Skip to main content
Log in

Serotonergic modulation of hippocampal theta activity in relation to hippocampal information processing

  • Review
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

Hippocampal theta activity is the result of the concerted activity of a group of nuclei located in the brain stem and the caudal diencephalic area, which are together referred to as the synchronizing ascending system. Serotonin is recognized as the only neurotransmitter able to desynchronize the hippocampal electroencephalographic. A theory has been developed in which serotonin, acting on medial septal neurons, modulates cholinergic/GABAergic inputs to the hippocampus and, thus, the cognitive processing mediated by this area. However, few studies have addressed the relationship between serotonin modulation of theta activity and cognition. In this review, we present a summary and analysis of the data relating serotonin and its theta activity modulation with cognition, and we also discuss the few works relating serotonin, theta activity and cognition as well as the theories regarding the serotonin regulation of memory processes organized by the hippocampus. We propose that serotonin depletion induces impairment of the relays coding the frequency of hippocampal theta activity, whereas depletion of the relays in which frequency is not coded induces improvements in spatial learning that are related to increased expression of high-frequency theta activity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Adams W, Kusljic S, van den Buuse M (2008) Serotonin depletion in the dorsal and ventral hippocampus: effects on locomotor hyperactivity, prepulse inhibition and learning and memory. Neuropharmacology 55:1048–1055

    PubMed  CAS  Google Scholar 

  • Aggleton JP, Brown MW (1999) Episodic memory, amnesia, and the hippocampal-anterior thalamic axis. Behav Brain Sci 22:425–444 (discussion 444–489)

    PubMed  CAS  Google Scholar 

  • Alreja M (1996) Excitatory actions of serotonin on GABAergic neurons of the medial septum and diagonal band of Broca. Synapse 22:15–27

    PubMed  CAS  Google Scholar 

  • Alreja M, Wu M, Liu W, Atkins JB, Leranth C, Shanabrough M (2000) Muscarinic tone sustains impulse flow in the septohippocampal GABA but not cholinergic pathway: implications for learning and memory. J Neurosci 20:8103–8110

    PubMed  CAS  Google Scholar 

  • Altman HJ, Ogren SO, Berman RF, Normile HJ (1989) The effects of p-chloroamphetamine, a depletor of brain serotonin, on the performance of rats in two types of positively reinforced complex spatial discrimination tasks. Behav Neural Biol 52:131–144

    PubMed  CAS  Google Scholar 

  • Altman HJ, Normile HJ, Galloway MP, Ramirez A, Azmitia EC (1990) Enhanced spatial discrimination learning in rats following 5,7-DHT-induced serotonergic deafferentation of the hippocampus. Brain Res 518:61–66

    PubMed  CAS  Google Scholar 

  • Ammassari-Teule M, Maho C, Sara SJ (1991) Clonidine reverses spatial learning deficits and reinstates theta frequencies in rats with partial fornix section. Behav Brain Res 45:1–8

    PubMed  CAS  Google Scholar 

  • Anchel H, Lindsley DB (1972) Differentiation of two reticulo-hypothalamic systems regulating hippocampal activity. Electroencephalogr Clin Neurophysiol 32:209–226

    PubMed  CAS  Google Scholar 

  • Andersen P, Bland HB, Myhrer T, Schwartzkroin PA (1979) Septo-hippocampal pathway necessary for dentate theta production. Brain Res 165:13–22

    PubMed  CAS  Google Scholar 

  • Andrews N, Hogg S, Gonzalez LE, File SE (1994) 5-HT1A receptors in the median raphe nucleus and dorsal hippocampus may mediate anxiolytic and anxiogenic behaviours respectively. Eur J Pharmacol 264:259–264

    PubMed  CAS  Google Scholar 

  • Arita H, Sakamoto M, Hirokawa Y, Okado N (1993) Serotonin innervation patterns differ among the various medullary motoneuronal groups involved in upper airway control. Exp Brain Res 95:100–110

    PubMed  CAS  Google Scholar 

  • Asaka Y, Mauldin KN, Griffin AL, Seager MA, Shurell E, Berry SD (2005) Nonpharmacological amelioration of age-related learning deficits: the impact of hippocampal theta-triggered training. Proc Natl Acad Sci USA 102:13284–13288

    PubMed  CAS  Google Scholar 

  • Assaf SY, Miller JJ (1978) The role of a raphe serotonin system in the control of septal unit activity and hippocampal desynchronization. Neuroscience 3:539–550

    PubMed  CAS  Google Scholar 

  • Azmitia EC (1978) The serotonin-producing neurons of the midbrain median and dorsal raphe nuclei. In: Iversen LL, Iversen SD, Snyder SH (eds) Handbook of psychopharmacology. Raven, New York, pp 233–262

    Google Scholar 

  • Aznar S, Qian ZX, Knudsen GM (2004) Non-serotonergic dorsal and median raphe projection onto parvalbumin- and calbindin-containing neurons in hippocampus and septum. Neuroscience 124:573–581

    PubMed  CAS  Google Scholar 

  • Bastiaansen MC, Posthuma D, Groot PF, de Geus EJ (2002) Event-related alpha and theta responses in a visuo-spatial working memory task. Clin Neurophysiol 113:1882–1893

    PubMed  Google Scholar 

  • Bennett TL, French J (1977) Electrical activity of the cat hippocampus during the species-typical gape response: evidence against the voluntary movement hypothesis. Behav Biol 21:432–437

    PubMed  CAS  Google Scholar 

  • Berry SD, Thompson RF (1978) Prediction of learning rate from the hippocampal electroencephalogram. Science 200:1298–1300

    PubMed  CAS  Google Scholar 

  • Bertrand F, Lehmann O, Lazarus C, Jeltsch H, Cassel JC (2000) Intraseptal infusions of 8-OH-DPAT in the rat impairs water-maze performances: effects on memory or anxiety? Neurosci Lett 279:45–48

