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J. Sprouse, G. Aghajanian (1987)
Electrophysiological responses of serotoninergic dorsal raphe neurons to 5‐HT1A and 5‐HT1B agonistsSynapse, 1
V. Varga, A. Losonczy, B. Zemelman, Z. Borhegyi, G. Nyiri, A. Domonkos, B. Hangya, Noémi Holderith, J. Magee, T. Freund (2009)
Fast Synaptic Subcortical Control of Hippocampal CircuitsScience, 326
J. McKenna, R. Vertes (2001)
Collateral projections from the median raphe nucleus to the medial septum and hippocampusBrain Research Bulletin, 54
B. Hangya, Z. Borhegyi, N. Szilágyi, T. Freund, V. Varga (2009)
GABAergic Neurons of the Medial Septum Lead the Hippocampal Network during Theta ActivityThe Journal of Neuroscience, 29
G. Kinney, B. Kocsis, R. Vertes (1995)
Injections of muscimol into the median raphe nucleus produce hippocampal theta rhythm in the urethane anesthetized ratPsychopharmacology, 120
R. Vertes, W. Fortin, A. Crane (1999)
Projections of the median raphe nucleus in the ratJournal of Comparative Neurology, 407
T. Freund, M. Antal (1988)
GABA-containing neurons in the septum control inhibitory interneurons in the hippocampusNature, 336
R. Vertes, Walter Hoover, G. Prisco (2004)
Theta rhythm of the hippocampus: subcortical control and functional significance.Behavioral and cognitive neuroscience reviews, 3 3
M. Alreja (1996)
Excitatory actions of serotonin on GABAergic neurons of the medial septum and diagonal band of brocaSynapse, 22
L. Calizo, Adaure Akanwa, Xiao-Hong Ma, Yu-zhen Pan, Julia Lemos, C. Craige, Lydia Heemstra, S. Beck (2011)
Raphe serotonin neurons are not homogenous: Electrophysiological, morphological and neurochemical evidenceNeuropharmacology, 61
V. Varga, B. Hangya, Kinga Kránitz, Anikó Ludányi, Rita Zemankovics, I. Katona, R. Shigemoto, T. Freund, Z. Borhegyi (2008)
The presence of pacemaker HCN channels identifies theta rhythmic GABAergic neurons in the medial septumThe Journal of Physiology, 586
V. Varga, A. Sik, T. Freund, B. Kocsis (2002)
GABAB receptors in the median raphe nucleus: distribution and role in the serotonergic control of hippocampal activityNeuroscience, 109
B. Peck, C. Vanderwolf (1991)
Effects of raphe stimulation on hippocampal and neocortical activity and behaviourBrain Research, 568
C. Gras, E. Herzog, G. Bellenchi, V. Bernard, P. Ravassard, M. Pohl, B. Gasnier, B. Giros, S. Mestikawy (2002)
A Third Vesicular Glutamate Transporter Expressed by Cholinergic and Serotoninergic NeuronsThe Journal of Neuroscience, 22
O. Vinogradova, J. Lisman (2001)
Hippocampus as comparator: Role of the two input and two output systems of the hippocampus in selection and registration of informationHippocampus, 11
J. Kiss, Á. Csáki, H. Bokor, M. Shanabrough, C. Léránth (2000)
The supramammillo-hippocampal and supramammillo-septal glutamatergic/aspartatergic projections in the rat: a combined [3H]d-aspartate autoradiographic and immunohistochemical studyNeuroscience, 97
B. Bland, S. Oddie (2001)
Theta band oscillation and synchrony in the hippocampal formation and associated structures: the case for its role in sensorimotor integrationBehavioural Brain Research, 127
G. Kinney, B. Kocsis, R. Vertes (1994)
Injections of excitatory amino acid antagonists into the median raphe nucleus produce hippocampal theta rhythm in the urethane-anesthetized ratBrain Research, 654
Kenneth Green, Kenneth Green, J. Rawlins, J. Rawlins (1979)
Hippocampal theta in rats under urethane: generators and phase relations.Electroencephalography and clinical neurophysiology, 47 4
J. Smythe, L. Colom, B. Bland (1992)
The extrinsic modulation of hippocampal theta depends on the coactivation of cholinergic and GABA-ergic medial septal inputsNeuroscience & Biobehavioral Reviews, 16
S. Mitchell, J. Rawlins, O. Steward, D. Olton (1982)
