The supramammillary area: its organization, functions and relationship to the hippocampus
Abstract
The supramammillary area of the hypothalamus, although small in size, can have profound modulatory effects on the hippocampal formation and related temporal cortex. It can control hippocampal plasticity and also has recently been shown to contain cells that determine the frequency of hippocampal rhythmical slow activity (theta rhythm). We review here its organization and anatomical connections providing an atlas and a new nomenclature. We then review its functions particularly in relation to its links with the hippocampus. Much of its control of behaviour and its differential activation by specific classes of stimuli is consistent with a tight relationship with the hippocampus. However, its ascending connections involve not only caudal areas of the cortex with close links to the hippocampus but also reciprocal connections with more rostral areas such as the infralimbic and anterior cingulate cortices. These latter areas appear to be the most rostral part of a network that, via the medial septum, hippocampus and lateral septum, is topographically mapped into the hypothalamus. The supramammillary area is thus diffusely connected with areas that control emotion and cognition and receives more topographically specific return information from areas that control cognition while also receiving ascending information from brain stem areas involved in emotion. We suggest that it is a key part of a network that recursively transforms information to achieve integration of cognitive and emotional aspects of goal-directed behaviour.
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CA2 pyramidal neurons integrate synaptic input from lateral entorhinal cortex, which conveys non-spatial information, with subcortical input from the serotonergic median raphe nucleus and the hypothalamic supramammillary nucleus.
“The finding that CA2 PNs integrate synaptic input from lateral EC (which conveys non-spatial information18) with subcortical input from both the serotonergic median raphe nucleus19 and the hypothalamic supramammillary nucleus20”
From The hippocampal CA2 region is essential for social memory (2014) · cites this paper as [20]
Cites
Gray, J. A. (1982) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00013066 · Cited by 4,477 · see citing works
A PROPOSED MECHANISM OF EMOTION
PAPEZ, J. W. (1937) · Archives of Neurology And Psychiatry · doi:10.1001/archneurpsyc.1937.02260220069003 · Cited by 3,563 · see citing works
Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning.
Phillips, R. G., & LeDoux, J. E. (1992) · Behavioral Neuroscience · doi:10.1037/0735-7044.106.2.274 · Cited by 3,292 · see citing works
Swanson, L. W. (1982) · Brain Research Bulletin · doi:10.1016/0361-9230(82)90145-9 · Cited by 1,718 · see citing works
The neuroanatomical and neurochemical basis of conditioned fear
Fendt, M., & Fanselow, M. S. (1999) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(99)00016-0 · Cited by 1,092 · see citing works
(1997) · Neuroscience · doi:10.1016/s0306-4522(97)00239-x · Cited by 707 · see citing works
Beck, C., & Fibiger, H. (1995) · The Journal of Neuroscience · doi:10.1523/jneurosci.15-01-00709.1995 · Cited by 547 · see citing works
Disinhibition of rat hippocampal pyramidal cells by GABAergic afferents from the septum.
Tóth, K., Freund, T. F., & Miles, R. (1997) · The Journal of Physiology · doi:10.1113/jphysiol.1997.sp022033 · Cited by 395 · see citing works
PHA-L analysis of projections from the supramammillary nucleus in the rat
Vertes, R. P. (1992) · Journal of Comparative Neurology · doi:10.1002/cne.903260408 · Cited by 299 · cited 9× · 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.…”
BackgroundInfluentialBorn, J., & Fehm, H. (2009) · Experimental and Clinical Endocrinology & Diabetes · doi:10.1055/s-0029-1211969 · Cited by 169 · cited 2× · see citing works
“, 1998; Rossi-Arnaud and Ammassari-Teule, 1992), and given the involvement of the hippocampus in the control of stress hormones (Bhatnagar et al., 1997; Born and Fehm, 1998; Brake et al., 1999; Ferrini et al., 1999; Herman et al., 1998; Uno et al., 1989).”
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Ikemoto, S. (2010) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.02.001 · Cited by 454 · see citing works
Hippocampal CA2 activity patterns change over time to a larger extent than between spatial contexts
Mankin, E. A., Diehl, G. W., Sparks, F. T., Leutgeb, S., & Leutgeb, J. K. (2015) · Neuron · doi:10.1016/j.neuron.2014.12.001 · Cited by 279 · 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
McNaughton, N., Kocsis, B., & Hajós, M. (2007) · Behavioural Pharmacology · doi:10.1097/fbp.0b013e3282ee82e3 · Cited by 187 · see citing works
Self-citationSmith, C. J. W., Poehlmann, M. L., Li, S., Ratnaseelan, A. M., Bredewold, R., & Veenema, A. H. (2017) · Brain Structure and Function · doi:10.1007/s00429-016-1260-7 · Cited by 143 · see citing works
Collins, A., Hill, L. E., Chandramohan, Y., Whitcomb, D., Droste, S. K., & Reul, J. M. H. M. (2009) · PLoS ONE · doi:10.1371/journal.pone.0004330 · Cited by 145 · see citing works
Boulland, J.-L., Jenstad, M., Boekel, A. J., Wouterlood, F. G., Edwards, R. H., Storm-Mathisen, J., & Chaudhry, F. A. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhn077 · Cited by 107 · see citing works
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
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Two major network domains in the dorsal raphe nucleus
Commons, K. G. (2015) · Journal of Comparative Neurology · doi:10.1002/cne.23748 · Cited by 46 · see citing works
Yang, J., Sadler, T. R., Givrad, T. K., Maarek, J.-M. I., & Holschneider, D. P. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2007.03.010 · Cited by 41 · see citing works
Hypothalamic Supramammillary Control of Cognition and Motivation
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Orzeł-Gryglewska, J., Matulewicz, P., & Jurkowlaniec, E. (2015) · Synapse · doi:10.1002/syn.21843 · Cited by 31 · see citing works
- Authors
- Pan, W.-X., & McNaughton, N.
- Affiliations
- University of Otago (NZ)
- Corresponding author
- McNaughton, Neil
- ORCID
- McNaughton, Neil
- Venue
- Progress in Neurobiology
- Publisher
- Elsevier BV
- Published
- 2004-10
- Volume
- 74
- Issue
- 3
- Pages
- 127-166
- ISSN
- 0301-0082 (ISSN-L)
- OpenAlex
- W1964678635
- Cited by
- 223
- References
- 10
- Citations by year
- 2026: 12 · 2025: 13 · 2024: 31 · 2023: 13 · 2022: 14 · 2021: 10 · 2020: 12 · 2019: 9 · 2018: 9 · 2017: 9 · 2016: 12 · 2015: 8 · 2014: 3 · 2013: 9 · 2012: 10
- FWCI
- 0.40
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Progress in Neurobiology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- hypothalamus, hippocampus, hippocampal plasticity, theta oscillations, structural connectivity, infralimbic cortex, anterior cingulate cortex, medial septum, lateral septum, emotions, cognition, goal-directed behavior, nomenclature
- MeSH terms
- Animals, Behavior, Animal, Brain Mapping, Cognition, Emotions, Hippocampus, Humans, Mammillary Bodies, Models, Neurological, Neural Pathways, Neurobiology
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