    PubMed  CAS  Google Scholar 

  • Bland BH, Oddie SD (2001) Theta band oscillation and synchrony in the hippocampal formation and associated structures: the case for its role in sensorimotor integration. Behav Brain Res 127:119–136

    PubMed  CAS  Google Scholar 

  • Bland BH, Whishaw IQ (1976) Generators and topography of hippocampal theta (RSA) in the anaesthetized and freely moving rat. Brain Res 118:259–280

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Bland BH, Konopacki J, Kirk IJ, Oddie SD, Dickson CT (1995) Discharge patterns of hippocampal theta-related cells in the caudal diencephalon of the urethan-anesthetized rat. J Neurophysiol 74:322–333

    PubMed  CAS  Google Scholar 

  • Bland BH, Trepel C, Oddie SD, Kirk IJ (1996) Intraseptal microinfusion of muscimol: effects on hippocampal formation theta field activity and phasic theta-ON cell discharges. Exp Neurol 138:286–297

    PubMed  CAS  Google Scholar 

  • Brashear HR, Zaborszky L, Heimer L (1986) Distribution of GABAergic and cholinergic neurons in the rat diagonal band. Neuroscience 17:439–451

    PubMed  CAS  Google Scholar 

  • Buno W Jr, Garcia-Sanchez JL, Garcia-Austt E (1978) Reset of hippocampal rhythmical activities by afferent stimulation. Brain Res Bull 3:21–28

    PubMed  Google Scholar 

  • Buzsaki G (2002) Theta oscillations in the hippocampus. Neuron 33:325–340

    PubMed  CAS  Google Scholar 

  • Buzsaki G (2005) Theta rhythm of navigation: link between path integration and landmark navigation, episodic and semantic memory. Hippocampus 15:827–840

    PubMed  Google Scholar 

  • Buzsaki G, Bragin A, Chrobak JJ, Nadasdy Z, Sik A, Hsu M et al (1994) Oscillatory and intermittent synchrony in the hippocampus: relevance to memory trace formation. In: Buzsak G, Singer W, Berthoz A, Christen Y (eds) Temporal coding in the brain. Springer, Berlin, pp 145–172

    Google Scholar 

  • Calizo LH, Akanwa A, Ma X, Pan YZ, Lemos JC, Craige C et al (2011) Raphe serotonin neurons are not homogenous: electrophysiological, morphological and neurochemical evidence. Neuropharmacology 61:524–543

    PubMed  CAS  Google Scholar 

  • Carli M, Lazarova M, Tatarczynska E, Samanin R (1992) Stimulation of 5-HT1A receptors in the dorsal hippocampus impairs acquisition and performance of a spatial task in a water maze. Brain Res 595:50–56

    PubMed  CAS  Google Scholar 

  • Carli M, Bonalumi P, Samanin R (1998) Stimulation of 5-HT1A receptors in the dorsal raphe reverses the impairment of spatial learning caused by intrahippocampal scopolamine in rats. Eur J Neurosci 10:221–230

    PubMed  CAS  Google Scholar 

  • Carli M, Silva S, Balducci C, Samanin R (1999) WAY 100635, a 5-HT1A receptor antagonist, prevents the impairment of spatial learning caused by blockade of hippocampal NMDA receptors. Neuropharmacology 38:1165–1173

    PubMed  CAS  Google Scholar 

  • Cassel JC, Jeltsch H (1995) Serotonergic modulation of cholinergic function in the central nervous system: cognitive implications. Neuroscience 69:1–41

    PubMed  CAS  Google Scholar 

  • Cassel JC, Duconseille E, Jeltsch H, Will B (1997) The fimbria-fornix/cingular bundle pathways: a review of neurochemical and behavioural approaches using lesions and transplantation techniques. Prog Neurobiol 51(6):663–716

    Google Scholar 

  • Chauviere L, Rafrafi N, Thinus-Blanc C, Bartolomei F, Esclapez M, Bernard C (2009) Early deficits in spatial memory and theta rhythm in experimental temporal lobe epilepsy. J Neurosci 29:5402–5410

    PubMed  CAS  Google Scholar 

  • Clements JR, Grant S (1990) Glutamate-like immunoreactivity in neurons of the laterodorsal tegmental and pedunculopontine nuclei in the rat. Neurosci Lett 120:70–73

    PubMed  CAS  Google Scholar 

  • Clemett DA, Punhani T, Duxon MS, Blackburn TP, Fone KC (2000) Immunohistochemical localisation of the 5-HT2C receptor protein in the rat CNS. Neuropharmacology 39:123–132

    PubMed  CAS  Google Scholar 

  • Coffey BJ, Shechter RL (2006) Treatment of co-morbid obsessive compulsive disorder, mood, and anxiety disorders. Adv Neurol 99:208–221

    PubMed  Google Scholar 

  • Colom LV, Castaneda MT, Reyna T, Hernandez S, Garrido-Sanabria E (2005) Characterization of medial septal glutamatergic neurons and their projection to the hippocampus. Synapse 58:151–164

    PubMed  CAS  Google Scholar 

  • Conrad LC, Leonard CM, Pfaff DW (1974) Connections of the median and dorsal raphe nuclei in the rat: an autoradiographic and degeneration study. J Comp Neurol 156:179–205

    PubMed  CAS  Google Scholar 

  • Cornwell BR, Johnson LL, Holroyd T, Carver FW, Grillon C (2008) Human hippocampal and parahippocampal theta during goal-directed spatial navigation predicts performance on a virtual Morris water maze. J Neurosci 28:5983–5990

    PubMed  CAS  Google Scholar 

  • Crooks R, Jackson J, Bland BH (2012) Dissociable pathways facilitate theta and non-theta states in the median raphe—septohippocampal circuit. Hippocampus 22:1567–1576

    PubMed  CAS  Google Scholar 

  • Crutcher KA, Madison R, Davis JN (1981) A study of the rat septohippocampal pathway using anterograde transport of horseradish peroxidase. Neuroscience 6:1961–1973

    PubMed  CAS  Google Scholar 

  • Deakin JF, Graeff FG (1991) 5-HT and mechanisms of defence. J Psychopharmacol 5:305–315

