Synaptic innervation to rat hippocampus by vasopressin-immuno-positive fibres from the hypothalamic supraoptic and paraventricular nuclei
Abstract
The neuropeptide arginine vasopressin (AVP) exerts a modulatory role on hippocampal excitability through vasopressin V(1A) and V(1B) receptors. However, the origin and mode of termination of the AVP innervation of the hippocampus remain unknown. We have used light and electron microscopy to trace the origin, distribution and synaptic relationships of AVP-immuno-positive fibres and nerve terminals in the rat hippocampus. Immuno-positive fibres were present in all areas (CA1-3, dentate gyrus) of the whole septo-temporal extent of the hippocampus; they had the highest density in the CA2 region, strongly increasing in density towards the ventral hippocampus. Two types of fibres were identified, both establishing synaptic junctions. Type A had large varicosities packed with immuno-positive large-granulated peptidergic vesicles and few small clear vesicles forming type I synaptic junctions with pyramidal neuron dendrites, dendritic spines and with axonal spines. Type B had smaller varicosities containing mostly small clear vesicles and only a few large-granulated vesicles and established type II synaptic junctions mainly with interneuron dendrites. The AVP-positive axons in stratum oriens appeared to follow and contact metabotropic glutamate receptor 1α (mGluR1α)-immuno-positive interneuron dendrites. Fluoro-Gold injection into the hippocampus revealed retrogradely labelled AVP-positive somata in hypothalamic supraoptic and paraventricular nuclei. Hypothalamo-hippocampal AVP-positive axons entered the hippocampus mostly through a ventral route, also innervating the amygdala and to a lesser extent through the dorsal fimbria fornix, in continuation of the septal AVP innervation. Thus, it appears the AVP-containing neurons of the magnocellular hypothalamic nuclei serve as important sources for hippocampal AVP innervation, although the AVP-expressing neurons located in amygdala and bed nucleus of the stria terminalis reported previously may also contribute.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Oxytocin and vasopressin-expressing cells in the paraventricular and supraoptic nuclei send projections to the hippocampus, with the highest fiber density seen in the CA2 region for vasopressin and CA2/CA3 regions for oxytocin projections.
“OXT and AVPexpressing cells in PVN and SON send projections to the hippocampus, with the highest fiber density seen in the CA2 region for AVP and CA2/CA3 regions for OXT projections (97-100).”
From Oxytocin, Vasopressin, and Social Behavior: From Neural Circuits to Clinical Opportunities (2022) · cites this paper as [97]
Cites
The rat brain in stereotaxic coordinates
Palkovits, M. (1983) · Neuropeptides · doi:10.1016/0143-4179(83)90049-5 · Cited by 28,959 · see citing works
The Rat Brain in Stereotaxic Coordinates
Paxinos, G., & Watson, C. (1983) · Elsevier eBooks · doi:10.1016/c2009-0-63235-9 · Cited by 28,585 · see citing works
(1991) · Medical Entomology and Zoology · Cited by 1,512 · see citing works
(2006) · doi:10.1093/acprof:oso/9780195100273.001.0001 · Cited by 1,186 · see citing works
Croonian Lecture - The antidiuretic hormone and the factors which determine its release
Verney, E. B. (1947) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1947.0037 · Cited by 1,106 · see citing works
