Supramammillary Nucleus Afferents to the Dentate Gyrus Co-release Glutamate and GABA and Potentiate Granule Cell Output
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The supramammillary nucleus (SuM) of the hypothalamus projects to the dentate gyrus (DG) and the CA2 region of the hippocampus. Although the SuM-to-hippocampus circuits have been implicated in spatial and emotional memory formation, little is known about precise neural connections between the SuM and hippocampus. Here, we report that axons of SuM neurons make monosynaptic connections to granule cells (GCs) and GABAergic interneurons, but not to hilar mossy cells, in the DG and co-release glutamate and γ-aminobutyric acid (GABA) at these synapses. Although inputs from the SuM can excite some interneurons, the inputs alone fail to generate spikes in GCs. However, despite the insufficient excitatory drive and GABAergic co-transmission, SuM inputs have net excitatory effects on GCs and can potentiate GC firing when temporally associated with perforant path inputs. Our results indicate that the SuM influences DG information processing by modulating GC outputs.
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Optogenetic activation of SuM terminals in dentate gyrus produces monosynaptic short-latency release of both GABA and glutamate onto granule cells and interneurons.
“Furthermore, optogenetic activation of SuM terminals in the DG produces monosynaptic, short-latency release of both GABA and glutamate onto postsynaptic granule cells and interneurons.29”
From Synaptic and circuit functions of multitransmitter neurons in the mammalian brain (2023) · cites this paper as [29]
Cites
Fiji: an open-source platform for biological-image analysis
Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., et al. (2012) · Nature Methods · doi:10.1038/nmeth.2019 · Cited by 66,890 · see citing works
Interneurons of the hippocampus
Freund, T. F., & Buzsáki, G. (1998) · Hippocampus · doi:10.1002/(sici)1098-1063(1996)6:4 · Cited by 3,423 · see citing works
The three-dimensional organization of the hippocampal formation: A review of anatomical data
Amaral, D. G., & Witter, M. P. (1989) · Neuroscience · doi:10.1016/0306-4522(89)90424-7 · Cited by 2,180 · see citing works
Neuronal Diversity and Temporal Dynamics: The Unity of Hippocampal Circuit Operations
Klausberger, T., & Somogyi, P. (2008) · Science · doi:10.1126/science.1149381 · Cited by 2,050 · see citing works
The Expression of Vesicular Glutamate Transporters Defines Two Classes of Excitatory Synapse
Fremeau, R. T., Troyer, M. D., Pahner, I., Nygaard, G. O., Tran, C. H., Reimer, R. J., Bellocchio, E. E., Fortin, D. L., Storm‐Mathisen, J., & Edwards, R. H. (2001) · Neuron · doi:10.1016/s0896-6273(01)00344-0 · Cited by 1,266 · see citing works
Synaptic plasticity, memory and the hippocampus: a neural network approach to causality
Neves, G., Cooke, S. F., & Bliss, T. (2007) · Nature reviews. Neuroscience · doi:10.1038/nrn2303 · Cited by 1,207 · see citing works
Spatial selectivity of unit activity in the hippocampal granular layer
Jung, M. W., & McNaughton, B. L. (1993) · Hippocampus · doi:10.1002/hipo.450030209 · Cited by 789 · 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
Place Cells, Grid Cells, and MemoryPreprint
Moser, M., Rowland, D. C., & Moser, E. I. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a021808 · Cited by 538 · see citing works
Subcortical afferents to the hippocampal formation in the monkey
Amaral, D. G., & Cowan, W. M. (1980) · Journal of Comparative Neurology · doi:10.1002/cne.901890402 · Cited by 390 · see citing works