    PubMed  CAS  Google Scholar 

  • Dursun SM, Szemis A, Andrews H, Whitaker P, Reveley MA (2000) Effects of clozapine and typical antipsychotic drugs on plasma 5-HT turnover and impulsivity in patients with schizophrenia: a cross-sectional study. J Psychiatry Neurosci 25:347–352

    PubMed  CAS  Google Scholar 

  • Eichenbaum H, Otto T, Cohen NJ (1992) The hippocampus—what does it do? Behav Neural Biol 57:2–36

    PubMed  CAS  Google Scholar 

  • Ekstrom AD, Caplan JB, Ho E, Shattuck K, Fried I, Kahana MJ (2005) Human hippocampal theta activity during virtual navigation. Hippocampus 15:881–889

    PubMed  Google Scholar 

  • Elvander-Tottie E, Eriksson TM, Sandin J, Ogren SO (2009) 5-HT(1A) and NMDA receptors interact in the rat medial septum and modulate hippocampal-dependent spatial learning. Hippocampus 19:1187–1198

    PubMed  CAS  Google Scholar 

  • Floresco SB, Seamans JK, Phillips AG (1997) Selective roles for hippocampal, prefrontal cortical, and ventral striatal circuits in radial-arm maze tasks with or without a delay. J Neurosci 17:1880–1890

    PubMed  CAS  Google Scholar 

  • Forchetti CM, Meek JL (1981) Evidence for a tonic GABAergic control of serotonin neurons in the median raphe nucleus. Brain Res 206:208–212

    PubMed  CAS  Google Scholar 

  • Fremeau RT Jr, Burman J, Qureshi T, Tran CH, Proctor J, Johnson J et al (2002) The identification of vesicular glutamate transporter 3 suggests novel modes of signaling by glutamate. Proc Natl Acad Sci USA 99:14488–14493

    PubMed  CAS  Google Scholar 

  • Freund TF, Antal M (1988) GABA-containing neurons in the septum control inhibitory interneurons in the hippocampus. Nature 336:170–173

    PubMed  CAS  Google Scholar 

  • Frotscher M, Leranth C (1985) Cholinergic innervation of the rat hippocampus as revealed by choline acetyltransferase immunocytochemistry: a combined light and electron microscopic study. J Comp Neurol 239:237–246

    PubMed  CAS  Google Scholar 

  • Furlan PM, Kallan MJ, Ten Have T, Pollock BG, Katz I, Lucki I (2001) Cognitive and psychomotor effects of paroxetine and sertraline on healthy elderly volunteers. Am J Geriatr Psychiatry 9:429–438

    PubMed  CAS  Google Scholar 

  • Gavrilov VV, Wiener SI, Berthoz A (1995) Enhanced hippocampal theta EEG during whole body rotations in awake restrained rats. Neurosci Lett 197:239–241

    PubMed  CAS  Google Scholar 

  • Gaykema RP, Luiten PG, Nyakas C, Traber J (1990) Cortical projection patterns of the medial septum-diagonal band complex. J Comp Neurol 293:103–124

    PubMed  CAS  Google Scholar 

  • Givens B (1996) Stimulus-evoked resetting of the dentate theta rhythm: relation to working memory. NeuroReport 8:159–163

    PubMed  CAS  Google Scholar 

  • Gogolak G, Petsche H, Sterc J, Stumpf C (1967) Septum cell activity in the rabbit under reticular stimulation. Brain Res 5:508–510

    PubMed  CAS  Google Scholar 

  • Gogolak G, Stumpf C, Petsche H, Sterc J (1968) The firing pattern of septal neurons and the form of the hippocampal theta wave. Brain Res 7:201–207

    PubMed  CAS  Google Scholar 

  • Graeff FG, Quintero S, Gray JA (1980) Median raphe stimulation, hippocampal theta rhythm and threat-induced behavioral inhibition. Physiol Behav 25:253–261

    PubMed  CAS  Google Scholar 

  • Green JD, Arduini AA (1954) Hippocampal electrical activity in arousal. J Neurophysiol 17:533–557

    PubMed  CAS  Google Scholar 

  • Griffin AL, Asaka Y, Darling RD, Berry SD (2004) Theta-contingent trial presentation accelerates learning rate and enhances hippocampal plasticity during trace eyeblink conditioning. Behav Neurosci 118:403–411

    PubMed  Google Scholar 

  • Gutierrez-Guzman BE, Hernandez-Perez JJ, Gonzalez-Burgos I, Feria-Velasco A, Medina R, Guevara MA et al (2011) Hippocampal serotonin depletion facilitates place learning concurrent with an increase in CA1 high frequency theta activity expression in the rat. Eur J Pharmacol 652:73–81

    PubMed  CAS  Google Scholar 

  • Gutierrez-Guzman BE, Hernandez-Perez JJ, Lopez-Vazquez MA, Fregozo CS, Guevara MA, Olvera-Cortes ME (2012) Serotonin depletion of supramammillary/posterior hypothalamus nuclei produces place learning deficiencies and alters the concomitant hippocampal theta activity in rats. Eur J Pharmacol 682:99–109

    PubMed  CAS  Google Scholar 

  • Gyermek L (1961) 5-Hydroxytryptamine antagonists. Pharmacol Rev 13:399–439

    PubMed  CAS  Google Scholar 

  • Hajos M, Hoffmann WE, Robinson DD, Yu JH, Hajos-Korcsok E (2003a) Norepinephrine but not serotonin reuptake inhibitors enhance theta and gamma activity of the septo-hippocampal system. Neuropsychopharmacology 28:857–864

    PubMed  CAS  Google Scholar 

  • Hajos M, Hoffmann WE, Weaver RJ (2003b) Regulation of septo-hippocampal activity by 5-hydroxytryptamine(2C) receptors. J Pharmacol Exp Ther 306:605–615

    PubMed  CAS  Google Scholar 

  • Hangya B, Borhegyi Z, Szilagyi N, Freund TF, Varga V (2009) GABAergic neurons of the medial septum lead the hippocampal network during theta activity. J Neurosci 29:8094–8102

