PHA-L analysis of projections from the supramammillary nucleus in the rat

Vertes, Robert P.

doi:10.1002/cne.903260408

Cited by 299Memory and Neural MechanismsNeuroscience and Neuropharmacology ResearchRegulation of Appetite and Obesity

PHA-L analysis of projections from the supramammillary nucleus in the rat

Vertes, Robert P.·1992·Journal of Comparative Neurology

DOI 10.1002/cne.903260408

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Abstract

The projections of the supramammillary nucleus (SUM) were examined in the rat by the anterograde anatomical tracer Phaseolus vulgaris leucoagglutinin (PHA-L). The majority of labeled fibers from SUM ascended through the forebrain within the medial forebrain bundle. SUM fibers were found to terminate heavily in the hippocampal formation, specifically within the granule cell layer and immediately adjoining molecular layer of the dentate gyrus. In addition, SUM fibers were shown to distribute densely to several structures with strong connections with the hippocampus, namely, the nucleus reunions of the thalamus, the medial and lateral septum, the entorhinal cortex, and the endopiriform nucleus. SUM fibers were also shown to project significantly to several additional subcortical and cortical sites. The subcortical sites were the dorsal raphe nucleus, the midbrain central gray, the fields of Forel/zona incerta, the dorsomedial hypothalamic area, midline/intralaminar nuclei of the thalamus (posterior paraventricular, rhomboid, central medial, intermediodorsal, and mediodorsal), the medial and lateral preoptic areas, the bed nucleus of the stria terminalis, the substantia innominata, the vertical limb of the diagonal band nucleus, and the claustrum. The cortical sites were the occipital, temporal, parietal, and frontal cortices. Some notable differences were observed in projections from the lateral as compared to the medial SUM. For example, fibers originating from the lateral SUM distributed heavily to the hippocampal formation and parts of the cortex, whereas those from the medial SUM projected sparsely to these two regions. The SUM projections to the hippocampal formation and associated structures may serve as the substrate for a SUM involvement in the generation of the theta rhythm of the hippocampus and the gating of information flow through the hippocampal formation.

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The nucleus of the diagonal band also receives innervations from the posterior hypothalamic area including the supramammillary nucleus.
“which also receives innervations from the posterior hypothalamic area including the supramammillary nucleus”
From Dopamine reward circuitry: Two projection systems from the ventral midbrain to the nucleus accumbens–olfactory tubercle complex (2007) · cites this paper as Vertes, 1992

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The dentate gyrus: fundamental neuroanatomical organization (dentate gyrus for dummies)
Amaral, D. G., Scharfman, H. E., & Lavenex, P. (2007) · Progress in brain research · doi:10.1016/s0079-6123(07)63001-5 · Cited by 888 · see citing works
“The major hypothalamic projection to the dentate gyrus arises from a population of large cells in the supramammillary area that caps and partially surrounds the medial mammillary nuclei ( Wyss et al., 1979; Dent et al., 1983; Vertes, 1993; Magloczky et al., 1994).”
Background
Connections of the rat lateral septal complex 1Published on the World Wide Web on 2 June 1997. 1
Risold, P. Y., & Swanson, L. W. (1997) · Brain Research Reviews · doi:10.1016/s0165-0173(97)00009-x · Cited by 671 · see citing works
The reinterpretation of dreams: An evolutionary hypothesis of the function of dreaming
Revonsuo, A. (2000) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00004015 · Cited by 676 · see citing works
Trpv1 Reporter Mice Reveal Highly Restricted Brain Distribution and Functional Expression in Arteriolar Smooth Muscle Cells
Cavanaugh, D. J., Chesler, A. T., Jackson, A. C., Sigal, Y. M., Yamanaka, H., Grant, R., O'Donnell, D., Nicoll, R. A., Shah, N. M., Julius, D., et al. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.6451-10.2011 · Cited by 542 · see citing works
“For example, SuM neurons are known to project heavily to the hippocampus (Vertes, 1992).”
Background
Fundamental Neuroscience
(2013) · Elsevier eBooks · doi:10.1016/c2010-0-65035-8 · Cited by 465 · see citing works
Brain reward circuitry beyond the mesolimbic dopamine system: a neurobiological theory
Ikemoto, S. (2010) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.02.001 · Cited by 454 · see citing works
Theta band oscillation and synchrony in the hippocampal formation and associated structures: the case for its role in sensorimotor integration
Bland, B. H., & Oddie, S. D. (2001) · Behavioural Brain Research · doi:10.1016/s0166-4328(01)00358-8 · Cited by 520 · see citing works
Limbic circuitry of the midline thalamus
Vertes, R. P., Linley, S. B., & Hoover, W. B. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.01.014 · Cited by 391 · see citing works
“They include: ACC/ventral pallidum, diagonal band nuclei, the anterior cortical, BLA and basomedial nuclei of the amygdala, VTA, the substantia nigra-pars compacta (SNc), the supramammillary nucleus, and the lateral entorhinal cortex (Groenewegen, 1988; Ray and Price, 1992; Vertes, 1992).”