GABA/glutamate co-release controls habenula output and is modified by antidepressant treatment
Shabel, S. J., Proulx, C. D., Piriz, J., & Malinow, R. (2014) · Science · doi:10.1126/science.1250469 · Cited by 369 · see citing works
Segal, M., & Landis, S. C. (1974) · Brain Research · doi:10.1016/0006-8993(74)90349-7 · Cited by 361 · see citing works
Single rodent mesohabenular axons release glutamate and GABA
Root, D. H., Mejias-Aponte, C. A., Zhang, S., Wang, H.-L., Hoffman, A. F., Lupica, C. R., & Morales, M. (2014) · Nature Neuroscience · doi:10.1038/nn.3823 · Cited by 349 · see citing works
Rapid Signaling at Inhibitory Synapses in a Dentate Gyrus Interneuron Network
Bartos, M., Vida, I., Frotscher, M., Geiger, J. R. P., & Jonas, P. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-08-02687.2001 · Cited by 325 · see citing works
Physiological Properties and Behavioral Correlates of Hippocampal Granule Cells and Mossy Cells
Senzai, Y., & Buzsáki, G. (2017) · Neuron · doi:10.1016/j.neuron.2016.12.011 · Cited by 322 · see citing works
Knierim, J. J., & Neunuebel, J. P. (2015) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2015.10.008 · Cited by 305 · 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 · see citing works
Spatial Representations of Granule Cells and Mossy Cells of the Dentate Gyrus
GoodSmith, D., Chen, X., Wang, C., Kim, S. H., Song, H., Burgalossi, A., Christian, K. M., & Knierim, J. J. (2017) · Neuron · doi:10.1016/j.neuron.2016.12.026 · Cited by 267 · see citing works
Haglund, L., Swanson, L. W., & Köhler, C. (1984) · The Journal of Comparative Neurology · doi:10.1002/cne.902290204 · Cited by 264 · see citing works
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
Induction of Fos immunoreactivity in the brain by exposure to the elevated plus-maze
Silveira, M. C. L., Sandner, G., & Graeff, F. G. (1993) · Behavioural Brain Research · doi:10.1016/0166-4328(93)90028-o · Cited by 231 · 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
Inhibitory synapses in the developing auditory system are glutamatergic
Gillespie, D. C., Kim, G., & Kandler, K. (2005) · Nature Neuroscience · doi:10.1038/nn1397 · Cited by 222 · 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
Dendritic Integration in Hippocampal Dentate Granule Cells
Krueppel, R., Remy, S., & Beck, H. (2011) · Neuron · doi:10.1016/j.neuron.2011.05.043 · Cited by 199 · see citing works
Hilar mossy cells of the dentate gyrus: a historical perspective
Scharfman, H. E., & Myers, C. E. (2013) · Frontiers in Neural Circuits · doi:10.3389/fncir.2012.00106 · Cited by 197 · see citing works
In Vivo Imaging of Dentate Gyrus Mossy Cells in Behaving Mice
Danielson, N., Turi, G. F., Ladow, M. A., Chavlis, S., Petrantonakis, P. C., Poirazi, P., & Losonczy, A. (2017) · Neuron · doi:10.1016/j.neuron.2016.12.019 · Cited by 185 · see citing works
Nitz, D. A., & McNaughton, B. L. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00614.2003 · Cited by 184 · see citing works
Shifted pallidal co-release of GABA and glutamate in habenula drives cocaine withdrawal and relapse
Meye, F. J., Soiza-Reilly, M., Smit, T., Diana, M. A., Schwarz, M. K., & Mameli, M. (2016) · Nature Neuroscience · doi:10.1038/nn.4334 · Cited by 173 · see citing works
Maglóczky, Z., Acsády, L., & Freund, T. F. (1994) · Hippocampus · doi:10.1002/hipo.450040316 · Cited by 158 · see citing works
Root, D. H., Zhang, S., Barker, D. J., Miranda-Barrientos, J., Liu, B., Wang, H.-L., & Morales, M. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.05.063 · Cited by 153 · 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