    PubMed  CAS  Google Scholar 

  • Harmer CJ, Bhagwagar Z, Cowen PJ, Goodwin GM (2002) Acute administration of citalopram facilitates memory consolidation in healthy volunteers. Psychopharmacology 163:106–110

    PubMed  CAS  Google Scholar 

  • Harrison CL, Ferrier N, Young AH (2004) Tolerability of high-dose venlafaxine in depressed patients. J Psychopharmacol 18:200–204

    PubMed  CAS  Google Scholar 

  • Hayes SM, Ryan L, Schnyer DM, Nadel L (2004) An fMRI study of episodic memory: retrieval of object, spatial, and temporal information. Behav Neurosci 118:885–896

    PubMed  Google Scholar 

  • Hinman JR, Penley SC, Long LL, Escabi MA, Chrobak JJ (2011) Septotemporal variation in dynamics of theta: speed and habituation. J Neurophysiol 105:2675–2686

    PubMed  Google Scholar 

  • Hoffmann LC, Berry SD (2009) Cerebellar theta oscillations are synchronized during hippocampal theta-contingent trace conditioning. Proc Natl Acad Sci USA 106:21371–21376

    PubMed  CAS  Google Scholar 

  • Huh CY, Goutagny R, Williams S (2010) Glutamatergic neurons of the mouse medial septum and diagonal band of Broca synaptically drive hippocampal pyramidal cells: relevance for hippocampal theta rhythm. J Neurosci 30:15951–15961

    PubMed  CAS  Google Scholar 

  • Jackson J, Dickson CT, Bland BH (2008) Median raphe stimulation disrupts hippocampal theta via rapid inhibition and state-dependent phase reset of theta-related neural circuitry. J Neurophysiol 99:3009–3026

    PubMed  Google Scholar 

  • Jacobson TK, Howe MD, Schmidt B, Hinman JR, Escabi MA, Markus EJ (2013) Hippocampal theta, gamma, and theta-gamma coupling: effects of aging, environmental change, and cholinergic activation. J Neurophysiol 109:1852–1865

    PubMed  Google Scholar 

  • Jakab RL, Leranth C (1995) Septum. In: Paxinos G (ed) The rat nervous system. Academic Press, San Diego, pp 405–442

    Google Scholar 

  • Jarrard LE (1993) On the role of the hippocampus in learning and memory in the rat. Behav Neural Biol 60:9–26

    PubMed  CAS  Google Scholar 

  • Jeewajee A, Lever C, Burton S, O’Keefe J, Burgess N (2008) Environmental novelty is signaled by reduction of the hippocampal theta frequency. Hippocampus 18:340–348

    PubMed  CAS  Google Scholar 

  • Jeltsch H, Bertrand F, Galani R, Lazarus C, Schimchowitsch S, Cassel JC (2004) Intraseptal injection of the 5-HT1A/5-HT7 agonist 8-OH-DPAT and working memory in rats. Psychopharmacology 175:37–46

    PubMed  CAS  Google Scholar 

  • Jeltsch-David H, Koenig J, Cassel JC (2008) Modulation of cholinergic functions by serotonin and possible implications in memory: general data and focus on 5-HT(1A) receptors of the medial septum. Behav Brain Res 195:86–97

    PubMed  CAS  Google Scholar 

  • Jung R, Kornmüller AE (1938) Eine Methodik der Ableitung lokalisierter Potentialschwankungen aus subcorticalen Hirngebieten. Arch Psychiatr 109:1–30

    Google Scholar 

  • Kalmbach BE, Ohyama T, Kreider JC, Riusech F, Mauk MD (2009) Interactions between prefrontal cortex and cerebellum revealed by trace eyelid conditioning. Learn Mem 16:86–95

    PubMed  Google Scholar 

  • Kantor S, Jakus R, Molnar E, Gyongyosi N, Toth A, Detari L et al (2005) Despite similar anxiolytic potential, the 5-hydroxytryptamine 2C receptor antagonist SB-242084 [6-chloro-5-methyl-1-[2-(2-methylpyrid-3-yloxy)-pyrid-5-yl carbamoyl]indoline] and chlordiazepoxide produced differential effects on electroencephalogram power spectra. J Pharmacol Exp Ther 315:921–930

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Kinney GG, Vogel GW, Feng P (1998) Brainstem carbachol injections in the urethane anesthetized rat produce hippocampal theta rhythm and cortical desynchronization: a comparison of pedunculopontine tegmental versus nucleus pontis oralis injections. Brain Res 809:307–313

    PubMed  CAS  Google Scholar 

  • Kirk IJ, McNaughton N (1991) Supramammillary cell firing and hippocampal rhythmical slow activity. NeuroReport 2:723–725

    PubMed  CAS  Google Scholar 

  • Kirk IJ, Oddie SD, Konopacki J, Bland BH (1996) Evidence for differential control of posterior hypothalamic, supramammillary, and medial mammillary theta-related cellular discharge by ascending and descending pathways. J Neurosci 16:5547–5554

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Kitchigina VF (2010) Theta oscillations and reactivity of hippocampal stratum oriens neurons. Sci World J 10:930–943

    Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Klimesch W (1999) EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis. Brain Res Brain Res Rev 29:169–195

    PubMed  CAS  Google Scholar 

  • Klimesch W, Doppelmayr M, Russegger H, Pachinger T (1996) Theta band power in the human scalp EEG and the encoding of new information. NeuroReport 7:1235–1240

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Koenig J, Lecourtier L, Cosquer B, Pereira PM, Cassel JC (2011) Spatial memory alterations by activation of septal 5HT 1A receptors: no implication of cholinergic septohippocampal neurons. Psychopharmacology 214:437–454

    PubMed  CAS  Google Scholar 

  • Kramis R, Vanderwolf CH, Bland BH (1975) 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 49:58–85