BackgroundInfluential
The structural organization of connections between hypothalamus and cerebral cortex 1Published on the World Wide Web on 2 June 1997. 1
Risold, P., Thompson, R. H., & Swanson, L. W. (1997) · Brain Research Reviews · doi:10.1016/s0165-0173(97)00007-6 · Cited by 347 · see citing works
Hippocampal Formation
Witter, M. P., & Amaral, D. G. (2004) · Elsevier eBooks · doi:10.1016/b978-012547638-6/50022-5 · Cited by 344 · see citing works
Projections from bed nuclei of the stria terminalis, anteromedial area: Cerebral hemisphere integration of neuroendocrine, autonomic, and behavioral aspects of energy balance
Dong, H.-W., & Swanson, L. W. (2006) · The Journal of Comparative Neurology · doi:10.1002/cne.20788 · Cited by 290 · see citing works
Afferent projections to nucleus reuniens of the thalamus
McKenna, J. T., & Vertes, R. P. (2004) · The Journal of Comparative Neurology · doi:10.1002/cne.20342 · Cited by 272 · see citing works
“Our interest in RE stems in part from our previous demonstrations that the supramammillary nucleus (SUM; Vertes, 1992) and the posterior nucleus of the hypothalamus (PH; Vertes et al., 1995) send pronounced projections to RE.”
BackgroundResult
Hippocampal theta rhythm: A tag for short‐term memory
Vertes, R. P. (2005) · Hippocampus · doi:10.1002/hipo.20118 · Cited by 319 · see citing works
Analysis of projections from the medial prefrontal cortex to the thalamus in the rat, with emphasis on nucleus reuniens
Vertes, R. P. (2001) · The Journal of Comparative Neurology · doi:10.1002/cne.10083 · Cited by 266 · see citing works
“The SUM projects strongly to RE (Vertes, 1992) and may relay a theta rhythmic signal from SUM to RE (Vertes and Kocsis, 1997) possibly involved in gating the flow of information from mPFC to HF, by means of RE, during theta-associated states or behaviors.”
Background
The Corticohippocampal Circuit, Synaptic Plasticity, and MemoryPreprint
Basu, J., & Siegelbaum, S. A. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a021733 · Cited by 244 · see citing works
“CA2 has also been reported to project to the supramammillary nucleus (Cui et al. 2013), a hypothalamic region long known to provide strong input to CA2 (Haglund et al. 1984; Vertes 1992; Magloczky et al. 1994; Ochiishi et al. 1999; Kiss et al. 2000).”
Background
Projections from bed nuclei of the stria terminalis, dorsomedial nucleus: Implications for cerebral hemisphere integration of neuroendocrine, autonomic, and drinking responses
Dong, H., & Swanson, L. W. (2005) · The Journal of Comparative Neurology · doi:10.1002/cne.20790 · Cited by 249 · see citing works
“…from 1) lateral regions of the lateral hypothalamic area (Allen and Cechetto, 1993), 2) the medial and lateral parts of the supramammillary nucleus (Vertes, 1992), 3) histaminergic neurons of the tuberomammillary nucleus (Inagaki et al., 1988), 4) dopaminergic neurons of the ventral tegmental and…”
Background
Organization of inputs to the dorsomedial nucleus of the hypothalamus: a reexamination with Fluorogold and PHAL in the rat
Thompson, R. H. (1998) · Brain Research Reviews · doi:10.1016/s0165-0173(98)00010-1 · Cited by 247 · see citing works
Characterization of neurons of the supramammillary nucleus and mammillary body that discharge rhythmically with the hippocampal theta rhythm in the rat
Kocsis, B., & Vertes, R. P. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-11-07040.1994 · Cited by 242 · see citing works
“The SUM not only projects densely to the DG but also to several structures with pronounced input to the hippocampus including the nucleus reuniens of the thalamus, the medial and lateral septum and the entorhinal cortex (Vertes, 1992).”
BackgroundInfluential
Hippocampus, theta, and spatial memory
O'Keefe, J. M. (1993) · Current Opinion in Neurobiology · doi:10.1016/0959-4388(93)90163-s · Cited by 226 · see citing works
The supramammillary area: its organization, functions and relationship to the hippocampus
Pan, W.-X., & McNaughton, N. (2004) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2004.09.003 · Cited by 223 · see citing works
“Efferents from SuM SuM sends ascending projections to the diencephalon and telencephalon (Swanson, 1976, 1982; Shibata, 1987; Vertes, 1992; Hayakawa et al., 1993; Thinschmidt, 1993; Risold and Swanson, 1997; Vertes et al., 1999; Swanson and Cowan, 1975, 1979; Conrad and Pfaff, 1976; Saper et al., 1976; Krayniak et al.…”
BackgroundInfluential
Connections of the nucleus incertus
Goto, M., Swanson, L. W., & Canteras, N. S. (2001) · The Journal of Comparative Neurology · doi:10.1002/cne.1303 · Cited by 219 · see citing works
“…nuclei, the medial septal nucleus and nucleus of the diagonal band, and the dorsal and ventral tegmental nuclei (Swanson, 1982; Haglund et al., 1984; Taube, 1988; Vertes, 1992; Vertes et al., 1995; Vertes and Kocsis, 1997; Oddie and Bland, 1998; Sharp and Cho, 2000; Kocsis et al., 2001).”
