  • 81. Shahidi S., Motamedi F., Naghdi N.: Effect of reversible inactivationof the supramammillary nucleus on spatial learning and memoryin rats. Brain Res., 2004; 1026: 267-274
    Google Scholar
  • 82. Sieb R.A.: A brain mechanism for attention. Med. Hypotheses,1990; 33: 145-153
    Google Scholar
  • 83. Sinnamon H.M.: Locomotor stepping elicited by electrical stimulationof the hypothalamus persists after lesion of descending fibersof passage. Physiol. Behav., 1990; 48: 261-266
    Google Scholar
  • 84. Siwek M.E., Müller R., Henseler C., Trog A., Lundt A., Wormuth C.,Broich K., Ehninger D., Weiergräber M., Papazoglou A.: Altered thetaoscillations and aberrant cortical excitatory activity in the 5XFADmodel of Alzheimer’s disease. Neural Plast., 2015; 2015: 781731
    Google Scholar
  • 85. Sławińska U., Kasicki S.: Theta-like rhythm in depth EEG activityof hypothalamic areas during spontaneous or electrically inducedlocomotion in the rat. Brain Res., 1995; 678: 117-126
    Google Scholar
  • 86. Sławińska U., Kasicki S.: The frequency of rat’s hippocampal thetarhythm is related to the speed of locomotion. Brain Res., 1998; 796:327-331
    Google Scholar
  • 87. Sziklas V., Petrides M.: Memory impairment following lesions tothe mammillary region of the rat. Eur. J. Neurosci., 1993; 5: 525-540
    Google Scholar
  • 88. Thinschmidt J.S., Kinney G.G., Kocsis B.: The supramammillary nucleus:Is it necessary for the mediation of hippocampal theta rhythm?Neuroscience, 1995; 67: 301-312
    Google Scholar
  • 89. Trojniar W., Jurkowlaniec E., Orzeł-Gryglewska J., Tokarski J.: Theeffect of lateral hypothalamic lesions on spontaneous EEG pattern inrats. Acta Neurobiol. Exp., 1987; 47: 27-43
    Google Scholar
  • 90. Vanderwolf C.H.: Hippocampal electrical activity and voluntarymovement in the rat. Electroencephalogr. Clin. Neurophysiol., 1969;26: 407-418
    Google Scholar
  • 91. Vanderwolf C.H.: An Odyssey Through the Brain, Behavior andthe Mind. Springer US, 2003
    Google Scholar
  • 92. Vanderwolf C.H., Baker G.B.: Evidence that serotonin mediatesnon-cholinergic neocortical low voltage fast activity, non-cholinergichippocampal rhythmical slow activity and contributes to intelligentbehavior. Brain Res., 1986; 374: 342-356
    Google Scholar
  • 93. Vertes R.P.: PHA-L analysis of projections from the supramammillarynucleus in the rat. J. Comp. Neurol., 1992; 326: 595-622
    Google Scholar
  • 94. Vertes R.P., Crane A.M., Colom L.V., Bland B.H.: Ascending projectionsof the posterior nucleus of the hypothalamus: PHA-L analysis inthe rat. J. Comp. Neurol., 1995; 359: 90-116
    Google Scholar
  • 95. Vertes R.P., Kocsis B.: Brainstem-diencephalo-septohippocampalsystems controlling the theta rhythm of the hippocampus. Neuroscience,1997; 81: 893-926
    Google Scholar
  • 96. Vertes R.P., Martin G.F.: Autoradiographic analysis of ascendingprojections from the pontine and mesencephalic reticular formationand the median raphe nucleus in the rat. J. Comp. Neurol., 1988;275: 511-541
    Google Scholar
  • 97. Vertes R.P., McKenna J.T.: Collateral projections from the supramammillarynucleus to the medial septum and hippocampus.Synapse, 2000; 38: 281-293
    Google Scholar
  • 98. Wang X.J.: Neurophysiological and computational principles ofcortical rhythms in cognition. Physiol. Rev., 2010; 90: 1195-1268
    Google Scholar
  • 99. Winson J.: Loss of hippocampal theta rhythm results in spatialmemory deficit in the rat. Science, 1978; 201: 160-163
    Google Scholar
  • 100. Woodnorth M.A., Kyd R.J., Logan B.J., Long M.A., McNaughtonN.: Multiple hypothalamic sites control the frequency of hippocampaltheta rhythm. Hippocampus, 2003; 13: 361-374
    Google Scholar
  • 101. Woodnorth M.A., McNaughton N.: Different systems in the posteriorhypothalamic nucleus of rats control theta frequency and triggermovement. Behav. Brain Res., 2005; 163: 107-114
    Google Scholar
  • 102. Woodnorth M.A., McNaughton N.: Benzodiazepine receptorsin the medial-posterior hypothalamus mediate the reduction of hippocampaltheta frequency by chlordiazepoxide. Brain Res., 2002; 954:194-201
    Google Scholar
  • 103. Yoder R.M., Pang K.C.: Involvement of GABAergic and cholinergicmedial septal neurons in hippocampal theta rhythm. Hippocampus,2005; 15: 381-392
    Google Scholar

Pełna treść artykułu

Przejdź do treści