Landgraf, R., & Neumann, I. D. (2004) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2004.05.001 · Cited by 1,059 · see citing works
Intra- and extrahypothalamic vasopressin and oxytocin pathways in the rat
Buijs, R. M., Swaab, D. F., Dogterom, J., & van Leeuwen, F. W. (1978) · Cell and Tissue Research · doi:10.1007/bf00224932 · Cited by 1,029 · see citing works
Fluoro-gold: a new fluorescent retrograde axonal tracer with numerous unique properties
Schmued, L. C., & Fallon, J. H. (1986) · Brain Research · doi:10.1016/0006-8993(86)91199-6 · Cited by 887 · see citing works
Intra- and extrahypothalamic vasopressin and oxytocin pathways in the rat
Buijs, R. M. (1978) · Cell and Tissue Research · doi:10.1007/bf00212323 · Cited by 830 · see citing works
de Vries, G. J., & Buijs, R. M. (1983) · Brain Research · doi:10.1016/0006-8993(83)90855-7 · Cited by 524 · see citing works
The osmoregulation of vasopressin
Robertson, G. L., Shelton, R. L., & Athar, S. (1976) · Kidney International · doi:10.1038/ki.1976.76 · Cited by 524 · see citing works
Vasopressin: Behavioral roles of an “original” neuropeptide
Caldwell, H. K., Lee, H.-J., Macbeth, A. H., & Young, W. S. (2008) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2007.10.007 · Cited by 504 · see citing works
Hatton, G. I. (1990) · Progress in Neurobiology · doi:10.1016/0301-0082(90)90017-b · Cited by 439 · see citing works
Vasopressin and oxytocin receptors in the central nervous system
Tribollet, E., & Barberis, C. (1996) · Critical Reviews™ in Neurobiology · doi:10.1615/critrevneurobiol.v10.i1.60 · Cited by 399 · see citing works
Bielsky, I. F., Hu, S.-B., Ren, X., Terwilliger, E. F., & Young, L. J. (2005) · Neuron · doi:10.1016/j.neuron.2005.06.031 · Cited by 367 · see citing works
Birnbaumer, M. (2000) · Trends in Endocrinology and Metabolism · doi:10.1016/s1043-2760(00)00304-0 · Cited by 343 · see citing works
Extrapituitary expression of the rat V1b vasopressin receptor gene.
Lolait, S. J., O’Carroll, A., Mahan, L. C., Felder, C. C., Button, D. C., Young, W. S., Mezey, É., & Brownstein, M. J. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.15.6783 · Cited by 337 · see citing works
Mesocorticolimbic Glutamatergic Pathway
Yamaguchi, T., Wang, H.-L., Li, X., Ng, T. H., & Morales, M. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.1598-11.2011 · Cited by 332 · see citing works
STUDIES OF THE CONNEXIONS OF THE FORNIX SYSTEM
Daitz, H. M., & Powell, T. P. S. (1954) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.17.1.75 · Cited by 320 · see citing works
Structural bases of vasopressin/oxytocin receptor function
Barberis, C., Mouillac, B., & Durroux, T. (1998) · Journal of Endocrinology · doi:10.1677/joe.0.1560223 · Cited by 311 · see citing works
Caffé, A. R., van Leeuwen, F. W., & Luiten, P. G. M. (1987) · Journal of Comparative Neurology · doi:10.1002/cne.902610206 · Cited by 286 · see citing works
Hernando, F., Schoots, O., Lolait, S. J., & Burbach, J. P. H. (2001) · Endocrinology · doi:10.1210/endo.142.4.8067 · Cited by 275 · 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
Wigger, A., Sánchez, M. M., Mathys, K. C., Ebner, K., Frank, E., Liu, D., Kresse, A. E., Neumann, I. D., Holsboer, F., Plotsky, P. M., et al. (2003) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300290 · Cited by 263 · see citing works
Buijs, R. M., & Swaab, D. F. (1979) · Cell and Tissue Research · doi:10.1007/bf00233648 · Cited by 262 · see citing works