Background
Hypothalamic and other connections with dorsal CA2 area of the mouse hippocampus
Cui, Z., Gerfen, C. R., & Young, W. S. (2013) · Journal of Comparative Neurology · doi:10.1002/cne.23263 · Cited by 214 · see citing works
“We confirmed earlier findings from tracer studies that SUM innervates the dorsal CA2 (Haglund et al., 1984; Vertes, 1992; Magloczky et al., 1994; Ochiishi et al., 1999; Kiss et al., 2000).”
Result
Organization of the avian “corticostriatal” projection system: A retrograde and anterograde pathway tracing study in pigeons
Veenman, C., Wild, J. M., & Reiner, A. J. (1995) · The Journal of Comparative Neurology · doi:10.1002/cne.903540108 · Cited by 217 · see citing works
Theta Rhythm of the Hippocampus: Subcortical Control and Functional Significance
Vertes, R. P., Hoover, W. B., & Prisco, G. V. D. (2004) · Behavioral and Cognitive Neuroscience Reviews · doi:10.1177/1534582304273594 · Cited by 213 · see citing works
“…to the hippocampus, whereas the SUM receives few fibers from the hippocampus but is the source of dense projections to the septum and hippocampus (Borhegyi et al., 1998; Haglund et al., 1984; Kiss et al., 2000; Leranth & Kiss, 1996; Magloczky et al., 1994; Vertes, 1992; Vertes & McKenna, 2000).”
BackgroundResult
The nucleus reuniens of the thalamus sits at the nexus of a hippocampus and medial prefrontal cortex circuit enabling memory and behaviorPreprint
der Weel, M. J. D.-V., Griffin, A. L., Ito, H., Shapiro, M. L., Witter, M. P., Vertes, R. P., & Allen, T. A. (2019) · Learning & Memory · doi:10.1101/lm.048389.118 · Cited by 201 · see citing works
Supramammillary glutamate neurons are a key node of the arousal system
Pedersen, N. P., Ferrari, L., Venner, A., Wang, J. L., Abbott, S. B. G., Vujovic, N., Arrigoni, E., Saper, C. B., & Fuller, P. M. (2017) · Nature Communications · doi:10.1038/s41467-017-01004-6 · Cited by 203 · see citing works
The claustrum in review
Mathur, B. N. (2014) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2014.00048 · Cited by 204 · see citing works
“903260408 Vertes, R. P., and Hoover, W. B. (2008). Projections of the paraventricular and”
Background
Evidence for Differential Control of Posterior Hypothalamic, Supramammillary, and Medial Mammillary Theta-Related Cellular Discharge by Ascending and Descending Pathways
Kirk, I. J., Oddie, S., Konopacki, J., & Bland, B. H. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-17-05547.1996 · Cited by 185 · see citing works
“in the frequency of SuM cell burst discharge), and that this frequency-coded information is then fed via the medial forebrain bundle (Veazy et al., 1982; Vertes, 1992) to the MS/vDBB.”
BackgroundMethodInfluential
Two types of corticopulvinar terminations: Round (type 2) and elongate (type 1)
Rockland, K. S. (1996) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19960422)368:1 · Cited by 129 · see citing works
Localization of glutamatergic/aspartatergic neurons projecting to the hypothalamic paraventricular nucleus studied by retrograde transport of [3H]d-aspartate autoradiography
Csáki, Á., Kocsis, K., Halász, B., & Kiss, J. (2000) · Neuroscience · doi:10.1016/s0306-4522(00)00411-5 · Cited by 179 · see citing works
An update on the connections of the ventral mesencephalic dopaminergic complex
Yetnikoff, L., Lavezzi, H. N., Reichard, R. A., & Zahm, D. S. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.04.010 · Cited by 172 · see citing works
“A somewhat similar situation may exist vis a vis a dense projection from the supramammillary nucleus to the lateral septum (Shepard et al, 1988; Vertes, 1992), of which about 40% of the neurons of origin are dopaminergic neurons (Swanson, 1982) residing in Hökfelt’s et al. (1984b) A10rv group.”
Background
Reconciling the different faces of hippocampal theta: The role of theta oscillations in cognitive, emotional and innate behaviors
Korotkova, T. M., Ponomarenko, A. A., Monaghan, C. K., Poulter, S. L., Cacucci, F., Wills, T. J., Hasselmo, M. E., & Lever, C. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.09.004 · Cited by 159 · see citing works
“The medial supramammillary nucleus (SuM) sends projections to the medial septum (Vertes, 1992), SuM cells exhibit theta-rhythmic activity and are phase-locked to hippocampal theta (Kirk and McNaughton N, 1991; Kocsis and Vertes 1997).”
Are periaqueductal gray and dorsal raphe the foundation of appetitive and aversive control? A comprehensive review
Silva, C., & McNaughton, N. (2019) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2019.02.001 · Cited by 156 · see citing works
“, 1991) and most of the supramammillary region (Vertes, 1992).”
Background
Principal cells are the postsynaptic targets of supramammillary afferents in the hippocampus of the rat
Maglóczky, Z., Acsády, L., & Freund, T. F. (1994) · Hippocampus · doi:10.1002/hipo.450040316 · Cited by 158 · see citing works
The supramammillary nucleus and the claustrum activate the cortex during REM sleep
Renouard, L., Billwiller, F., Ogawa, K., Clément, O., Camargo, N., Abdelkarim, M., Gay, N., Scoté-Blachon, C., Touré, R., Libourel, P.-A., et al. (2015) · Science Advances · doi:10.1126/sciadv.1400177 · Cited by 152 · see citing works
“In addition, in agreement with a previous study (20), a large number of anterogradely labeled fibers were observed in the dentate gyrus in close proximity to FOS neurons after CTb injection in the SUML in REM sleep hypersomniac rats (Fig.”
