Hippocampal theta rhythm: A tag for short-term memory

Hippocampus

Volumn 15, Issue 7, 2005, Pages 923-935

  Vertes, Robert P ^a  

^a FLORIDA ATLANTIC UNIVERSITY   (United States)

Author keywords

Heterosynaptic plasticity; Homosynaptic plasticity; Long term potentiation; Median raphe nucleus; NMDA receptors; Supramammillary nucleus

Indexed keywords

GLUTAMIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

BRAIN CORTEX; BRAIN FUNCTION; BRAIN STEM; CORTICAL SYNCHRONIZATION; DIENCEPHALON; EXPLORATORY BEHAVIOR; HIPPOCAMPUS; HIPPOCAMPUS THETA RHYTHM; HUMAN; LOCOMOTION; LONG TERM MEMORY; LONG TERM POTENTIATION; MAMMAL; MEMORY CONSOLIDATION; NERVE CELL MEMBRANE STEADY POTENTIAL; NONHUMAN; POSTSYNAPTIC MEMBRANE; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PUNISHMENT; REINFORCEMENT; REVIEW; REWARD; SENSORY STIMULATION; SEPTUM PELLUCIDUM; SHORT TERM MEMORY; SIGNAL TRANSDUCTION; THALAMOCORTICAL TRACT;

AFFERENT PATHWAYS; ANIMALS; BRAIN STEM; EXPLORATORY BEHAVIOR; HIPPOCAMPUS; HUMANS; LONG-TERM POTENTIATION; MEMORY, SHORT-TERM; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPTIC TRANSMISSION; THETA RHYTHM;

EID: 27644517889     PISSN: 10509631     EISSN: None     Source Type: Journal    
DOI: 10.1002/hipo.20118     Document Type: Review

References (138)