Distribution of vesicular glutamate transporter mRNA in rat hypothalamus
Ziegler, D. R., Cullinan, W. E., & Herman, J. P. (2002) · Journal of Comparative Neurology · doi:10.1002/cne.10257 · Cited by 241 · see citing works
Nonapeptides and the evolutionary patterning of sociality
GOODSON, J. (2008) · Progress in brain research · doi:10.1016/s0079-6123(08)00401-9 · Cited by 228 · see citing works
Frosch, M. P., Anthony, D. C., & Girolami, U. D. (2010) · Elsevier eBooks · doi:10.1016/b978-1-4377-0792-2.50033-x · Cited by 228 · see citing works
Young, W. S., Li, J., Wersinger, S. R., & Palkovits, M. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.08.040 · Cited by 222 · see citing works
Handbook of Brain Microcircuits
(2010) · Oxford University Press eBooks · doi:10.1093/med/9780195389883.001.0001 · Cited by 197 · see citing works
Morales, M., & Wang, S. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-15-06732.2002 · Cited by 175 · see citing works
Hou-Yu, A., Lamme, A., Zimmerman, E. A., & Silverman, A. (2008) · Neuroendocrinology · doi:10.1159/000124651 · Cited by 160 · see citing works
Maglóczky, Z., Acsády, L., & Freund, T. F. (1994) · Hippocampus · doi:10.1002/hipo.450040316 · Cited by 158 · see citing works
Landgraf, R., Neumann, I., & Schwarzberg, H. (1988) · Brain Research · doi:10.1016/0006-8993(88)90689-0 · Cited by 137 · see citing works
Vasopressin and oxytocin receptors
Zingg, H. H. (1996) · Baillière s Clinical Endocrinology and Metabolism · doi:10.1016/s0950-351x(96)80314-4 · Cited by 137 · see citing works
Vasopressin innervation of the mouse ( <i>Mus musculus</i> ) brain and spinal cord
Rood, B. D., & De Vries, G. J. (2011) · Journal of Comparative Neurology · doi:10.1002/cne.22635 · Cited by 134 · see citing works
Fluro-Gold: composition, and mechanism of uptake
Wessendorf, M. W. (1991) · Brain Research · doi:10.1016/0006-8993(91)90241-m · Cited by 127 · see citing works
Distribution of messenger RNA for the vasopressin V1a receptor in the CNS of male and female rats
Szot, P., Bale, T. L., & Dorsa, D. M. (1994) · Molecular Brain Research · doi:10.1016/0169-328x(94)90111-2 · Cited by 125 · see citing works
Raggenbass, M. (2001) · Progress in Neurobiology · doi:10.1016/s0301-0082(00)00064-2 · Cited by 120 · see citing works
Sofroniew, M. V. (1985) · Neuroscience · doi:10.1016/0306-4522(85)90217-9 · Cited by 113 · see citing works
Thibonnier, M., Berti‐Mattera, L. N., Dulin, N. O., Conarty, D. M., & Mattera, R. (1999) · Progress in brain research · doi:10.1016/s0079-6123(08)61568-x · Cited by 112 · see citing works
Stemmelin, J., Lukovic, L., Salome, N., & Griebel, G. (2005) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300562 · Cited by 112 · see citing works
Kosaka, T. (1980) · Journal of Neurocytology · doi:10.1007/bf01205024 · Cited by 111 · see citing works
Takács, V. T., Klausberger, T., Somogyi, P., Freund, T. F., & Gulyás, A. I. (2011) · Hippocampus · doi:10.1002/hipo.20974 · Cited by 99 · see citing works
A quantitative study of the fornixmamillo-thalamic system.
Powell, T. P. S., Guillery, R. W., & Cowan, W. M. (1957) · PubMed · Cited by 83 · see citing works
Buijs, R. M., Pool, C. W., van Heerikhuize, J. J., Sluiter, A. A., van der Sluis, P. J., Ramkema, M., van der Woude, T. P., & van der Beek, E. M. (1989) · Data Archiving and Networked Services (DANS) · Cited by 82 · see citing works
Iontophoretic injection of fluoro-gold and other fluorescent tracers.