Result
Primary reinforcing effects of nicotine are triggered from multiple regions both inside and outside the ventral tegmental area
Ikemoto, S., Qin, M., & Liu, Z.-H. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.4542-05.2006 · Cited by 151 · see citing works
“The supramammillary nucleus does not project to the nucleus accumbens or olfactory tubercle, but to the septal and hippocampal complexes (Vertes, 1992), which have not been implicated clearly in primary reinforcement.”
Background
Anatomical Substrates of Hypothalamic Integration
Simerly, R. B. (2004) · Elsevier eBooks · doi:10.1016/b978-012547638-6/50015-8 · Cited by 148 · see citing works
Making memories of stressful events: a journey along epigenetic, gene transcription, and signaling pathways
Reul, J. M. H. M. (2014) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2014.00005 · Cited by 147 · see citing works
Theta-Modulated Head Direction Cells in the Rat Anterior Thalamus
Tsanov, M., Chah, E., Vann, S. D., Reilly, R. B., Erichsen, J. T., Aggleton, J. P., & O’Mara, S. M. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.0353-11.2011 · Cited by 145 · see citing works
“The supramammillary nucleus is a part of an ascending system involving the medial septum (Vertes, 1992; Borhegyi et al., 1998) and this system is proposed as the cholinergic pacemaker of theta in the hippocampodiencephalic circuit (Brazhnik and Vinogradova, 1986).”
Background
Anatomical, Electrophysiological and Pharmacological Studies of Ascending Brainstem Hippocampal Synchronizing Pathways
Bland, B. H. (1998) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(97)00013-4 · Cited by 145 · see citing works
Septal networks: relevance to theta rhythm, epilepsy and Alzheimer's disease
Colom, L. V. (2006) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2005.03630.x · Cited by 142 · see citing works
The medial supramammillary nucleus, spatial learning and the frequency of hippocampal theta activity
Pan, W. X., & McNaughton, N. (1997) · Brain Research · doi:10.1016/s0006-8993(97)00431-9 · Cited by 142 · see citing works
The Role of Theta-Range Oscillations in Synchronising and Integrating Activity in Distributed Mnemonic Networks
Kirk, I. J., & MACKAY, J. (2003) · Cortex · doi:10.1016/s0010-9452(08)70874-8 · Cited by 141 · see citing works
Hippocampal Formation Theta Activity and Movement Selection
Oddie, S. (1998) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(97)00003-1 · Cited by 140 · see citing works
Orexin receptor 2 expression in the posterior hypothalamus rescues sleepiness in narcoleptic mice
Mochizuki, T., Arrigoni, E., Marcus, J., Clark, E. L., Yamamoto, M., Honer, M., Borroni, E., Lowell, B. B., Elmquist, J. K., & Scammell, T. E. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1012456108 · Cited by 137 · see citing works
“The role of these cells in the control of wakefulness has not yet been tested directly, but they could promote arousal through their projections to the cortex and basal forebrain (24, 25).”
Background
Frequency Modulation of Hippocampal Theta by the Supramammillary Nucleus, and Other Hypothalamo–Hippocampal Interactions: Mechanisms and Functional Implications
Kirk, I. J. (1998) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(97)00015-8 · Cited by 130 · see citing works
Connection matrix of the hippocampal formation: I. The dentate gyrus
Patton, P. E., & McNaughton, B. L. (1995) · Hippocampus · doi:10.1002/hipo.450050402 · Cited by 129 · see citing works
“…studies, as well as by electro-physiology (retrograde: Harley et al., 1983; Pasquier and Reinoso-Suarez, 1978; Magl6czky et al., 1994 anterograde: Dent et al., 1983; Haglund et al., 1984; Segal, 1979; Wyss et al., 197%; Vertes, 1992; Magloczky et al., 1994 electrophysiology: Mizumori er al., 1389).”
Background
The Transition from Slow-wave Sleep to Paradoxical Sleep: Evolving Facts and Concepts of the Neurophysiological Processes Underlying the Intermediate Stage of Sleep
Gottesmann, C. (1996) · Neuroscience & Biobehavioral Reviews · doi:10.1016/0149-7634(95)00055-0 · Cited by 131 · see citing works
Gonadal Steroids, Learning, and Memory
Dohanich, G. P. (2002) · Elsevier eBooks · doi:10.1016/b978-012532104-4/50024-x · Cited by 130 · see citing works
Evidence of a Spatial Encoding Deficit in Rats with Lesions of the Mammillary Bodies or Mammillothalamic Tract
Vann, S. D., & Aggleton, J. P. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-08-03506.2003 · Cited by 129 · see citing works
“In this context it should also be noted that the supramammillary nuclei do not project through the MTT (Vertes, 1992).”