    PubMed  CAS  Google Scholar 

  • Kudina TA, Sudnitsyn VV, Kutyreva EV, Kichigina VF (2004) The serotonin reuptake inhibitor fluoxetine suppresses theta oscillations in the electroencephalogram of the rabbit hippocampus. Neurosci Behav Physiol 34:929–933

    PubMed  CAS  Google Scholar 

  • Lawson VH, Bland BH (1993) The role of the septohippocampal pathway in the regulation of hippocampal field activity and behavior: analysis by the intraseptal microinfusion of carbachol, atropine, and procaine. Exp Neurol 120:132–144

    PubMed  CAS  Google Scholar 

  • Lee MG, Chrobak JJ, Sik A, Wiley RG, Buzsaki G (1994) Hippocampal theta activity following selective lesion of the septal cholinergic system. Neuroscience 62:1033–1047

    PubMed  CAS  Google Scholar 

  • Lehmann O, Jeltsch H, Lehnardt O, Pain L, Lazarus C, Cassel JC (2000) Combined lesions of cholinergic and serotonergic neurons in the rat brain using 192 IgG-saporin and 5,7-dihydroxytryptamine: neurochemical and behavioural characterization. Eur J Neurosci 12:67–79

    PubMed  CAS  Google Scholar 

  • Lehmann O, Bertrand F, Jeltsch H, Morer M, Lazarus C, Will B et al (2002a) 5,7-DHT-induced hippocampal 5-HT depletion attenuates behavioural deficits produced by 192 IgG-saporin lesions of septal cholinergic neurons in the rat. Eur J Neurosci 15:1991–2006

    PubMed  Google Scholar 

  • Lehmann O, Jeltsch H, Lazarus C, Tritschler L, Bertrand F, Cassel JC (2002b) Combined 192 IgG-saporin and 5, 7-dihydroxytryptamine lesions in the male rat brain: a neurochemical and behavioral study. Pharmacol Biochem Behav 72:899–912

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Leranth C, Vertes RP (1999) Median raphe serotonergic innervation of medial septum/diagonal band of broca (MSDB) parvalbumin-containing neurons: possible involvement of the MSDB in the desynchronization of the hippocampal EEG. J Comp Neurol 410:586–598

    PubMed  CAS  Google Scholar 

  • Leranth C, Carpi D, Buzsaki G, Kiss J (1999) The entorhino-septo-supramammillary nucleus connection in the rat: morphological basis of a feedback mechanism regulating hippocampal theta rhythm. Neuroscience 88(3):701–718

    Google Scholar 

  • Leung LW, Lopes da Silva FH, Wadman WJ (1982) Spectral characteristics of the hippocampal EEG in the freely moving rat. Electroencephalogr Clin Neurophysiol 54:203–219

    PubMed  CAS  Google Scholar 

  • Leung LS, Martin LA, Stewart DJ (1994) Hippocampal theta rhythm in behaving rats following ibotenic acid lesion of the septum. Hippocampus 4:136–147

    PubMed  CAS  Google Scholar 

  • Li S, Topchiy I, Kocsis B (2007) 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 61:412–419

    PubMed  CAS  Google Scholar 

  • Li JY, Kuo TB, Hsieh IT, Yang CC (2012) Changes in hippocampal theta rhythm and their correlations with speed during different phases of voluntary wheel running in rats. Neuroscience 213:54–61

    PubMed  CAS  Google Scholar 

  • Ly S, Pishdari B, Lok LL, Hajos M, Kocsis B (2013) Activation of 5-HT6 receptors modulates sleep-wake activity and hippocampal theta oscillation. ACS Chem Neurosci 4:191–199

    PubMed  CAS  Google Scholar 

  • Macadar AW, Chalupa LM, Lindsley DB (1974) Differentiation of brain stem loci which affect hippocampal and neocortical electrical activity. Exp Neurol 43:499–514

    PubMed  CAS  Google Scholar 

  • Maho C, Dutrieux G, Ammassari-Teule M (1988) Parallel modifications of spatial memory performances, exploration patterns, and hippocampal theta rhythms in fornix-damaged rats: reversal by oxotremorine. Behav Neurosci 102:601–604

    PubMed  CAS  Google Scholar 

  • Martinez-Gonzalez C, Wang HL, Micklem BR, Bolam JP, Mena-Segovia J (2012) Subpopulations of cholinergic, GABAergic and glutamatergic neurons in the pedunculopontine nucleus contain calcium-binding proteins and are heterogeneously distributed. Eur J Neurosci 35:723–734

    PubMed  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Matulewicz P, Orzel-Gryglewska J, Hunt MJ, Trojniar W, Jurkowlaniec E (2010) Hippocampal theta rhythm after serotonergic activation of the pedunculopontine tegmental nucleus in anesthetized rats. Brain Res Bull 83:257–261

    PubMed  CAS  Google Scholar 

  • McCartney H, Johnson AD, Weil ZM, Givens B (2004) Theta reset produces optimal conditions for long-term potentiation. Hippocampus 14:684–687

    PubMed  Google Scholar 

  • McKenna JT, Vertes RP (2001) Collateral projections from the median raphe nucleus to the medial septum and hippocampus. Brain Res Bull 54:619–630

    PubMed  CAS  Google Scholar 

  • McMahon LL, Kauer JA (1997) Hippocampal interneurons are excited via serotonin-gated ion channels. J Neurophysiol 78:2493–2502

    PubMed  CAS  Google Scholar 

  • McNamara RK, Skeleton RW (1993) Effects of intracranial infusions of chlordiazepoxide on spatial learning in the Morris water maze. I. Neuroanatomical specificity. Behav Brain Res 59:175–191

    PubMed  CAS  Google Scholar 

  • McNaughton N, Azmitia EC, Williams JH, Buchan A, Gray JA (1980a) Septal elicitation of hippocampal theta rhythm after localized de-afferentation of serotoninergic fibers. Brain Res 200:259–269

    PubMed  CAS  Google Scholar 

  • McNaughton N, Kelly PH, Gray JA (1980b) Unilateral blockade of the dorsal ascending noradrenergic bundle and septal elicitation of hippocampal theta rhythm. Neurosci Lett 18:67–72