Mizumori, S. J. Y., McNaughton, B. L., & Barnes, C. A. (1989) · Journal of Neurophysiology · doi:10.1152/jn.1989.61.1.15 · Cited by 136 · see citing works
Wang, Y., Kakizaki, T., Sakagami, H., Saito, K., Ebihara, S., Kato, M., Hirabayashi, M., Saito, Y., Furuya, N., & Yanagawa, Y. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.09.010 · Cited by 132 · see citing works
Nonrandom Local Circuits in the Dentate Gyrus
Larimer, P., & Strowbridge, B. W. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.3612-08.2008 · Cited by 122 · see citing works
Extrinsic afferent systems to the dentate gyrus
Léránth, C., & Hajszán, T. (2007) · Progress in brain research · doi:10.1016/s0079-6123(07)63004-0 · Cited by 116 · 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
Ito, H., Moser, E. I., & Moser, M. (2018) · Neuron · doi:10.1016/j.neuron.2018.07.021 · Cited by 106 · see citing works
Chronic Loss of CA2 Transmission Leads to Hippocampal Hyperexcitability
Boehringer, R., Polygalov, D., Huang, A. J. Y., Middleton, S. J., Robert, V., Wintzer, M. E., Piskorowski, R. A., Chevaleyre, V., & McHugh, T. J. (2017) · Neuron · doi:10.1016/j.neuron.2017.04.014 · Cited by 105 · see citing works
Hashimotodani, Y., Nasrallah, K., Jensen, K. R., Chávez, A. E., Carrera, D., & Castillo, P. E. (2017) · Neuron · doi:10.1016/j.neuron.2017.07.028 · Cited by 104 · see citing works
Self-citationSoussi, 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
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
A potent inhibitory monosynaptic hypothalamo-hippocampal connection
Segal, M. (1979) · Brain Research · doi:10.1016/0006-8993(79)90762-5 · Cited by 82 · see citing works
Differential Recruitment of Dentate Gyrus Interneuron Types by Commissural Versus Perforant Pathways
Hsu, T., Lee, C.-T., Tai, M.-H., & Lien, C. (2015) · Cerebral Cortex · doi:10.1093/cercor/bhv127 · Cited by 78 · see citing works
Input-specific plasticity at excitatory synapses mediated by endocannabinoids in the dentate gyrus
Chiu, C. Q., & Castillo, P. E. (2007) · Neuropharmacology · doi:10.1016/j.neuropharm.2007.06.026 · Cited by 73 · see citing works
Tepper, J. M., Young, S. J., & Groves, P. M. (1984) · Brain Research · doi:10.1016/0006-8993(84)90597-3 · Cited by 66 · see citing works
Dent, J. A., Galvin, N. J., Stanfield, B. B., & Cowan, W. M. (1983) · Brain Research · doi:10.1016/0006-8993(83)91220-9 · Cited by 64 · see citing works
Shahidi, ., Motamedi, F., & Naghdi, N. (2004) · Brain Research · doi:10.1016/j.brainres.2004.08.030 · Cited by 60 · see citing works
Santín, L. J., Aguirre, J. A., Rubio, S., Begega, A., Miranda, R., & Arias, J. L. (2003) · Physiology & Behavior · doi:10.1016/s0031-9384(03)00060-x · Cited by 56 · see citing works
Halasy, K., Hajszán, T., Kovács, É. G., Lâm, T., & Léránth, C. (2004) · Hippocampus · doi:10.1002/hipo.20006 · Cited by 50 · see citing works
Scharfman, H. E. (1993) · Journal of Neurophysiology · doi:10.1152/jn.1993.70.2.742 · Cited by 49 · see citing works
Mixed neurotransmission in the hippocampal mossy fibers
Münster‐Wandowski, A., Gómez‐Lira, G., & Gutiérrez, R. (2013) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2013.00210 · Cited by 47 · see citing works
Carre, G. P., & Harley, C. W. (1991) · Brain Research · doi:10.1016/0006-8993(91)91415-w · Cited by 46 · see citing works
Roberts, V. J., Barth, S., Meunier, H., & Vale, W. (1996) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19960115)364:3 · Cited by 45 · see citing works
Wirtshafter, D., Stratford, T. R., & Shim, I. (1998) · Brain Research · doi:10.1016/s0006-8993(97)01555-2 · Cited by 45 · see citing works
An EM autoradiographic study of the hypothalamo-hippocampal projection