1. Aghajanian GK, Foote WE, Sheard MH. 1968. Lysergic acid diethylamide sensitive neuronal units in midbrain raphe: Science 161:706-708.
2. Aghajanian GK, Foote WE, Sheard MH. 1970. Action of psychotogenic drugs on single midbrain raphe neurons. J Pharmacol Exp Ther 171:178-187.
3. Asaka Y, Griffin AL, Berry SD. 2002. Reversible septal inactivation disrupts hippocampal slow-wave and unit activity and impairs trace conditioning in rabbits (Oryctolagus cuniculus). Behav Neurosci 116:434-442.
4. Assaf SY, Miller JJ. 1978. Role of a raphe serotonin system in control of septal unit activity and hippocampal desynchronization. Neuroscience 3:539-550.
5. Bach ME, Hawkins RD, Osman M, Kandel ER, Mayford M. 1995. Impairment of spatial but not contextual memory in CaMKII mutant mice with a selective loss of hippocampal LTP in the range of the theta frequency. Cell 81:905-915.
6. Baddeley A. 1986. Working memory. Oxford: Clarendon.
7. Baddeley A. 1998. Recent developments in working memory. Curr Opin Neurobiol 8:234-238.
8. Bailey CH, Giustetto M, Huang YY, Hawkins RD, Kandel ER. 2000. Is heterosynaptic modulation essential for stabilizing Hebbian plasticity and memory? Nat Rev Neurosci 1:1-20.
9. Basar E, Schurmann M, Sakowitz O. 2001. The selectively distributed theta system: functions. Int J Psychophysiol 39:197-212.
10. Bastiaansen M, Hagoort P. 2003. Event-induced theta responses as a window on the dynamics of memory. Cortex 39:967-992.
11. Bland BH. 1986. The physiology and pharmacology of hippocampal formation theta rhythms. Prog Neurobiol 26:1-54.
12. Bland BH, Colom LV. 1993. Extrinsic and intrinsic properties underlying oscillation and synchrony in limbic cortex. Prog Neurobiol 41:157-208.
13. Bland BH, Colom LV, Konopacki J, Roth SH. 1988. Intracellular records of carbachol-induced theta rhythm in hippocampal slices. Brain Res 447:364-368.
14. Bland BH, Colom LV, Ford RD. 1990. Responses of septal theta-on and theta-off cells to activation of the dorsomedial-posterior hypothalamic region. Brain Res Bull 24:71-79.
15. Bland BH, Oddie SD, Colom LV, Vertes RP. 1994. Extrinsic modulation of medial septal cell discharges by the ascending brainstem hippocampal synchronizing pathway. Hippocampus 4:649-660.
16. Bland BH, Konopacki J, Kirk IJ, Oddie SD, Dickson CT. 1995. Discharge patterns of hippocampal theta-related cells in the caudal diencephalon of the urethane-anesthetized rat. J Neurophysiol 74:322-333.
17. Bland BH, Konopacki J, Dyck RH. 2002. Relationship between membrane potential oscillations and rhythmic discharges in identified hippocampal theta-related cells. J Neurophysiol 88:3046-3066.
18. Bland BH, Konopacki J, Dyck RH. Heterogeneity among hippocampal pyramidal neurons revealed by their relation to theta-band oscillation and synchrony. Exp Neurol, in press (PMID: 16023636, Epub ahead of print).
19. Bliss TVP, Collingridge GL. 1993. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31-39.
20. Bocian R, Konopacki J. 2004. The effect of posterior hypothalamic injection of cholinergic agents on hippocampal formation theta in freely moving cat. Brain Res Bull 63:283-294.
21. Borhegyi Z, Magloczky Z, Acsady L, Freund TF. 1998. The supramammillary nucleus innervates cholinergic and GABAergic neurons in the medial septum-diagonal band of Broca complex. Neuroscience 82:1053-1065.
22. Bramham CR, Srebro B. 1989. Synaptic plasticity in the hippocampus is modulated by behavioral state. Brain Res 493:74-86.
23. Brazhnik ES, Vinogradova OS, Karanov AM. 1985. Frequency modulation of neuronal theta-bursts in rabbit's septum by low-frequency repetitive stimulation of the afferent pathways. Neuroscience 14:501-508.
24. Buhot MC. 1997. Serotonin receptors in cognitive behaviors. Curr Opin Neurobiol 7:243-254.
25. Buzsaki G. 2002. Theta oscillations in the hippocampus. Neuron 33:325-340.