    PubMed  CAS  Google Scholar 

  • McNaughton N, Ruan M, Woodnorth MA (2006) Restoring theta-like rhythmicity in rats restores initial learning in the Morris water maze. Hippocampus 16:1102–1110

    PubMed  Google Scholar 

  • Meltzer H (1989) Serotonergic dysfunction in depression. Br J Psychiatry Suppl 8:25–31

    PubMed  Google Scholar 

  • Mena-Segovia J, Micklem BR, Nair-Roberts RG, Ungless MA, Bolam JP (2009) GABAergic neuron distribution in the pedunculopontine nucleus defines functional subterritories. J Comp Neurol 515:397–408

    PubMed  CAS  Google Scholar 

  • Milner B (1972) Disorders of learning and memory after temporal lobe lesions in man. Clin Neurosurg 19:421–446

    PubMed  CAS  Google Scholar 

  • Mitchell SJ, Rawlins JN, Steward O, Olton DS (1982) 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 2:292–302

    PubMed  CAS  Google Scholar 

  • Monmaur P, Thomson MA (1986) Spatial distribution of hippocampal-dentate theta rhythm following colchicine injection into the hippocampal formation of the rat. Brain Res 365:269–277

    PubMed  CAS  Google Scholar 

  • Montoya CP, Heynen AJ, Faris PD, Sainsbury RS (1989) Modality specific type 2 theta production in the immobile rat. Behav Neurosci 103:106–111

    PubMed  CAS  Google Scholar 

  • Nilsson OG, Bjorklund A (1992) Behaviour-dependent changes in acetylcholine release in normal and graft-reinnervated hippocampus: evidence for host regulation of grafted cholinergic neurons. Neuroscience 49:33–44

    PubMed  CAS  Google Scholar 

  • Nilsson OG, Leanza G, Rosenblad C, Lappi DA, Wiley RG, Bjorklund A (1992) Spatial learning impairments in rats with selective immunolesion of the forebrain cholinergic system. NeuroReport 3:1005–1008

    PubMed  CAS  Google Scholar 

  • Nishikawa T, Scatton B (1985) Inhibitory influence of GABA on central serotonergic transmission. Raphe nuclei as the neuroanatomical site of the GABAergic inhibition of cerebral serotonergic neurons. Brain Res 331:91–103

    PubMed  CAS  Google Scholar 

  • Nitz DA, McNaughton BL (1999) Hippocampal EEG and unit activity responses to modulation of serotonergic median raphe neurons in the freely behaving rat. Learn Mem 6:153–167

    PubMed  CAS  Google Scholar 

  • Nokia MS, Penttonen M, Korhonen T, Wikgren J (2008) Hippocampal theta (3–8 Hz) activity during classical eyeblink conditioning in rabbits. Neurobiol Learn Mem 90:62–70

    PubMed  Google Scholar 

  • Nowacka A, Jurkowlaniec E, Trojniar W (2002) Microinjection of procaine into the pedunculopontine tegmental nucleus suppresses hippocampal theta rhythm in urethane-anesthetized rats. Brain Res Bull 58:377–384

    PubMed  CAS  Google Scholar 

  • O′keefe J, Nadel L (1978) The hippocampus as a cognitive map. Clarendon Press, Oxford

    Google Scholar 

  • Oddie SD, Bland BH (1998) Hippocampal formation theta activity and movement selection. Neurosci Biobehav Rev 22:221–231

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Olvera-Cortes E, Cervantes M, Gonzalez-Burgos I (2002) Place-learning, but not cue-learning training, modifies the hippocampal theta rhythm in rats. Brain Res Bull 58:261–270

    PubMed  CAS  Google Scholar 

  • Olvera-Cortes E, Guevara MA, Gonzalez-Burgos I (2004) Increase of the hippocampal theta activity in the Morris water maze reflects learning rather than motor activity. Brain Res Bull 62:379–384

    PubMed  Google Scholar 

  • Olvera-Cortes ME, Garcia-Alcantar I, Gutierrez-Guzman B, Hernandez-Perez JJ, Lopez-Vazquez MA, Cervantes M (2012) Differential learning-related changes in theta activity during place learning in young and old rats. Behav Brain Res 226:555–562

    PubMed  Google Scholar 

  • Pan WX, McNaughton N (1997) The medial supramammillary nucleus, spatial learning and the frequency of hippocampal theta activity. Brain Res 764:101–108

    PubMed  CAS  Google Scholar 

  • Peck BK, Vanderwolf CH (1991) Effects of raphe stimulation on hippocampal and neocortical activity and behaviour. Brain Res 568:244–252

    PubMed  CAS  Google Scholar 

  • Petsche H, Stumpf C (1960) Topographic and toposcopic study of origin and spread of the regular synchronized arousal pattern in the rabbit. Electroencephalogr Clin Neurophysiol 12:589–600

    PubMed  CAS  Google Scholar 

  • Petsche H, Stumpf C, Gogolak G (1962) 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 14:202–211

    PubMed  CAS  Google Scholar 

  • Pitsikas N, Sakellaridis N (2005) The 5-HT2C receptor antagonist RO 60-0491 counteracts rats’ retention deficits in a recognition memory task. Brain Res 1054:200–202

    PubMed  CAS  Google Scholar 

  • Porter R, Adey WR, Brown TS (1964) Effects of small hippocampal lesions on locally recorded potentials and on behavior performance in the cat. Exp Neurol 10:216–235

    PubMed  CAS  Google Scholar 

  • Reznic J, Staubli U (1997) Effects of 5-HT3 receptor antagonism on hippocampal cellular activity in the freely moving rat. J Neurophysiol 77:517–521

    PubMed  CAS  Google Scholar 

  • Riedel WJ, Klaassen T, Schmitt JA (2002) Tryptophan, mood, and cognitive function. Brain Behav Immun 16:581–589

