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

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

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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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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 118
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 120
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
“…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 107
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 112
“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
Active Spatial Information Processing in the Septo-Hippocampal System
Ono, T., & Nishijo, H. (1999) · Hippocampus · doi:10.1002/(sici)1098-1063(1999)9:4 · Cited by 17
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
“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 102
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
“…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 110
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 97
“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
Cell cycle kinetics in the embryonic mouse corpus striatum
Bhide, P. G. (1996) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19961028)374:4 · Cited by 73
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 91
Ultrastructural localization of dynorphin in the dentate gyrus in human temporal lobe epilepsy: A study of reorganized mossy fiber synapses
Zhang, N., & Houser, C. R. (1999) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19990322)405:4 · Cited by 100
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
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
“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
“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
“…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
Collateral projections from the supramammillary nucleus to the medial septum and hippocampus
Vertes, R. P., & McKenna, J. T. (2000) · Synapse · doi:10.1002/1098-2396(20001201)38:3 · Cited by 92
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 94
“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
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 85
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
“…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
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
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
Major diencephalic inputs to the hippocampus
Vertes, R. P. (2015) · Progress in brain research · doi:10.1016/bs.pbr.2015.03.008 · Cited by 88
“…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 90
“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
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 87
“…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
Prenatal exposure to moderate levels of ethanol can have long-lasting effects on hippocampal synaptic plasticity in adult offspring
Sutherland, R. J., McDonald, R. J., & Savage, D. D. (1997) · Hippocampus · doi:10.1002/(sici)1098-1063(1997)7:2 · Cited by 178
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 76
“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
Metabolic and neurochemical plasticity of ?-aminobutyric acid-immunoreactive neurons in the adult macaque striate cortex following monocular impulse blockade: Quantitative electron microscopic analysis
Nie, F., & Wong‐Riley, M. T. T. (1996) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19960701)370:3 · Cited by 30
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
“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

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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