Stanfield, B. B., & Cowan, W. M. (1984) · Brain Research · doi:10.1016/0006-8993(84)90596-1 · Cited by 44 · see citing works
Nakanishi, K., Saito, H., & Abe, K. (2001) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2001.01446.x · Cited by 43 · see citing works
Local and Long-Range Circuit Connections to Hilar Mossy Cells in the Dentate Gyrus
Sun, Y., Grieco, S. F., Holmes, T. C., & Xu, X. (2017) · eNeuro · doi:10.1523/eneuro.0097-17.2017 · Cited by 40 · see citing works
Ito, M., Shirao, T., Doya, K., & Sekino, Y. (2009) · Neuroscience Research · doi:10.1016/j.neures.2009.04.013 · Cited by 38 · see citing works
Hernández-Pérez, J. J., Gutiérrez-Guzmán, B. E., López‐Vázquez, M. A., & Olvera‐Cortés, M. E. (2015) · Frontiers in Pharmacology · doi:10.3389/fphar.2015.00250 · Cited by 33 · see citing works
Aranda, L., Begega, A., Sánchez-López, J., Aguirre, J. A., Arias, J. L., & Santín, L. J. (2008) · Physiology & Behavior · doi:10.1016/j.physbeh.2008.01.024 · Cited by 31 · see citing works
Nakano, Y., Karube, F., Hirai, Y., Kobayashi, K., Hioki, H., Okamoto, S., Kameda, H., & Fujiyama, F. (2018) · Journal of Neuroscience Research · doi:10.1002/jnr.24214 · Cited by 14 · see citing works
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Molecularly defined and spatially resolved cell atlas of the whole mouse brain
Zhang, M., Pan, X., Jung, W., Halpern, A. R., Eichhorn, S. W., Lei, Z., Cohen, L., Smith, K. A., Tasic, B., Yao, Z., et al. (2023) · Nature · doi:10.1038/s41586-023-06808-9 · Cited by 506 · see citing works
A hypothalamic novelty signal modulates hippocampal memory
Chen, S., He, L., Huang, A. J. Y., Boehringer, R., Robert, V., Wintzer, M. E., Polygalov, D., Weitemier, A. Z., Tao, Y., Gu, M., et al. (2020) · Nature · doi:10.1038/s41586-020-2771-1 · Cited by 258 · see citing works
An Integrated Index: Engrams, Place Cells, and Hippocampal Memory
Goode, T. D., Tanaka, K. Z., Sahay, A., & McHugh, T. J. (2020) · Neuron · doi:10.1016/j.neuron.2020.07.011 · Cited by 158 · see citing works
Li, Y., Luo, Y., Chen, Z.-K., Quintanilla, L., Chérasse, Y., Zhang, L., Lazarus, M., Huang, Z., & Song, J. (2022) · Nature Neuroscience · doi:10.1038/s41593-022-01065-x · Cited by 153 · see citing works
Contributions of adult neurogenesis to dentate gyrus network activity and computations
Tuncdemir, S. N., Lacefield, C., & Hen, R. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.112112 · Cited by 97 · see citing works
HippoBellum: Acute Cerebellar Modulation Alters Hippocampal Dynamics and Function
Zeidler, Z., Hoffmann, K., & Krook-Magnuson, E. I. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.0763-20.2020 · Cited by 98 · see citing works
Diversity and function of corticopetal and corticofugal GABAergic projection neurons
Melzer, S., & Monyer, H. (2020) · Nature reviews. Neuroscience · doi:10.1038/s41583-020-0344-9 · Cited by 94 · see citing works
Li, Y., Luo, Y., Xie, L., Tart, D. S., Sheehy, R. N., Zhang, L., Coleman, L. G., Chen, X., & Song, J. (2023) · Cell stem cell · doi:10.1016/j.stem.2023.02.006 · Cited by 87 · see citing works
Li, Y., Bao, H., Luo, Y., Chérasse, Y., Sullivan, H. A., Quintanilla, L., Wickersham, I. R., Lazarus, M., Shih, Y. I., & Song, J. (2020) · eLife · doi:10.7554/elife.53129 · Cited by 83 · see citing works
Cellular taxonomy and spatial organization of the murine ventral posterior hypothalamus
Mickelsen, L. E., Flynn, W. F., Springer, K., Wilson, L., Beltrami, E. J., Bolisetty, M. T., Robson, P., & Jackson, A. C. (2020) · eLife · doi:10.7554/elife.58901 · Cited by 78 · see citing works
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