    PubMed  CAS  Google Scholar 

  • Riedel WJ, Sobczak S, Schmitt JA (2003) Tryptophan modulation and cognition. Adv Exp Med Biol 527:207–213

    PubMed  CAS  Google Scholar 

  • Riedel WJ, Eikmans K, Heldens A, Schmitt JA (2005) Specific serotonergic reuptake inhibition impairs vigilance performance acutely and after subchronic treatment. J Psychopharmacol 19:12–20

    PubMed  CAS  Google Scholar 

  • Riekkinen M, Sirvio J, Toivanen T, Riekkinen P Jr (1995) Combined treatment with a 5HT1A receptor agonist and a muscarinic acetylcholine receptor antagonist disrupts water maze navigation behavior. Psychopharmacology 122:137–146

    PubMed  CAS  Google Scholar 

  • Ruan M, Young CK, McNaughton N (2011) Minimal driving of hippocampal theta by the supramammillary nucleus during water maze learning. Hippocampus 21:1074–1081

    PubMed  Google Scholar 

  • Sailer S, Stumpf C (1957) Beeinflussbarkeit der Rhinencephalen tatigkeit des Kaninchens. Arch Exp Pathol Pharmakol 231:63–77

    CAS  Google Scholar 

  • Sainsbury RS, Heynen A, Montoya CP (1987) Behavioral correlates of hippocampal type 2 theta in the rat. Physiol Behav 39:513–519

    PubMed  CAS  Google Scholar 

  • Sambeth A, Meeter M, Blokland A (2009) Hippocampal theta frequency and novelty. Hippocampus 19:407–408 (author reply 409–410)

    PubMed  Google Scholar 

  • Sarihi A, Motamedi F, Naghdi N, Rashidy-Pour A (2000) Lidocaine reversible inactivation of the median raphe nucleus has no effect on reference memory but enhances working memory versions of the Morris water maze task. Behav Brain Res 114:1–9

    PubMed  CAS  Google Scholar 

  • Satoh K, Armstrong DM, Fibiger HC (1983) A comparison of the distribution of central cholinergic neurons as demonstrated by acetylcholinesterase pharmacohistochemistry and choline acetyltransferase immunohistochemistry. Brain Res Bull 11:693–720

    PubMed  CAS  Google Scholar 

  • Schmitt JA, Jorissen BL, Sobczak S, van Boxtel MP, Hogervorst E, Deutz NE et al (2000) Tryptophan depletion impairs memory consolidation but improves focussed attention in healthy young volunteers. J Psychopharmacol 14:21–29

    PubMed  CAS  Google Scholar 

  • Schmitt JA, Kruizinga MJ, Riedel WJ (2001) Non-serotonergic pharmacological profiles and associated cognitive effects of serotonin reuptake inhibitors. J Psychopharmacol 15:173–179

    PubMed  CAS  Google Scholar 

  • Segal M (1975) Physiological and pharmacological evidence for a serotonergic projection to the hippocampus. Brain Res 94:115–131

    PubMed  CAS  Google Scholar 

  • Segal M (1976) 5-HT antagonists in rat hippocampus. Brain Res 103:161–166

    PubMed  CAS  Google Scholar 

  • Semba K, Fibiger HC (1989) Organization of central cholinergic systems. Prog Brain Res 79:37–63

    PubMed  CAS  Google Scholar 

  • Shahidi S, Motamedi F, Naghdi N (2004) Effect of reversible inactivation of the supramammillary nucleus on spatial learning and memory in rats. Brain Res 1026:267–274

    PubMed  CAS  Google Scholar 

  • Smythe JW, Cristie 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

    PubMed  CAS  Google Scholar 

  • Sobczak S, Honig A, Schmitt JA, Riedel WJ (2003) Pronounced cognitive deficits following an intravenous l-tryptophan challenge in first-degree relatives of bipolar patients compared to healthy controls. Neuropsychopharmacology 28:711–719

    PubMed  CAS  Google Scholar 

  • Sorman E, Wang D, Hajos M, Kocsis B (2011) Control of hippocampal theta rhythm by serotonin: role of 5-HT2c receptors. Neuropharmacology 61:489–494

    PubMed  CAS  Google Scholar 

  • Sotty F, Danik M, Manseau F, Laplante F, Quirion R, Williams S (2003) Distinct electrophysiological properties of glutamatergic, cholinergic and GABAergic rat septohippocampal neurons: novel implications for hippocampal rhythmicity. J Physiol 551:927–943

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Staubli U, Xu FB (1995) Effects of 5-HT3 receptor antagonism on hippocampal theta rhythm, memory, and LTP induction in the freely moving rat. J Neurosci 15:2445–2452

    PubMed  CAS  Google Scholar 

  • Steckler T, Sahgal A (1995) The role of serotonergic–cholinergic interactions in the mediation of cognitive behaviour. Behav Brain Res 67:165–199

    PubMed  CAS  Google Scholar 

  • Steininger TL, Wainer BH, Blakely RD, Rye DB (1997) Serotonergic dorsal raphe nucleus projections to the cholinergic and noncholinergic neurons of the pedunculopontine tegmental region: a light and electron microscopic anterograde tracing and immunohistochemical study. J Comp Neurol 382:302–322

    PubMed  CAS  Google Scholar 

  • Stubley-Weatherly L, Harding JW, Wright JW (1996) Effects of discrete kainic acid-induced hippocampal lesions on spatial and contextual learning and memory in rats. Brain Res 716:29–38

    PubMed  CAS  Google Scholar 

  • Stumpf C, Petsche H, Gogolak G (1962) The significance of the rabbit’s septum as a relay station between the midbrain and the hippocampus. II. The differential influence of drugs upon both the septal cell firing pattern and the hippocampus theta activity. Electroencephalogr Clin Neurophysiol 14:212–219

    PubMed  CAS  Google Scholar 

  • Takano Y, Hanada Y (2009) The driving system for hippocampal theta in the brainstem: an examination by single neuron recording in urethane-anesthetized rats. Neurosci Lett 455:65–69