Medial septal area lesions disrupt theta rhythm and cholinergic staining in medial entorhinal cortex and produce impaired radial arm maze behavior in rats, 2
R. Vertes (1981)
An analysis of ascending brain stem systems involved in hippocampal synchronization and desynchronization.Journal of neurophysiology, 46 5
Tsuneyuki Yamamoto, Shigenori Watanabe, R. Oishi, S. Ueki (1979)
Effects of midbrain raphe stimulation and lesion on EEG activity in ratsBrain Research Bulletin, 4
Mark Stewart, Steven Fox (1989)
Two populations of rhythmically bursting neurons in rat medial septum are revealed by atropine.Journal of neurophysiology, 61 5
Elin Sörman, Da-ning Wang, M. Hajós, B. Kocsis (2011)
Control of hippocampal theta rhythm by serotonin: Role of 5-HT2c receptorsNeuropharmacology, 61
B. Bland, Shandra Declerck, Jesse Jackson, S. Glasgow, S. Oddie (2007)
Septohippocampal properties of N‐methyl‐D‐aspartate‐induced theta‐band oscillation and synchronySynapse, 61
E. Azmitia, M. Segal (1978)
An autoradiographic analysis of the differential ascending projections of the dorsal and median raphe nuclei in the ratJournal of Comparative Neurology, 179
T. Freund, A. Gulyás, L. Acsády, T. Görcs, K. Tóth (1990)
Serotonergic control of the hippocampus via local inhibitory interneurons.Proceedings of the National Academy of Sciences of the United States of America, 87
D. Wirtshafter, M. Klitenick, K. Asin (1987)
Evidence against serotonin involvement in the hyperactivity produced by injections of muscimol into the median raphe nucleusPharmacology Biochemistry and Behavior, 27
M. Frotscher, C. Léránth (1985)
Cholinergic innervation of the rat hippocampus as revealed by choline acetyltransferase immunocytochemistry: A combined light and electron microscopic studyJournal of Comparative Neurology, 239
Jesse Jackson, B. Bland, M. Antle (2009)
Nonserotonergic projection neurons in the midbrain raphe nuclei contain the vesicular glutamate transporter VGLUT3Synapse, 63
B. Bland, L. Colom (1993)
Extrinsic and intrinsic properties underlying oscillation and synchrony in limbic cortexProgress in Neurobiology, 41
Min Wu, M. Shanabrough, C. Léránth, M. Alreja (2000)
Cholinergic Excitation of Septohippocampal GABA But Not Cholinergic Neurons: Implications for Learning and MemoryThe Journal of Neuroscience, 20
E. Maru, L. Takahashi, S. Iwahara (1979)
Effects of median raphe nucleus lesions on hippocampal EEG in the freely moving ratBrain Research, 163
D. Nitz, B. McNaughton (1999)
Hippocampal EEG and unit activity responses to modulation of serotonergic median raphe neurons in the freely behaving rat.Learning & memory, 6 2
Carey Huh, R. Goutagny, Sylvain Williams (2010)
Glutamatergic Neurons of the Mouse Medial Septum and Diagonal Band of Broca Synaptically Drive Hippocampal Pyramidal Cells: Relevance for Hippocampal Theta RhythmThe Journal of Neuroscience, 30
L. Colom, Maria Castañeda, T. Reyna, Sofia Hernandez, E. Garrido‐sanabria (2005)
Characterization of medial septal glutamatergic neurons and their projection to the hippocampusSynapse, 58
J. Kiss, Á. Csáki, H. Bokor, K. Kocsis, Bernat Kocsis (2002)
Possible glutamatergic/aspartatergic projections to the supramammillary nucleus and their origins in the rat studied by selective [3H]D-aspartate labelling and immunocytochemistryNeuroscience, 111
Jesse Jackson, C. Dickson, B. Bland (2008)
Median raphe stimulation disrupts hippocampal theta via rapid inhibition and state-dependent phase reset of theta-related neural circuitry.Journal of neurophysiology, 99 6
S. Assaf, J. Miller (1978)
The role of a raphe serotonin system in the control of septal unit activity and hippocampal desynchronizationNeuroscience, 3
K. Asin, D. Wirtshafter, H. Fibiger (1985)
Electrolytic, but not 5,7-dihydroxytryptamine, lesions of the nucleus medianus raphe impair acquisition of a radial maze task.Behavioral and neural biology, 44 3
J. Winson (1978)