26. Corradetti R, Ballerini L, Pugliese AM, Pepeu G. 1992. Serotonin blocks the long-term potentiation induced by primed burst stimulation in the CA1 region of rat hippocampal slices. Neuroscience 46:511-518.
27. Diamond DM, Dunwiddie TV, Rose GM. 1988. Characteristics of hippocampal primed burst potentiation in vitro and in the awake rat. J Neurosci 8:4079-4088.
28. Fell J, Klaver P, Elfadil H, Schaller C, Elger CE, Fernandez G. 2003. Rhinal-hippocampal theta coherence during declarative memory formation: interaction with γ synchronization? Eur J Neurosci 17:1082-1088.
29. Frey U, Morris RGM. 1997. Synaptic tagging and long-term potentiation. Nature 385:533-536.
30. Frey U, Morris RGM. 1998a. Synaptic tagging: implications for late maintenance of hippocampal long-term potentiation. Trends Neurosci 21:181-188.
31. Frey U, Morris RGM. 1998b. Weak before strong: dissociating synaptic tagging and plasticity-factor accounts of late-LTP. Neuropharmacology 37:545-552.
32. Frey U, Krug M, Reymann KG, Matthies H. 1988. Anisomycin, an inhibitor of protein synthesis, blocks late phases of LTP phenomena in the hippocampal CA1 region in vitro. Brain Res 452:57-65.
33. Frey U, Matthies H, Reymann KG, Matthies H. 1991. The effect of dopaminergic D1 receptor blockade during tetanization on the expression of long-term potentiation in the rat CA1 region in vitro. Neurosci Lett 129:111-114.
34. Frey S, Bergado-Rosado J, Seidenbecher T, Pape HC, Frey JU. 2001. Reinforcement of early long-term potentiation (early-LTP) in dentate gyrus by stimulation of the basolateral amygdala: heterosynaptic induction mechanisms of late-LTP. J Neurosci 21:3697-3703.
35. Fujita Y, Sato T. 1964. Intracellular records from hippocampal pyramidal cells in rabbit during theta rhythm activity. J Neurophysiol 27:1012-1025.
36. Fuster JM. 2001. The prefrontal cortex - an update: time is of the essence. Neuron 30:319-333.
37. Garcia-Munoz A, Barrio LC, Buno W. 1993. Membrane potential oscillations in CA1 hippocampal pyramidal neurons in vitro: intrinsic rhythms and fluctuations entrained by sinusoidal injected current. Exp Brain Res 97:325-333.
38. Gray JA, McNaughton N. 2000. The neuropsychology of anxiety. 2nd ed. New York: Oxford University Press.
39. Green JD, Arduini AA. 1954. Hippocampal electrical activity in arousal. J Neurophysiol 17:533-557.
40. Gustafsson B, Wigstrom H, Abraham WC, Huang YY. 1987. Long-term potentiation in the hippocampus using depolarizing current pulses as the conditioning stimulus to single volley synaptic potentials. J Neurosci 7:774-780.
41. Haglund L, Swanson LW, Kohler C. 1984. The projection of the supramammillary nucleus to the hippocampal formation: an immunohistochemical and anterograde transport study with the lectin PHA-L in the rat. J Comp Neurol 229:171-185.
42. Hajszan T, Alreja M, Leranth C. 2004. Intrinsic vesicular glutamate transporter 2-immunoreactive input to septohippocampal parvalbumin-containing neurons: novel glutamatergic local circuit cells. Hippocampus 14:499-509.
43. Hasselmo ME. 2000. Septal modulation of hippocampal dynamics: what is the function of the theta rhythm? In: Numan R, editor. The behavioral neuroscience of the septal region. New York: Springer-Verlag. p 92-114.
44. Hasselmo ME, Bodelon C, Wyble BP. 2002. A proposed function for hippocampal theta rhythm: separate phases of encoding and retrieval enhance reversal of prior learning. Neural Comp 14:793-817.
45. Hebb DO. 1949. The organization of behavior: a neuropsychological theory. New York: Wiley.
46. Hersi AI, Rowe W, Gaudreau P, Quirion R. 1995. Dopamine D1 receptor ligands modulate cognitive performance and hippocampal acetylcholine release in memory-impaired aged rats. Neuroscience 69:1067-1074.