Synaptic and circuit functions of multitransmitter neurons in the mammalian brain
Wallace, M. L., & Sabatini, B. L. (2023) · Neuron · doi:10.1016/j.neuron.2023.06.003 · Cited by 59 · see citing works
Billwiller, F., Castillo, L., Elseedy, H., Ivanov, A., Scapula, J., Ghestem, A., Carponcy, J., Salin, P. A., Bras, H., Abdelmeguid, N. E., et al. (2020) · Brain Structure and Function · doi:10.1007/s00429-020-02146-y · Cited by 59 · see citing works
Stone, T. W. (2021) · Neuroscience · doi:10.1016/j.neuroscience.2021.06.007 · Cited by 45 · see citing works
Hypothalamic Supramammillary Control of Cognition and Motivation
Kesner, A. J., Mozaffarilegha, M., Thirtamara Rajamani, K., Arima, Y., Harony-Nicolas, H., Hashimotodani, Y., Ito, H. T., Song, J., & Ikemoto, S. (2023) · The Journal of Neuroscience · doi:10.1523/jneurosci.1320-23.2023 · Cited by 35 · see citing works
Kowalczyk, T., Staszelis, A., Kaźmierska-Grębowska, P., Tokarski, K., & Caban, B. (2021) · Neuroscience · doi:10.1016/j.neuroscience.2021.07.001 · Cited by 14 · see citing works
Long-Range GABAergic Projections of Cortical Origin in Brain Function
Urrutia-Piñones, J., Morales-Moraga, C., Sanguinetti, N. K., Escobar, A. P., & Chiu, C. Q. (2022) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2022.841869 · Cited by 33 · see citing works
Li, M., Kinney, J. L., Jiang, Y., Lee, D. K., Wu, Q., Lee, D., Xiong, W., & Sun, Q. (2023) · Journal of Neuroscience · doi:10.1523/jneurosci.1910-22.2023 · Cited by 34 · see citing works
Ajibola, M. I., Wu, J., Abdulmajeed, W. I., & Lien, C. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.0410-21.2021 · Cited by 31 · see citing works
The little brain and the seahorse: Cerebellar-hippocampal interactions
Froula, J. M., Hastings, S. D., & Krook-Magnuson, E. I. (2023) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2023.1158492 · Cited by 34 · see citing works
Dynamic interplay between GABAergic networks and developing neurons in the adult hippocampus
Trinchero, M. F., Giacomini, D., & Schinder, A. F. (2021) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2021.03.008 · Cited by 30 · see citing works
Li, J., Sun, X., You, Y., Li, Q., Wei, C., Zhao, L., Sun, M., Meng, H., Zhang, T., Yue, W., et al. (2022) · Science Advances · doi:10.1126/sciadv.abk1238 · Cited by 28 · see citing works
Intersectional mapping of multi-transmitter neurons and other cell types in the brain
Xu, J., Jo, A., DeVries, R. P., Deniz, S., Cherian, S., Sunmola, I., Song, X., Marshall, J. J., Gruner, K. A., Daigle, T. L., et al. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111036 · Cited by 27 · see citing works
Neural Progenitor Cells and the Hypothalamus
Makrygianni, E. A., & Chrousos, G. P. (2023) · Cells · doi:10.3390/cells12141822 · Cited by 26 · see citing works
Tabuchi, E., Sakaba, T., & Hashimotodani, Y. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2119636119 · Cited by 23 · see citing works
Amaral, D. G., Lavenex, P., & Insausti, R. (2025) · Oxford University Press eBooks · doi:10.1093/med/9780190065324.003.0003 · Cited by 19 · see citing works
Mircheva, Y., Peralta, M. R., & Tóth, K. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.2976-18.2019 · Cited by 15 · see citing works
Szlaga, A., Sambak, P., Trenk, A., Guguła, A., Singleton, C. E., Drwiȩga, G., Błasiak, T., Ma, S., Gundlach, A. L., & Błasiak, A. (2022) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2022.836116 · Cited by 14 · see citing works
Rovira-Esteban, L., Hájos, N., Nagy, G. A., Crespo, C., Nácher, J., Varea, E., & Blasco‐Ibáñez, J. M. (2020) · eNeuro · doi:10.1523/eneuro.0323-19.2020 · Cited by 16 · see citing works