Background
Morphological properties of intracellularly labeled layer I neurons in rat neocortex
Zhou, F.-M., & Hablitz, J. J. (1996) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19961209)376:2 · Cited by 79 · see citing works
Discharge patterns of hippocampal theta-related cells in the caudal diencephalon of the urethan-anesthetized rat
Bland, B. H., Konopacki, J., Kirk, I. J., Oddie, S., & Dickson, C. T. (1995) · Journal of Neurophysiology · doi:10.1152/jn.1995.74.1.322 · Cited by 126 · see citing works
Neural circuits underlying the generation of theta oscillations
Pignatelli, M., Beyeler, A., & Leinekugel, X. (2011) · Journal of Physiology-Paris · doi:10.1016/j.jphysparis.2011.09.007 · Cited by 124 · see citing works
“, 1998) and to the hippocampus (Vertes, 1992), innervating the granule cell layer of the dentate gyrus and the pyramidal cell layer of the CA2-CA3 region (Maglóczky et al.”
Background
The midline posterior hypothalamic region comprises a critical part of the ascending brainstem hippocampal synchronizing pathway
Oddie, S., Bland, B. H., Colom, L. V., & Vertes, R. P. (1994) · Hippocampus · doi:10.1002/hipo.450040408 · Cited by 125 · see citing works
Localization of the neurons active during paradoxical (REM) sleep and projecting to the locus coeruleus noradrenergic neurons in the rat
Verret, L., Fort, P., Gervasoni, D., Léger, L., & Luppi, P. (2006) · The Journal of Comparative Neurology · doi:10.1002/cne.20891 · Cited by 125 · see citing works
“A number of studies showed that these two structures might act as relays in the ascending theta-synchronizing system (Robinson and Whishaw, 1974; Kirk and McNaughton, 1991; Vertes, 1992; Kirk, 1998).”
Background
Neurocircuitry of drug reward
Ikemoto, S., & Bonci, A. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.04.031 · Cited by 122 · see citing works
“The SuM robustly projects to the entire septo-hippocampus formation (Vertes, 1992).”
Background
Distinct patterns of neuronal inputs and outputs of the juxtaparaventricular and suprafornical regions of the lateral hypothalamic area in the male rat
Hahn, J. D., & Swanson, L. W. (2010) · Brain Research Reviews · doi:10.1016/j.brainresrev.2010.02.002 · Cited by 121 · see citing works
Glucagon‐like peptide‐1 in the rat brain: Distribution of expression and functional implication
Gu, G., Roland, B. L., Tomaselli, K. J., Dolman, C. S., Lowe, C., & Heilig, J. S. (2012) · The Journal of Comparative Neurology · doi:10.1002/cne.23282 · Cited by 119 · see citing works
“…reticular formation (Saper et al., 1976, 1979; Watts and Swanson, 1987; Watts et al., 1987; Simerly and Swanson, 1988; Ter Horst et al., 1989; Vertes, 1992; Moga and Moore, 1997; Groenewegen and Witter, 2004; Saper, 2004), the CEA, and the infralimbic cortex and the subiculum (Groenewegen,…”
Background
Ascending projections of the posterior nucleus of the hypothalamus: PHA‐L analysis in the rat
Vertes, R. P., Crane, A. M., Colom, L. V., & Bland, B. H. (1995) · The Journal of Comparative Neurology · doi:10.1002/cne.903590107 · Cited by 116 · see citing works
Hippocampal Formation
Cappaert, N. L. M., van Strien, N. M., & Witter, M. P. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-374245-2.00020-6 · Cited by 110 · see citing works
The role of the medial supramammillary nucleus in the control of hippocampal theta activity and behaviour in rats
Pan, W. X., & McNaughton, N. (2002) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2002.02267.x · Cited by 112 · see citing works
“…nucleus (mSUM) is a small nucleus that overlies the mammillary bodies medially. mSUM connects with the septo-hippocampal system (Vertes, 1988; Vertes, 1992) and is involved in the control of the frequency of hippocampal theta rhythm (Kirk & McNaughton, 1991; Kirk & McNaughton, 1993; Kocsis &…”
Background
Immunohistochemical mapping of neuropeptides in the premamillary region of the hypothalamus in rats
Lantos, T., Görcs, T. J., & Palkovits, M. (1995) · Brain Research Reviews · doi:10.1016/0165-0173(94)00013-f · Cited by 111 · see citing works
Supramammillary Nucleus Modulates Spike-Time Coordination in the Prefrontal-Thalamo-Hippocampal Circuit during Navigation
Ito, H., Moser, E. I., & Moser, M. (2018) · Neuron · doi:10.1016/j.neuron.2018.07.021 · Cited by 106 · see citing works
“We hypothesized that SUM in the hypothalamus might be such a structure, because SUM has projections to mPFC, NR, and hippocampal areas CA2 and dentate gyrus, which can influence CA1 (Amaral and Cowan, 1980; Haglund et al., 1984; Vertes, 1992; Vertes et al., 1995; McKenna and Vertes, 2004).”