47. Holscher C, Anwyl R, Rowan MJ. 1997. Stimulation on the positive phase of hippocampal theta rhythm induces long-term potentiation that can be depotentiated by stimulation on the negative phase in area CA1 in vivo. J Neurosci 17:6470-6477.
48. Huang YY, Kandel ER. 1995. D1/D5 receptor agonists induce a protein synthesis-dependent late potentiation in the CA1 region of the hippocampus. Proc Natl Acad Sci USA 92:2446-2450.
49. Huerta PT, Lisman JE. 1993. Heightened synaptic plasticity of hippocampal CA1 neurons during a cholinergically induced rhythmic state. Nature 364:723-725.
50. Huerta PT, Lisman JE. 1995. Bidirectional synaptic plasticity induced by a single burst during cholinergic theta oscillation in CA1 in vitro. Neuron 15:1053-1063.
51. Huerta PT, Lisman JE. 1996. Low-frequency stimulation at the troughs of theta-oscillation induces long-term depression of previously potentiated CA1 synapses. J Neurophysiol 75:877-884.
52. Hyman JM, Wyble BP, Goyal V, Rossi CA, Hasselmo ME. 2003. Stimulation in hippocampal region CA1 in behaving rats yields long-term potentiation when delivered to the peak of theta and long-term depression when delivered to the trough. J Neurosci 23:11725-11731.
53. Jacobs BL, Azmitia EC. 1992. Structure and function of the brain serotonin system. Physiol Rev 72:165-229.
54. Jacobs BL, Heym J, Steinfels GF. 1984. Physiological and behavioral analysis of raphe unit activity. In: Iverson LL, Iversen SD, Snyder SH, editors. Handbook of psychopharmacology. New York: Plenum. p 343-395.
55. Kahana MJ, Sekuler R, Caplan JB, Kirschen M, Madsen JR. 1999. Human theta oscillations exhibit task dependence during virtual maze navigation. Nature 399:781-784.
56. Kamondi A, Acsady L, Wang XJ, Buzsaki G. 1998. Theta oscillations in somata and dendrites of hippocampal pyramidal cells in vivo: activity-dependent phase-precession of action potentials. Hippocampus 8:244-261.
57. Kandel ER, Tauc L. 1965a. Heterosynaptic facilitation in neurones of the abdominal ganglion of Aplysia depilans. J Physiol 181:1-27.
58. Kandel ER, Tauc L. 1965b. Mechanism of heterosynaptic facilitation in the giant cell of the abdominal ganglion of Aplysia depilans. J Physiol 181:28-47.
59. Kinney GG, Kocsis B, Vertes RP. 1994. Injections of excitatory amino acid antagonists into the median raphe nucleus produce hippocampal theta rhythm in the urethane-anesthetized rat. Brain Res 654:96-104.
60. Kinney GG, Kocsis B, Vertes RP. 1995. Injections of muscimol into the median raphe nucleus produce hippocampal theta rhythm in the urethane-anesthetized rat. Psychopharmacology 120:244-248.
61. Kinney GG, Kocsis B, Vertes RP. 1996. Medial septal unit firing characteristics following injections of 8-OH-DPAT into the median raphe nucleus. Brain Res 708:116-122.
62. Kirk IJ, Mackay JC. 2003. The role of theta-range oscillations in synchronising and integrating activity in distributed mnemonic networks. Cortex 39:993-1008.
63. Kirk IJ, McNaughton N. 1991. Supramammillary cell firing and hippocampal rhythmical slow activity. Neuroreport 2:723-725.
64. Kirk IJ, McNaughton N. 1993. Mapping the differential effects of procaine on frequency and amplitude of reticularly elicited hippocampal rhythmical slow activity. Hippocampus 3:517-526.
65. Kiss J, Csaki A, Bokor H, Shanabrough M, Leranth C. 2000. The supramammillo-hippocampal and supramammillo-septal glutamatergic/aspartatergic projections in the rat: a combined [3H]D-aspartate autoradiographic and immunohistochemical study. Neuroscience 97:657-669.
66. Kitchigina VF, Kudina TA, Kutyreva EV, Vinogradova OS. 1999. Neuronal activity of the septal pacemaker of theta rhythm under the influence of stimulation and blockade of the median raphe nucleus in the awake rabbit. Neuroscience 94:453-463.
67. Klimesch W. 1999. EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis. Brain Res Rev 29:169-195.