Widespread co-release of glutamate and GABA throughout the mouse brain
Ceballos, C. C., Ma, L., Qin, M., & Zhong, H. (2024) · Communications Biology · doi:10.1038/s42003-024-07198-y · Cited by 19 · see citing works
Cattaneo, S., Ripamonti, M., Bedogni, F., Sessa, A., & Taverna, S. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/566984 · Cited by 14 · see citing works
Noncanonical circuits, states, and computations of the hippocampus
Farrell, J. S., & Soltész, I. (2025) · Science · doi:10.1126/science.adv4420 · Cited by 13 · see citing works
Luo, Y., Li, L., Chen, Z.-K., Dong, P., Xie, L., Farmer, W. T., Yu, Q.-S., Jiang, L.-X., Su, W.-K., Liu, H., et al. (2025) · Neuron · doi:10.1016/j.neuron.2025.09.006 · Cited by 14 · see citing works
Analytical approaches to examine gamma-aminobutyric acid and glutamate vesicular co-packaging
Kim, S., & Sabatini, B. L. (2023) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2022.1076616 · Cited by 10 · see citing works
Lipp, H., & Wolfer, D. P. (2022) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.958067 · Cited by 11 · see citing works
Hirai, H., Sakaba, T., & Hashimotodani, Y. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111871 · Cited by 11 · see citing works
Cover, K. K., Lieberman, A. G., Heckman, M. M., & Mathur, B. N. (2023) · eLife · doi:10.7554/elife.83627 · Cited by 11 · see citing works
cFOS as a biomarker of activity maturation in the hippocampal formation
Pompeiano, M., & Colonnese, M. T. (2023) · Frontiers in Neuroscience · doi:10.3389/fnins.2023.929461 · Cited by 13 · see citing works
Structural and Functional Properties of Hippocampal Neurons
Spruston, N., Piskorowski, R. A., Chevaleyre, V., Eyre, M. D., McBain, C. J., & Bartos, M. (2025) · Oxford University Press eBooks · doi:10.1093/med/9780190065324.003.0005 · Cited by 11 · see citing works
Hypothalamic regulation of hippocampal CA1 interneurons by the supramammillary nucleus
Jiang, Y., Lee, D. K., Guo, W., Li, M., & Sun, Q. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.114898 · Cited by 10 · see citing works
Kim, H. R., Dey, S., Sekerková, G., & Martina, M. (2024) · Journal of Neuroscience · doi:10.1523/jneurosci.0653-24.2024 · Cited by 9 · see citing works
Yamazaki, R., Wang, D., Laet, A. D., Maciel, R. M., Agnorelli, C., Cabrera, S., Arthaud, S., Libourel, P., Fort, P., Lee, H. S., et al. (2021) · SLEEP · doi:10.1093/sleep/zsab173 · Cited by 9 · see citing works
Loss of oxytocin receptors in hilar mossy cells impairs social discrimination
Hung, Y.-C., Wu, Y., Chien, M.-E., Lin, Y., Tsai, C., & Hsu, K. (2023) · Neurobiology of Disease · doi:10.1016/j.nbd.2023.106311 · Cited by 9 · see citing works
Escobedo, A., Holloway, S.-A., Votoupal, M., Cone, A. L., Skelton, H. E., Legaria, A. A., Ndiokho, I., Floyd, T., Kravitz, A. V., Bruchas, M. R., et al. (2023) · eLife · doi:10.7554/elife.90972 · Cited by 11 · see citing works
Billwiller, F., Castillo, L., Elseedy, H., Ivanov, A. I., Scapula, J., Ghestem, A., Carponcy, J., Salin, P. A., Bras, H., Abdelmeguid, N. E., et al. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/584862 · Cited by 9 · see citing works
Casaglia, E., & Luppi, P. (2022) · Journal of Sleep Research · doi:10.1111/jsr.13633 · Cited by 8 · see citing works
Takahashi, J., Yamada, D., Nagano, W., Sano, Y., Furuichi, T., & Saitoh, A. (2023) · PLoS ONE · doi:10.1371/journal.pone.0294113 · Cited by 8 · see citing works
Zhang, Y., Stoelzel, C. R., Ezrokhi, M., Tsai, T., & Cincotta, A. H. (2021) · Neuroscience · doi:10.1016/j.neuroscience.2021.05.005 · Cited by 6 · see citing works
Interactions of Cholecystokinin and Glutamatergic Systems in Feeding Behavior of Neonatal Chickens.