Influential
Complimentary roles for hippocampal versus subicular/entorhinal place cells in coding place, context, and events
Sharp, P. E. (1999) · Hippocampus · doi:10.1002/(sici)1098-1063(1999)9:4 · Cited by 125 · see citing works
Intraseptal procaine abolishes hypothalamic stimulation-induced wheel- running and hippocampal theta field activity in rats
Oddie, S., Stefanek, W., Kirk, I. J., & Bland, B. H. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-05-01948.1996 · Cited by 106 · see citing works
“Fibers from the PO reach the MS via nuclei in the caudal diencephalon, namely the supramamillary nucleus and the posterior hypothalamic nucleus (Vertes, 1982, 1984, 1988); both nuclei project to the MS (Vertes, 1992; Vertes et al., 1995).”
Background
The supramammillo-hippocampal and supramammillo-septal glutamatergic/aspartatergic projections in the rat: a combined [3H]d-aspartate autoradiographic and immunohistochemical study
Kiss, J., Csáki, Á., Bokor, H., Shanabrough, M., & Léránth, C. (2000) · Neuroscience · doi:10.1016/s0306-4522(00)00127-5 · Cited by 104 · see citing works
A Novel Entorhinal Projection to the Rat Dentate Gyrus: Direct Innervation of Proximal Dendrites and Cell Bodies of Granule Cells and GABAergic Neurons
Deller, T., Martı́nez, A., Nitsch, R., & Frotscher, M. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-10-03322.1996 · Cited by 104 · see citing works
“…axons (Nyakas et al., 1987; Gaykema et al., 1990) enter the hippocampus and fascia dentata via the fimbria and hilus, fibers of hypothalamic origin (Vertes, 1992) terminate directly above the granule cell layer, and the overwhelming majority of noradrenergic and serotonergic fibers terminates…”
Background
Organization of ventral tegmental area projections to the ventral tegmental area–nigral complex in the rat
Ferreira, J. G. P., Del-Fava, F., Hasue, R. H., & Shammah‐Lagnado, S. J. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.02.003 · Cited by 101 · see citing works
A Population of Supramammillary Area Calretinin Neurons Terminating on Medial Septal Area Cholinergic and Lateral Septal Area Calbindin-Containing Cells Are Aspartate/Glutamatergic
Léránth, C., & Kiss, J. Z. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-23-07699.1996 · Cited by 100 · see citing works
“Recent studies, however, demonstrated that the LS‐medial septum pathway is nonexistent or extremely sparse ( Staiger and Nurnberger, 1991; Leranth et al., 1992; Witter et al., 1992).”
Background
Direct catecholaminergic-cholinergic interactions in the basal forebrain. II. Substantia nigra-ventral tegmental area projections to cholinergic neurons
Gaykema, R. P. A., & Záborszky, L. (1996) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19961028)374:4 · Cited by 103 · see citing works
Possible glutamatergic/aspartatergic projections to the supramammillary nucleus and their origins in the rat studied by selective [3H]D-aspartate labelling and immunocytochemistry
Kiss, J., Csáki, Á., Bokor, H., Kocsis, K., & Kocsis, B. (2002) · Neuroscience · doi:10.1016/s0306-4522(02)00037-4 · Cited by 95 · see citing works
Three‐dimensional reconstruction of the antennal lobe in Drosophila melanogaster
Laissue, P. P., Reiter, C., Hiesinger, P. R., Halter, S., Fischbach, K. F., & Stocker, R. F. (1999) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19990322)405:4 · Cited by 421 · see citing works
Supramammillary Nucleus Afferents to the Dentate Gyrus Co-release Glutamate and GABA and Potentiate Granule Cell Output
Hashimotodani, Y., Karube, F., Yanagawa, Y., Fujiyama, F., & Kano, M. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.11.016 · Cited by 92 · see citing works
Intracellular recordings from medial septal neurons during hippocampal theta rhythm
Brazhnik, E. S., & Fox, S. E. (1997) · Experimental Brain Research · doi:10.1007/pl00005653 · Cited by 94 · see citing works
“Afferents from the supramammillary nucleus may contribute to the pacing of the rhythmicity ( Vertes 1992; Kocsis and Vertes 1994).”
Background
Heterogeneity of the supramammillary–hippocampal pathways: evidence for a unique GABAergic neurotransmitter phenotype and regional differences
Soussi, R., Zhang, N., Tahtakran, S., Houser, C. R., & Esclapez, M. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07329.x · Cited by 90 · see citing works
“that predominantly innervate the dentate gyrus throughout the dorsal and ventral hippocampus and the CA2 ⁄ CA3a region of the dorsal hippocampus (Wyss et al., 1979; Haglund et al., 1984; Saper, 1985; Vertes, 1992;Maglóczky et al., 1994).”
BackgroundInfluential
Connections of the lateral hypothalamic area juxtadorsomedial region in the male rat
Hahn, J. D., & Swanson, L. W. (2012) · The Journal of Comparative Neurology · doi:10.1002/cne.23064 · Cited by 87 · see citing works
“…to the dentate gyrus from the SUMl, in contrast to an exclusively glutamatergic (and differently organized) projection to the dentate gyrus from the SUMm (Soussi et al., 2010)—more widespread topographic differences between the connections of the SUMm and SUMl are also apparent (Vertes, 1992).”