68. Kocsis B, Vertes RP. 1994. Characterization of neurons of the supramammillary nucleus and mammillary body that discharge rhythmically with the hippocampal theta rhythm in the rat. J Neurosci 14:7040-7052.
69. Kocsis B, Vertes RP. 1996. Midbrain raphe cell firing and hippocampal theta rhythm in urethane-anaesthetized rats. Neuroreport 7:2867-2872.
70. Kocsis B, Vertes RP. 1997. Phase relations of rhythmic neuronal firing in the supramammillary nucleus and mammillary body to the hippocampal theta activity in urethane-anesthetized rats. Hippocampus 7:204-214.
71. Konopacki J, Bland BH, Colom LV, Oddie SD. 1992. In vivo intracellular correlates of hippocampal formation theta-on and theta-off cells. Brain Res 586:247-255.
72. Krug M, Lossner B, Ott T. 1984. Anisomycin blocks the late phase of long-term potentiation in the dentate gyrus of freely moving rats. Brain Res Bull 13:39-42.
73. Larson J, Wong D, Lynch G. 1986. Patterned stimulation at the theta frequency is optimal for the induction of hippocampal long-term potentiation. Brain Res 368:347-350.
74. Leranth C, Kiss J. 1996. A population of supramammillary area calretinin neurons terminating on medial septal area cholinergic and lateral septal area calbindin-containing cells are aspartate/glutamatergic. J Neurosci 16:7699-7710.
75. Leung L-WS, Yim CY. 1986. Intracellular records of theta rhythm in hippocampal CA1 cells of the rat. Brain Res 367:323-327.
76. Leung L-WS, Yim CY. 1991. Intrinsic membrane potential oscillations in hippocampal neurons in vitro. Brain Res 553:261-274.
77. Leutgeb S, Mizumori SJY. 1999. Excitotoxic septal lesions result in spatial memory deficits and altered flexibility of hippocampal single-unit representations. J Neurosci 19:6661-6672.
78. Levy WB, Steward O. 1983. Temporal contiguity requirements for long-term associative potentiation/depression in the hippocampus. Neuroscience 8:791-797.
79. Lisman J. 1994. The CaM kinase II hypothesis for the storage of synaptic memory. Trends Neurosci 17:406-412.
80. Macadar AW, Chalupa LM, Lindsley DB. 1974. Differentiation of brain stem loci which affect hippocampal and neocortical electrical activity. Exp Neurol 43:499-514.
81. Magloczky Z, Acsady L, Freund TF. 1994. Principal cells are the postsynaptic targets of supramammillary afferents in the hippocampus of the rat. Hippocampus 4:322-334.
82. Malenka RC, Nicoll RA. 1999. Long-term potentiation - a decade of progress? Science 285:1870-1874.
83. Martin KC, Kosik KS. 2002. Synaptic tagging - who's it? Nat Rev Neurosci 3:813-820.
84. Martin KC, Casadio A, Zhu H, Yaping E, Rose JC, Chen M, Bailey CH, Kandel ER. 1997. Synapse-specific, long-term facilitation of aplysia sensory to motor synapses: a function for local protein synthesis in memory storage. Cell 91:927-938.
85. Maru E, Takahashi LK, Iwahara S. 1979. Effects of median raphe nucleus lesions on hippocampal EEG in the freely moving rat. Brain Res 163:223-234.
86. Matthies H, Becker A, Schroeder H, Kraus J, Hollt V, Krug M. 1997. Dopamine D1-deficient mutant mice do not express the late phase of hippocampal long-term potentiation. Neuroreport 8:3533-3535.
87. Mayford M, Wang J, Kandel ER, Odell TJ. 1995. CaMKII regulates the frequency-response function of hippocampal synapses for the production of both LTD and UP. Cell 81:891-904.
88. Mayford M, Bach ME, Huang YY, Wang L, Hawkins RD, Kandel ER. 1996. Control of memory formation through regulated expression of a CaMKII transgene. Science 274:1678-1683.
89. McCartney H, Johnson AD, Weil ZM, Givens B. 2004. Theta reset produces optimal conditions for long-term potentiation. Hippocampus 14:684-687.
90. McGaugh JL. 2000. Memory - a century of consolidation. Science 287:248-251.
91. McGaugh JL. 2004. The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annu Rev Neurosci 27:1-28.