Jelokhani, M., Vazir, B., Zendehdel, M., & Jahandideh, A. (2022) · PubMed Central · doi:10.22092/ari.2022.357300.2015 · Cited by 6 · see citing works
The Role of the Dentate Gyrus in Mediating Hippocampal Functions: The Healthy Brain
Kitchigina, V. F., Shubina, L., & Popova, I. Y. (2023) · Neuroscience and Behavioral Physiology · doi:10.1007/s11055-023-01372-1 · Cited by 7 · see citing works
Kitchigina, V. F., & Shubina, L. (2023) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2023.110759 · Cited by 5 · see citing works
Hirai, H., Konno, K., Yamasaki, M., Watanabe, M., Sakaba, T., & Hashimotodani, Y. (2024) · eLife · doi:10.7554/elife.99711.3 · Cited by 15 · see citing works
Silkis, I. G., & Markevich, V. A. (2020) · Neurochemical Journal · doi:10.1134/s181971242004011x · Cited by 3 · see citing works
Traceable stimulus-dependent rapid molecular changes in dendritic spines in the brain
Kuboyama, K., Inoue, T., Hashimotodani, Y., Itoh, T., Suzuki, T., Tetsuzawa, A., Ohtsuka, Y., Kinoshita, R., Takara, R., Miyazawa, T., et al. (2020) · Scientific Reports · doi:10.1038/s41598-020-72248-4 · Cited by 3 · see citing works
Escobedo, A., Holloway, S.-A., Votoupal, M., Cone, A. L., Skelton, H. E., Legaria, A. A., Ndiokho, I., Floyd, T., Kravitz, A. V., Bruchas, M. R., et al. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.09.22.507167 · Cited by 3 · see citing works
Prevalent co-release of glutamate and GABA throughout the mouse brainPreprint
Ceballos, C. C., Ma, L., Qin, M., & Zhong, H. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.03.27.587069 · Cited by 3 · see citing works
Top-down regulation of subcortical regions by hippocampal long-range inhibition
Kinney, J. L., Robinson, H. L., Wang, H., Jiang, Y., Zhou, M., Lee, D. K., Li, M., Oliva, A., & Sun, Q. (2025) · Current Biology · doi:10.1016/j.cub.2025.10.062 · Cited by 4 · see citing works
Hippocampo–supramammillary coupling across sleep and wake
Caneo, M., Espinosa, N., Lazcano, G., Aguilera, A., Lara-Vásquez, A., & Fuentealba, P. (2026) · Scientific Reports · doi:10.1038/s41598-026-37066-0 · Cited by 2 · see citing works
Liu, Q., Luo, X., Liang, Z., Qin, D., Wang, M., & Guo, W. (2026) · Cell stem cell · doi:10.1016/j.stem.2026.02.008 · Cited by 2 · see citing works
Diencephalic modulation of the hippocampus in affective and cognitive behavior
Vertes, R. P., Linley, S. B., Rojas, A. K. P., Lamothe, K., & Allen, T. A. (2024) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2024.101377 · Cited by 2 · see citing works
Escobedo, A., Holloway, S.-A., Votoupal, M., Cone, A. L., Skelton, H. E., Legaria, A. A., Ndiokho, I., Floyd, T., Kravitz, A. V., Bruchas, M. R., et al. (2024) · eLife · doi:10.7554/elife.90972.3 · Cited by 1 · see citing works
Tian, T., Qin, X. Y., Li, B., Wang, Y. T., & Yang, X. (2025) · Translational Psychiatry · doi:10.1038/s41398-025-03564-4 · Cited by 1 · see citing works
Cissé, Y., Brace, C. S., Hsu, V., Yuede, C. M., Rensing, N. R., Wong, M., & Imai, S. (2026) · iScience · doi:10.1016/j.isci.2026.115741 · Cited by 1 · see citing works
A hypothalamic–hippocampal circuit-driven plasticity in fasciola cinereum mediates social memory
Qin, H., Wang, X., Jian, T., Li, Q., Liang, S., Tao, J., Wang, R., Chen, Q., Liu, B., Zhang, K., et al. (2026) · Vita · doi:10.15302/vita.2026.08.0071 · Cited by 1 · see citing works
Hippocampal Physiology in the Behaving Animal
Krupic, J., & O'Keefe, J. M. (2025) · Oxford University Press eBooks · doi:10.1093/med/9780190065324.003.0011 · Cited by 1 · see citing works
Colocalization of Neurotransmitters in Hippocampus and Afferent Systems: Possible Functional Role
Kitchigina, V. F. (2025) · Biochemistry (Moscow) · doi:10.1134/s0006297924603915 · Cited by 1 · see citing works
µ-Opioid Receptor Control of Glutamate/GABA Coreleasing SUM and VTA Projections to the Dentate Gyrus
Oleinichenko, D. (2025) · Journal of Neuroscience · doi:10.1523/jneurosci.0095-25.2025 · Cited by 1 · see citing works
Silkis, I. G. (2021) · Neuroscience and Behavioral Physiology · doi:10.1007/s11055-021-01169-0 · Cited by 1 · see citing works