Background
SPECT tracer [123I]IBZM has similar affinity to dopamine D2 and D3 receptors
Videb�k, C., Toska, K., Scheideler, M. A., Paulson, O. B., & Knudsen, G. M. (2000) · Synapse · doi:10.1002/1098-2396(20001201)38:3 · Cited by 38 · see citing works
The supramammillo–septal–hippocampal pathway mediates sensorimotor gating impairment and hyperlocomotion induced by MK-801 and ketamine in rats
Ma, J., & Leung, L.-W. S. (2007) · Psychopharmacology · doi:10.1007/s00213-006-0667-x · Cited by 90 · see citing works
“The SUM is connected to the MS (Vertes 1992), and the SUM and the MS, respectively, control the frequency and the amplitude of the hippocampal theta rhythm (Bland et al.”
BackgroundMethodInfluential
MEMORY AND THE REGION OF THE MAMMILLARY BODIES
Sziklas, V. (1998) · Progress in Neurobiology · doi:10.1016/s0301-0082(97)00064-6 · Cited by 88 · see citing works
Supramammillary regulation of locomotion and hippocampal activity
Farrell, J. S., Lovett-Barron, M., Klein, P., Sparks, F. T., Gschwind, T., Ortiz, A. L., Ahanonu, B., Bradbury, S., Terada, S., Oijala, M., et al. (2021) · Science · doi:10.1126/science.abh4272 · Cited by 87 · see citing works
Dynamic changes in the direction of the theta rhythmic drive between supramammillary nucleus and the septohippocampal system
Kocsis, B., & Kamiński, M. (2006) · Hippocampus · doi:10.1002/hipo.20180 · Cited by 86 · see citing works
“…Borhegyi et al., 2004; Lee et al., 2005), posterior hypothalamus (PH) (Kirk and McNaughton, 1991; Kocsis and Vertes, 1994; Bland et al., 1995; Kocsis and Vertes, 1997), and brainstem (Kocsis and Vertes, 1992; Bassant and Poindessous-Jazat, 2001; Kocsis et al., 2001; Viana Di Prisco et al., 2002).”
Background
Extrinsic modulation of medial septal cell discharges by the ascending brainstem hippocampal synchronizing pathway
Bland, B. H., Oddie, S., Colom, L. V., & Vertes, R. P. (1994) · Hippocampus · doi:10.1002/hipo.450040604 · Cited by 85 · see citing works
The entorhino-septo-supramammillary nucleus connection in the rat: morphological basis of a feedback mechanism regulating hippocampal theta rhythm
Léránth, C., Carpi, D., Buzsáki, G., & Kiss, J. (1999) · Neuroscience · doi:10.1016/s0306-4522(98)00245-0 · Cited by 85 · see citing works
High level of adenosine A1 receptor-like immunoreactivity in the CA2/CA3a region of the adult rat hippocampus
Ochiishi, T., Saitoh, Y., Yukawa, A., Saji, M., Ren, Y., Shirao, T., Miyamoto, H., Nakata, H., & Sekino, Y. (1999) · Neuroscience · doi:10.1016/s0306-4522(99)00179-7 · Cited by 83 · see citing works
Major diencephalic inputs to the hippocampus
Vertes, R. P. (2015) · Progress in brain research · doi:10.1016/bs.pbr.2015.03.008 · Cited by 83 · see citing works
“…and thus abolishing LTP. 4 SUM: ROLE IN THE THETA RHYTHM In addition to direct inputs to the hippocampus, SUM distributes to several forebrain structures with connections to the hippocampus, that is, to the RE, the endopiriform nucleus, the medial and lateral septum, and the EC (Vertes, 1992).”
BackgroundResultInfluential
Structural and functional organization of the midline and intralaminar nuclei of the thalamus
Vertes, R. P., Linley, S. B., & Rojas, A. K. P. (2022) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.964644 · Cited by 82 · see citing works
“They include the tuberomammillary, supramammillary, dorsomedial, posterior, lateral and parasubthalamic nuclei (Vertes, 1992; Vertes et al., 1995; Goto and Swanson, 2004; Kirouac et al., 2005, 2006; Li and Kirouac, 2012).”
Background
Distribution of calretinin-containing neurons relative to other neurochemically-identified cell types in the medial septum of the rat
Kiss, J., Maglóczky, Z., Somogyi, J., & Freund, T. F. (1997) · Neuroscience · doi:10.1016/s0306-4522(96)00508-8 · Cited by 80 · see citing works
Afferent and efferent connections of the interpeduncular nucleus with special reference to circuits involving the habenula and raphe nuclei
Lima, L. B., Bueno, D., Leite, F., Souza, S., Gonçalves, L., Furigo, I. C., Donato, J., & Metzger, M. (2017) · The Journal of Comparative Neurology · doi:10.1002/cne.24217 · Cited by 80 · see citing works
“…bidirectional character of IP connections with structures such as NI, MnR, SuM, and septum, as well the rich reciprocal interconnections between the latter (e.g., Goto et al., 2001; Vertes, 1988, 1992; Vertes et al., 1999), support a hypothesis recently outlined by S anchez-P erez et al. (2015).”