Loss of hippocampal theta rhythm results in spatial memory deficit in the rat.Science, 201 4351
G. Buzsáki (2002)
Theta Oscillations in the HippocampusNeuron, 33
O. Vinogradova, V. Kitchigina, T. Kudina, K. Zenchenko (1999)
Spontaneous activity and sensory responses of hippocampal neurons during persistent theta-rhythm evoked by median raphe nucleus blockade in rabbitNeuroscience, 94
K. Halasy, R. Miettinen, E. Szabat, T. Freund (1992)
GABAergic Interneurons are the Major Postsynaptic Targets of Median Raphe Afferents in the Rat Dentate GyrusEuropean Journal of Neuroscience, 4
Shaomin Li, V. Varga, A. Sik, B. Kocsis (2005)
GABAergic control of the ascending input from the median raphe nucleus to the limbic system.Journal of neurophysiology, 94 4
C. Léránth, R. Vertes (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 EEGJournal of Comparative Neurology, 410
R. Vertes, B. Kocsis (1997)
Brainstem-diencephalo-septohippocampal systems controlling the theta rhythm of the hippocampus.Neuroscience, 81 4
V. Kitchigina, T. Kudina, E. Kutyreva, O. Vinogradova (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 rabbitNeuroscience, 94
C. Köhler, S. Lorens (1978)
Open field activity and avoidance behavior following serotonin depletion: A comparison of the effects of parachlorophenylalanine and electrolytic midbrain raphe lesionsPharmacology Biochemistry and Behavior, 8
B. Bland (2008)
Information Processing by Neuronal Populations: Anatomical, physiological, and pharmacological properties underlying hippocampal sensorimotor integration
Florence Sotty, M. Danik, F. Manseau, F. Laplante, Rémi Quirion, Sylvain Williams (2003)
Distinct electrophysiological properties of glutamatergic, cholinergic and GABAergic rat septohippocampal neurons: novel implications for hippocampal rhythmicityThe Journal of Physiology, 551
G. Kinney, B. Kocsis, R. Vertes (1996)
Medial septal unit firing characteristics following injections of 8-OH-DPAT into the median raphe nucleusBrain Research, 708
B. Kocsis, R. Vertes (1996)
Midbrain raphe cell firing and hippocampal theta rhythm in urethane‐anaesthetized ratsNeuroReport, 7
Shaomin Li, I. Topchiy, B. Kocsis (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 ratsSynapse, 61
M. Stewart, S. Fox (1989)
Detection of an atropine-resistant component of the hippocampal theta rhythm in urethane-anesthetized ratsBrain Research, 500
R. Fremeau, Jonathon Burman, Tayyaba Qureshi, Cindy Tran, J. Proctor, Juliette Johnson, Hui Zhang, D. Sulzer, D. Copenhagen, J. Storm-Mathisen, R. Reimer, F. Chaudhry, R. Edwards (2002)
The identification of vesicular glutamate transporter 3 suggests novel modes of signaling by glutamateProceedings of the National Academy of Sciences of the United States of America, 99
S. Beck, Yu-zhen Pan, Adaure Akanwa, L. Kirby (2004)
Median and dorsal raphe neurons are not electrophysiologically identical.Journal of neurophysiology, 91 2
M. Hasselmo (2006)
The role of acetylcholine in learning and memoryCurrent Opinion in Neurobiology, 16
W. Liu, M. Alreja (1997)
Atypical antipsychotics block the excitatory effects of serotonin in septohippocampal neurons in the ratNeuroscience, 79
Jeffery Sprouse, G. Aghajanian (1986)
(-)-Propranolol blocks the inhibition of serotonergic dorsal raphe cell firing by 5-HT1A selective agonists.European journal of pharmacology, 128 3
R. Vertes, G. Kinney, B. Kocsis, W. Fortin (1994)
Pharmacological suppression of the median raphe nucleus with serotonin1a agonists, 8-OH-DPAT and buspirone, produces hippocampal theta rhythm in the ratNeuroscience, 60
Axelle Simon, F. Poindessous-jazat, P. Dutar, J. Epelbaum, M. Bassant (2006)
Firing Properties of Anatomically Identified Neurons in the Medial Septum of Anesthetized and Unanesthetized Restrained RatsThe Journal of Neuroscience, 26
V. Crunelli, M. Segal (1985)