92. McNaughton N, Azmitia EC, Williams JH, Buchan A, Gray JA. 1980. Septal elicitation of hippocampal theta rhythm after localized de-afferentation of serotoninergic fibers. Brain Res 200:259-269.
93. McNaughton N, Richardson J, Gore C. 1986. Reticular elicitation of hippocampal slow waves: common effects of some anxiolytic drugs. Neuroscience 19:899-903.
94. M'Harzi M, Jarrard LE. 1992. Effects of medial and lateral septal lesions on acquisition of a place and cue radial maze task. Behav Brain Res 49:159-165.
95. Mizumori SJY, Perez GM, Alvarado MC, Barnes CA, McNaughton BL. 1990. Reversible inactivation of the medial septum differentially affects two forms of learning in rats. Brain Res 528:12-20.
96. Nunez A, Garcia-Austt E, Buno W. 1987. Intracellular theta rhythm generation in identified hippocampal pyramids. Brain Res 416: 289-300.
97. Nunez A, Garcia-Austt E, Buno W. 1990. Synaptic contributions to theta rhythm genesis in rat CA1-CA3 hippocampal pyramidal neurons in vivo. Brain Res 533:176-179.
98. O'Carroll CM, Morris RG. 2004. Heterosynaptic co-activation of glutamatergic and dopaminergic afferents is required to induce persistent long-term potentiation. Neuropharmacology 47:324-332.
99. Oddie SD, Bland BH, Colom LV, Vertes RP. 1994. The midline posterior hypothalamic region comprises a critical part of the ascending brainstem hippocampal synchronizing pathway. Hippocampus 4:454-473.
100. O'Keefe J, Burgess N. 1999. Theta activity, virtual navigation and the human hippocampus. Trends Cogn Sci 3:403-406.
101. Pan WX, McNaughton N. 2004. The supramammillary area: its organization, functions and relationship to the hippocampus. Prog Neurobiol 74:127-166.
102. Pang PT, Lu B. 2004. Regulation of late-phase LTP, long-term memory in normal and aging hippocampus: role of secreted proteins tPA and BDNF. Ageing Res Rev 3:407-430.
103. Pavlides C, Greenstein YJ, Grudman M, Winson J. 1988. Long-term potentiation in the dentate gyrus is induced preferentially on the positive phase of theta-rhythm. Brain Res 439:383-387.
104. Raghavachari S, Kahana MJ, Rizzuto DS, Caplan JB, Kirschen MP, Bourgeois B, Madsen JR, Lisman JE. 2001. Gating of human theta oscillations by a working memory task. J Neurosci 21:3175-3183.
105. Rasmussen K, Heym J, Jacobs BL. 1984. Activity of serotonin-containing neurons in nucleus centralis superior of freely moving cats. Exp Neurol 83:302-317.
106. Richter-Levin G, Akirav I. 2003. Emotional tagging of memory formation - in the search for neural mechanisms. Brain Res Rev 43: 247-256.
107. Rotenberg A, Mayford M, Hawkins RD, Kandel ER, Muller RU. 1996. Mice expressing activated CaMKII lack low frequency LTP and do not form stable place cells in the CA1 region of the hippocampus. Cell 87:1351-1361.
108. Sajikumar S, Frey JU. 2004. Late-associativity, synaptic tagging, and the role of dopamine during LTP and LTD. Neurobiol Learn Mem 82:12-25.
109. Sarnthein J, Petsche H, Rappelsberger P, Shaw GL, von Stein A. 1998. Synchronization between prefrontal and posterior association cortex during human working memory. Proc Natl Acad Sci USA 95:7092-7096.
110. Seidenbecher T, Reymann KG, Balschun D. 1997. A post-tetanic time window for the reinforcement of long-term potentiation by appetitive and aversive stimuli. Proc Natl Acad Sci USA 94:1494-1499.
111. Smythe JW, Christie BR, Colom LV, Lawson VH, Bland BH. 1991. Hippocampal theta field activity and theta-on/theta-off cell discharges are controlled by an ascending hypothalamo-septal pathway. J Neurosci 11:2241-2248.
112. 1B agonists. Synapse 1:3-9.
113. Staubli U, Lynch G. 1987. Stable hippocampal long-term potentiation elicited by 'theta' pattern stimulation. Brain Res 435:227-234.
114. Staubli U, Otaky N. 1994. Serotonin controls the magnitude of LTP induced by theta bursts via an action on NMDA-receptor-mediated responses. Brain Res 643:10-16.