Background
REM sleep-active hypothalamic neurons may contribute to hippocampal social-memory consolidation
Qin, H., Fu, L., Jian, T., Jin, W., Liang, M., Li, J., Chen, Q., Yang, X., Du, H., Liao, X., et al. (2022) · Neuron · doi:10.1016/j.neuron.2022.09.004 · Cited by 78 · see citing works
Selective immunolesions of hippocampal cholinergic input fail to impair spatial working memory
McMahan, R. W., Sobel, T. J., & Baxter, M. G. (1997) · Hippocampus · doi:10.1002/(sici)1098-1063(1997)7:2 · Cited by 109 · see citing works
Local circuit allowing hypothalamic control of hippocampal area CA2 activity and consequences for CA1
Robert, V., Therreau, L., Chevaleyre, V., Lepicard, E., Viollet, C., Cognet, J., Huang, A. J. Y., Boehringer, R., Polygalov, D., McHugh, T. J., et al. (2021) · eLife · doi:10.7554/elife.63352 · Cited by 74 · see citing works
“The hypothalamic supramammillary (SuM) nucleus sends projections to both area CA2 and 49 the dentate gyrus (Haglund et al., 1984; Vertes, 1992).”
Background
Classification of theta‐related cells in the entorhinal cortex: Cell discharges are controlled by the ascending brainstem synchronizing pathway in parallel with hippocampal theta‐related cells
Dickson, C. T., Kirk, I. J., Oddie, S., & Bland, B. H. (1995) · Hippocampus · doi:10.1002/hipo.450050404 · Cited by 74 · see citing works
Ventral pallidostriatal pathway in the monkey: Evidence for modulation of basal ganglia circuits
Spooren, W. P. J. M., Lynd‐Balta, E., Mitchell, S., & Haber, S. N. (1996) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19960701)370:3 · Cited by 76 · see citing works
Similar effects of medial supramammillary or systemic injection of chlordiazepoxide on both theta frequency and fixed-interval responding
Woodnorth, M., & McNaughton, N. (2002) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/cabn.2.1.76 · Cited by 67 · see citing works
“A transduction role for the mSuM of brainstem impulses bound for the medial septum is consistent with tracing studies that have identified projections to the mSuM from the RPO (Vertes & Martin, 1988) and other brainstem structures (Hayakawa, Ito, & Zyo, 1993) and from the mSuM to the medial septum via the median foreb…”
BackgroundMethod

The claustrum is a target for projections from the supramammillary nucleus in the rat
Barbier, M., & Risold, P. (2019) · Neuroscience · doi:10.1016/j.neuroscience.2019.03.045 · Cited by 30 · see citing works
The projection of the supramammillary nucleus to the hippocampal formation: An immunohistochemical and anterograde transport study with the lectin PHA‐L in the rat
Haglund, L., Swanson, L. W., & Köhler, C. (1984) · The Journal of Comparative Neurology · doi:10.1002/cne.902290204 · Cited by 264 · see citing works
Ascending projections of the posterior nucleus of the hypothalamus: PHA‐L analysis in the rat
Vertes, R. P., Crane, A. M., Colom, L. V., & Bland, B. H. (1995) · The Journal of Comparative Neurology · doi:10.1002/cne.903590107 · Cited by 116 · see citing works
SPECT tracer [123I]IBZM has similar affinity to dopamine D2 and D3 receptors
Videb�k, C., Toska, K., Scheideler, M. A., Paulson, O. B., & Knudsen, G. M. (2000) · Synapse · doi:10.1002/1098-2396(20001201)38:3 · Cited by 38 · see citing works
Distribution of hippocampal CA1 and subicular efferents in the prefrontal cortex of the rat studied by means of anterograde transport of Phaseolus vulgaris ‐leucoagglutinin
Jay, T. M., & Witter, M. P. (1991) · The Journal of Comparative Neurology · doi:10.1002/cne.903130404 · Cited by 841 · see citing works

Authors: Vertes, R. P.
Affiliations: Florida Atlantic University (US)
Corresponding author: Vertes, Robert P.
ORCID: Vertes, Robert P.
Venue: Journal of Comparative Neurology
Publisher: Wiley
Published: 1992-12-22
Volume: 326
Issue: 4
Pages: 595-622
ISSN: 0021-9967 (ISSN-L)
1096-9861
DOI: 10.1002/cne.903260408
OpenAlex: W2029127832
Cited by: 299
References: 92
Citations by year: 2026: 11 · 2025: 4 · 2024: 9 · 2023: 14 · 2022: 14 · 2021: 10 · 2020: 7 · 2019: 10 · 2018: 6 · 2017: 10 · 2016: 8 · 2015: 10 · 2014: 9 · 2013: 7 · 2012: 11
FWCI: 3.82
Type: journal article
Language: en
Open access: closed
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor, 4309 d)
Locations: The Journal of Comparative Neurology (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health (5r01mh045075-06)
National Institute of Mental Health (MH-45075)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Regulation of Appetite and Obesity
Keywords: supramammillary nucleus, anterograde tracing, Phaseolus vulgaris leucoagglutinin, hippocampal formation, dentate gyrus, medial forebrain bundle, thalamic nuclei, septum, entorhinal cortex, endopiriform nucleus, dorsal raphe nucleus, thalamus, preoptic area, bed nucleus of the stria terminalis, substantia innominata, diagonal band of Brodmann, claustrum, theta oscillations
MeSH terms: Animals, Cerebral Cortex, Hippocampus, Male, Mammillary Bodies, Mesencephalon, Neural Pathways, Phytohemagglutinins, Prosencephalon, Rats, Sprague-Dawley, Rats

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PHA-L analysis of projections from the supramammillary nucleus in the rat

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