An electrophysiological study of neurones in the rat median raphe and their projections to septum and hippocampusNeuroscience, 15
S. Assaf, J. Miller (1978)
Neuronal transmission in the dentate gyrus: role of inhibitory mechanismsBrain Research, 151
J. Sprouse (1991)
Inhibition of dorsal raphe cell firing by MDL 73005EF, a novel 5-HT1A receptor ligand.European journal of pharmacology, 201 2-3
S. Oddie, I. Kirk, I. Whishaw, B. Bland (1997)
Hippocampal formation is involved in movement selection: evidence from medial septal cholinergic modulation and concurrent slow-wave (theta rhythm) recordingBehavioural Brain Research, 88
C. Fornal, W. Litto, C. Metzler, F. Marrosu, K. Tada, B. Jacobs (1994)
Single-unit responses of serotonergic dorsal raphe neurons to 5-HT1A agonist and antagonist drug administration in behaving cats.The Journal of pharmacology and experimental therapeutics, 270 3
R. Moore, A. Halaris (1975)
Hippocampal innervation by serotonin neurons of the midbrain raphe in the ratJournal of Comparative Neurology, 164
V. Lawson, B. Bland (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 ProcaineExperimental Neurology, 120
G. Prisco, Zimbul Albo, R. Vertes, B. Kocsis (2002)
Discharge properties of neurons of the median raphe nucleus during hippocampal theta rhythm in the ratExperimental Brain Research, 145
R. Vertes (1992)
PHA‐L analysis of projections from the supramammillary nucleus in the ratJournal of Comparative Neurology, 326
N. McNaughton, E. Azmitia, J. Williams, A. Buchan, J. Gray (1980)
Septal elicitation of hippocampal theta rhythm after localized de-afferentation of serotoninergic fibersBrain Research, 200
(2000)
J Neurosci
I. Kirk, N. McNaughton (1993)
Mapping the differential effects of procaine on frequency and amplitude of reticularly elicited hippocampal rhythmical slow activityHippocampus, 3
Hippocampal theta rhythms in vivo are modulated by a synchronizing projection from the medial septum (MS) and a desynchronizing input from the median raphe nucleus (MRn) of the brainstem. Inactivation of the MS suppresses theta rhythms while inactivation of the median raphe produces persistent theta. However, different pathways arise from within the MS and the median raphe and therefore different brain states could be facilitated by different forms of median raphe or septohippocampal inputs. Here, we found in urethane anesthetized rats that suppression of outputs from the MRn with procaine leads to persistent hippocampal theta as previously reported. The discharge properties of hippocampal theta‐related cells recorded during both spontaneously occurring theta and MRn 8‐OH‐DPAT‐induced theta did not differ significantly. This persistent theta was abolished by inactivation of the MS with either procaine or atropine sulfate. Selective inactivation of serotonergic median raphe outputs with the 5‐HT‐1A agonist (8‐OH‐DPAT) induced theta that was also abolished by medial septal inactivation using procaine. Thus, persistent theta following complete median raphe inactivation or selective serotonergic inactivation arises from a median raphe to MS pathway. However, 8‐OH‐DPAT infusions into the median raphe together with atropine infusions in the MS did not abolish theta activity. These data suggest that the non‐serotonergic (possibly glutamatergic) median raphe projections to the MS can facilitate the generation of hippocampal theta in the absence of medial septal cholinergic tone. These results demonstrate that dissociable neuronal pathways in the median raphe–MS–hippocampal circuit promote different brain states (theta or non‐theta) and a median raphe non‐serotonergic (likely glutamatergic) system may serve a separate function from the ascending serotonergic raphe projection in the regulation of hippocampal network activity. © 2011 Wiley Periodicals, Inc.
Hippocampus – Wiley
Published: Jul 1, 2012
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