115. 3 receptor antagonism on hippocampal theta rhythm, memory, and LTP induction in the freely moving rat. J Neurosci 15:2445-2452.
116. Strata F. 1998. Intrinsic oscillations in CA3 hippocampal pyramids: physiological relevance to theta rhythm generation. Hippocampus 8:666-679.
117. Swanson-Park JL, Coussens CM, Mason-Parker SE, Raymond CR, Hargreaves EL, Dragunow M, Cohen AS, Abraham WC. 1999. A double dissociation within the hippocampus of dopamine D1/D5 receptor and β-adrenergic receptor contributions to the persistence of long-term potentiation. Neuroscience 92:485-497.
118. Vanderwolf CH. 1969. Hippocampal electrical activity and voluntary movement in rat. Electroenceph Clin Neurophysiol 26:407-418.
119. Varga V, Sik A, Freund TF, Kocsis B. 2002. GABA(B) receptors in the median raphe nucleus: distribution and role in the serotonergic control of hippocampal activity. Neuroscience 109:119-132.
120. Vertes RP. 1977. Selective firing of rat pontine gigantocellular neurons during movement and REM sleep. Brain Res 128:146-152.
121. Vertes RP. 1979. Brain stem gigantocellular neurons: patterns of activity during behavior and sleep in the freely moving rat. J Neurophysiol 42:214-228.
122. Vertes RP. 1980. Brain stem activation of the hippocampus: a role for the magnocellular reticular formation and the MLF. Electroenceph Clin Neurophysiol 50:48-58.
123. Vertes RP. 1981. An analysis of ascending brain stem systems involved in hippocampal synchronization and desynchronization. J Neurophysiol 46:1140-1159.
124. Vertes RP. 1982. Brain stem generation of the hippocampal EEG. Prog Neurobiol 19:159-186.
125. Vertes RP. 1986. Brainstem modulation of the hippocampus. Anatomy, physiology and significance. In: Isaacson RL, Pribram KH, editors. The hippocampus. Vol 4. New York: Plenum. p 41-75.
126. Vertes RP. 1988. Brainstem afferents to the basal forebrain in the rat. Neuroscience 24:907-935.
127. Vertes RP. 1990. Fundamentals of brainstem anatomy: a behavioral perspective. In: Klemm WR, Vertes RP, editors. Brainstem mechanisms of behavior. New York: Wiley. p 33-103.
128. Vertes RP. 1992. PHA-L analysis of projections from the supramammillary nucleus in the rat. J Comp Neur 326:595-622.
129. Vertes RP, Kocsis B. 1997. Brainstem-diencephalo-septohippocampal systems controlling the theta rhythm of the hippocampus. Neuroscience 81:893-926.
130. Vertes RP, Martin GF. 1988. Autoradiographic analysis of ascending projections from the pontine and mesencephalic reticular formation and the median raphe nucleus in the rat. J Comp Neurol 275:511-541.
131. Vertes RP, McKenna JT. 2000. Collateral projections from the supramammillary nucleus to the medial septum and hippocampus. Synapse 38:281-293.
132. 1A agonists, 8-OH-DPAT and buspirone, produces hippocampal theta-rhythm in the rat. Neuroscience 60:441-451.
133. Vertes RP, Hoover WB, Viana Di Prisco G. 2004. Theta rhythm of the hippocampus: subcortical control and functional significance. Behav Cogn Neurosci Rev 3:173-200.
134. Viana Di Prisco G, Albo Z, Vertes RP, Kocsis B. 2002. Discharge properties of neurons of the median raphe nucleus during hippocampal theta rhythm in the rat. Exp Brain Res 145:383-394.
135. Vinogradova OS, Kitchigina VF, Kudina TA, Zenchenko KI. 1999. Spontaneous activity and sensory responses of hippocampal neurons during persistent theta-rhythm evoked by median raphe nucleus blockade in rabbit. Neuroscience 94:745-753.
136. Winson J. 1972. Interspecies differences in occurrence of theta. Behav Biol 7:479-487.
137. Winson J. 1978. Loss of hippocampal theta rhythm results in spatial memory deficit in rat. Science 201:160-163.
138. Yamamoto T, Watanabe S, Oishi R, Ueki S. 1979. Effects of midbrain raphe stimulation and lesion on EEG activity in rats. Brain Res Bull 4:491-495. 9