Kitchigina, V. F., & Shubina, L. (2022) · Preprints.org · doi:10.20944/preprints202212.0046.v1 · Cited by 1 · see citing works
Escobedo, A., Holloway, S.-A., Votoupal, M., Cone, A. L., Skelton, H. E., Legaria, A. A., Ndiokho, I., Floyd, T., Kravitz, A. V., Bruchas, M. R., et al. (2023) · eLife · doi:10.7554/elife.90972.1
Escobedo, A., Holloway, S.-A., Votoupal, M., Cone, A. L., Skelton, H. E., Legaria, A. A., Ndiokho, I., Floyd, T., Kravitz, A. V., Bruchas, M. R., et al. (2024) · eLife · doi:10.7554/elife.90972.2
Hirai, H., Konno, K., Yamasaki, M., Watanabe, M., Sakaba, T., & Hashimotodani, Y. (2024) · eLife · doi:10.7554/elife.99711.1
Hirai, H., Konno, K., Yamasaki, M., Watanabe, M., Sakaba, T., & Hashimotodani, Y. (2024) · eLife · doi:10.7554/elife.99711.2 · Cited by 1 · see citing works
Lateral septum activation as a central hub for reversing chronic stress-induced novelty-avoidance
Chang, C., Sung, S., Chen, C.-S., Sung, K.-C., Wang, H., & Hsiao, Y. (2025) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2025.111436
Chatzi, C. A., Simmonds, A. N., Veshagh, A., Ellingson, A. J., Krush, M., McLean, T., Schnell, E., & Westbrook, G. L. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.02.22.707119
Rovira-Esteban, L., Vieco-Martí, I., Herraiz-Cabanes, J., Varea, E., Nácher, J., Crespo, C., & Blasco‐Ibáñez, J. M. (2026) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2026.1749335
Zhou, C., Cheng, S., Zheng, H., Zou, X., Bi, Y., & Wang, H. (2026) · Cell & Bioscience · doi:10.1186/s13578-026-01591-2
Wan, F., Wang, L., Wang, Q., Yang, J., & Liu, C. (2026) · CNS Neuroscience & Therapeutics · doi:10.1002/cns.70962
Neurotransmitter co-transmission: synaptic architectures, functional logic, and emerging tools
Tunc‐Ozcan, E. (2026) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2026.1862021
Barreira, L. M. C., Gapp, H., & Albrecht, A. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.07.30.741717
Glassburn, L., Havener, E., Stangler, O., de Velasco, E. M. F., & Krook-Magnuson, E. I. (2026) · The Journal of Physiology · doi:10.1113/jp291809
Circuit-specific remodeling of synaptic co-transmission in stress-responsive networks
Park, H., Kim, H., Sim, M., Ham, D., & Chung, C. (2026) · Animal Cells and Systems · doi:10.1080/19768354.2026.2730204
Aurfan, Z., Fransson, A., Davidsson, J., Risling, M., Günther, M., & Thams, S. (2026) · Neurobiology of Disease · doi:10.1016/j.nbd.2026.107612
- Authors
- Hashimotodani, Y., Karube, F., Yanagawa, Y., Fujiyama, F., & Kano, M.
- Affiliations
- Doshisha University (JP)
- Gunma University (JP)
- The University of Tokyo Institutes for Advanced Study (JP)
- Corresponding author
- Hashimotodani, Yuki
- Kano, Masanobu
- Venue
- Cell Reports
- Publisher
- Elsevier BV
- Published
- 2018-12
- Volume
- 25
- Issue
- 10
- Pages
- 2704-2715.e4
- ISSN
- 2211-1247 (ISSN-L)
- OpenAlex
- W2902420892
- Cited by
- 92
- References
- 63
- Citations by year
- 2026: 13 · 2025: 10 · 2024: 15 · 2023: 16 · 2022: 13 · 2021: 8 · 2020: 10 · 2019: 7
- FWCI
- 3.72
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Cell Reports (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Institutional Repositories DataBase (IRDB) (submittedVersion, cc-by)
- Funders
- Japan Society for the Promotion of Science (JSPS)
- Brain Mapping by Integrated Neurotechnologies for Disease Studies (Brain/MINDS)
- Strategic Research Program for Brain Sciences (SRPBS)
- Japan Agency for Medical Research and Development (AMED)
- Brain Science Foundation
- Tokyo Society of Medical Sciences
- 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
- supramammillary nucleus, dentate gyrus, granule cells, GABAergic interneurons, monosynaptic connections, perforant path, hippocampus, hypothalamus, mossy cells, synaptic potentiation
- MeSH terms
- Action Potentials, Afferent Pathways, Animals, gamma-Aminobutyric Acid, Hypothalamus, Posterior, Interneurons, Mice, Inbred C57BL, Synapses, Glutamic Acid, Dentate Gyrus, Perforant Pathway, Mossy Fibers, Hippocampal, Optogenetics
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