    PubMed  CAS  Google Scholar 

  • Tibrewal P, Kumar HB, Shubha GN, Subhashree D, Purushottam M, Thennarasu K et al (2010) Association of serotonin transporter gene polymorphisms with obsessive-compulsive disorder (OCD) in a south Indian population. Indian J Med Res 132:690–695

    PubMed  CAS  Google Scholar 

  • Toth K, Freund TF, Miles R (1997) Disinhibition of rat hippocampal pyramidal cells by GABAergic afferents from the septum. J Physiol 500:463–474

    PubMed  CAS  Google Scholar 

  • Vanderwolf CH (1969) Hippocampal electrical activity and voluntary movement in the rat. Electroencephalogr Clin Neurophysiol 26:407–418

    PubMed  CAS  Google Scholar 

  • Vanderwolf CH (1987) Near-total loss of ‘learning’ and ‘memory’ as a result of combined cholinergic and serotonergic blockade in the rat. Behav Brain Res 23:43–57

    PubMed  CAS  Google Scholar 

  • Vanderwolf CH (1988) Cerebral activity and behavior: control by central cholinergic and serotonergic systems. Int Rev Neurobiol 30:225–340

    PubMed  CAS  Google Scholar 

  • Vanderwolf CH, Baker GB (1986) Evidence that serotonin mediates non-cholinergic neocortical low voltage fast activity, non-cholinergic hippocampal rhythmical slow activity and contributes to intelligent behavior. Brain Res 374:342–356

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Velluti JC, Buño WJ (1973) Actividad rítmica del hipocampo y movimiento. Acta Physiol Lat 23:361

    Google Scholar 

  • Vertes RP (1981) An analysis of ascending brain stem systems involved in hippocampal synchronization and desynchronization. J Neurophysiol 46:1140–1159

    PubMed  CAS  Google Scholar 

  • Vertes RP (1986) Brainstem modulation of the hippocampus. Anatomy, physiology and significance. In: Isaacson RL, Pribram KH (eds) The hippocampus. Plenum, New York, pp 41–75

    Google Scholar 

  • Vertes RP (1991) A PHA-L analysis of ascending projections of the dorsal raphe nucleus in the rat. J Comp Neurol 313:643–668

    PubMed  CAS  Google Scholar 

  • Vertes RP (2005) Hippocampal theta rhythm: a tag for short-term memory. Hippocampus 15:923–935

    PubMed  CAS  Google Scholar 

  • Vertes RP, Kocsis B (1997) Brainstem-diencephalon-septohippocampal systems controlling the theta rhythm of the hippocampus. Neuroscience 81:893–926

    PubMed  CAS  Google Scholar 

  • Vertes RP, Linley SB (2007) Comparison of projections of the dorsal and median raphe nuclei, with some functional considerations. Int Congr Ser 1304:98–120

    Google Scholar 

  • Vertes RP, Colom LV, Fortin WJ, Bland BH (1993) Brainstem sites for the carbachol elicitation of the hippocampal theta rhythm in the rat. Exp Brain Res 96:419–429

    PubMed  CAS  Google Scholar 

  • Vertes RP, Kinney GG, Kocsis B, Fortin WJ (1994) Pharmacological suppression of the median raphe nucleus with serotonin1A agonists, 8-OH-DPAT and buspirone, produces hippocampal theta rhythm in the rat. Neuroscience 60:441–451

    PubMed  CAS  Google Scholar 

  • Vertes RP, Fortin WJ, Crane AM (1999) Projections of the median raphe nucleus in the rat. J Comp Neurol 407:555–582

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Vinogradova OS (1995) Expression, control, and probable functional significance of the neuronal theta-rhythm. Prog Neurobiol 45:523–583

    PubMed  CAS  Google Scholar 

  • Vinogradova OS (2001) Hippocampus as comparator: role of the two input and two output systems of the hippocampus in selection and registration of information. Hippocampus 11:578–598

    PubMed  CAS  Google Scholar 

  • Vinogradova OS, Brazhnik ES, Stafekhina VS, Kichigina VF (1995) Modulation of septal influences on hippocampal neurons by cholinergic substances. Neurosci Behav Physiol 25:453–461

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Wang HL, Morales M (2009) Pedunculopontine and laterodorsal tegmental nuclei contain distinct populations of cholinergic, glutamatergic and GABAergic neurons in the rat. Eur J Neurosci 29:340–358

    PubMed  Google Scholar 

  • Watrous AJ, Fried I, Ekstrom AD (2011) Behavioral correlates of human hippocampal delta and theta oscillations during navigation. J Neurophysiol 105:1747–1755

    PubMed  Google Scholar 

  • Williams JM, Givens B (2003) Stimulation-induced reset of hippocampal theta in the freely performing rat. Hippocampus 13:109–116

    PubMed  CAS  Google Scholar 

  • Winson J (1978) Loss of hippocampal theta rhythm results in spatial memory deficit in the rat. Science 201:160–163

    PubMed  CAS  Google Scholar 

  • Wirtshafter D, Asin KE (1983) Impaired radial maze performance in rats with electrolytic median raphe lesions. Exp Neurol 79:412–421

    PubMed  CAS  Google Scholar 

  • Woolley ML, Marsden CA, Fone KC (2004) 5-HT6 receptors. Curr Drug Targets CNS Neurol Disord 3:59–79

    PubMed  CAS  Google Scholar 

  • Yoder RM, Pang KC (2005) Involvement of GABAergic and cholinergic medial septal neurons in hippocampal theta rhythm. Hippocampus 15:381–392

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the Consejo Nacional de Ciencia y Tecnología no. CB-2010-01 and no. CB-2010-01/150959.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to María Esther Olvera-Cortés.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Olvera-Cortés, M.E., Gutiérrez-Guzmán, B.E., López-Loeza, E. et al. Serotonergic modulation of hippocampal theta activity in relation to hippocampal information processing. Exp Brain Res 230, 407–426 (2013). https://doi.org/10.1007/s00221-013-3679-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-013-3679-x

Keywords

Navigation