Schmued, L. C., & Heimer, L. (1990) · Journal of Histochemistry & Cytochemistry · doi:10.1177/38.5.2332627 · Cited by 80 · see citing works
Castel, M., Feinstein, N., Cohen, S., & Harari, N. (1990) · The Journal of Comparative Neurology · doi:10.1002/cne.902980204 · Cited by 68 · see citing works
HAGINOYA, M., & Matsumoto, S. (1991) · Journal of the Japan Society of Colour Material · doi:10.4011/shikizai1937.64.34 · Cited by 63 · see citing works
Hypothalamic vasopressin system regulation by maternal separation: Its impact on anxiety in rats
Zhang, L., Hernández, V. S., Liu, B., Medina‐Pizarro, M., Nava-Kopp, A. T., Irles, C., & Morales, M. A. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.03.046 · Cited by 60 · see citing works
Schmued, L. C., Kyriakidis, K., Fallon, J. H., & Ribak, C. E. (1989) · Journal of Neurocytology · doi:10.1007/bf01190836 · Cited by 58 · see citing works
Ambalavanar, R., & Morris, R. (1989) · Brain Research · doi:10.1016/0006-8993(89)90133-9 · Cited by 55 · see citing works
Vasopressin induction of long‐lasting potentiation of synaptic transmission in the dentate gyrus
Chen, C., Brinton, R. D., Shors, T. J., & Thompson, R. F. (1993) · Hippocampus · doi:10.1002/hipo.450030211 · Cited by 54 · see citing works
Hippocampus: Intrinsic Organization
Somogyi, P. (2010) · Oxford University Press eBooks · doi:10.1093/med/9780195389883.003.0015 · Cited by 52 · see citing works
Glutamatergic innervation of the hypothalamic median eminence and posterior pituitary of the rat
Hrabovszky, E., Deli, L., Turi, G. F., Kalló, I., & Liposits, Z. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.10.053 · Cited by 39 · see citing works
Molecular Aspects of Vasopressin Receptor Function
Schöneberg, T., Kostenis, E., Liu, J., Gudermann, T. W., & Wess, J. (1998) · Advances in experimental medicine and biology · doi:10.1007/978-1-4615-4871-3_44 · Cited by 37 · see citing works
Identification of vasopressin in the subfornical organ region: effects of dehydration
Summy‐Long, J. Y., KEIL, L. C., & Severs, W. B. (1978) · Brain Research · doi:10.1016/0006-8993(78)90458-4 · Cited by 33 · see citing works
Urban, I. J. A. (1999) · Progress in brain research · doi:10.1016/s0079-6123(08)61576-9 · Cited by 31 · see citing works
Advances in Vasopressin and Oxytocin — From Genes to Behaviour to Disease
(2008) · Progress in brain research · doi:10.1016/s0079-6123(08)00453-6 · Cited by 28 · see citing works
Effects of arginine-vasopressin (AVP) on long-term potentiation in intact anesthetized rats
Dubrovsky, B. O., Tatarinov, A. L., Gijsbers, K., Harris, J., & Tsiodras, A. (2003) · Brain Research Bulletin · doi:10.1016/s0361-9230(02)00961-9 · Cited by 25 · see citing works
Hippocampus: Intrinsic Organization
Somogyi, P., & Klausberger, T. (2017) · Oxford University Press eBooks · doi:10.1093/med/9780190636111.003.0017 · Cited by 22 · see citing works
Gene Regulation System of Vasopressin and Corticotoropin-Releasing Hormone
Yoshida, M. (2008) · Gene Regulation and Systems Biology · doi:10.4137/grsb.s424 · Cited by 20 · see citing works
Persson, S., & Havton, L. A. (2009) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2009.07.017 · Cited by 19 · see citing works
Zhang, L., Medina‐Pizarro, M., Hernández, V. S., Estrada, F. S., & Vega‐González, A. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.03.059 · Cited by 19 · see citing works
Secretory cells of the supraoptic nucleus have central as well as neurohypophysial projections
Inyushkin, A. N., Orlans, H. O., & Dyball, R. E. J. (2009) · Journal of Anatomy · doi:10.1111/j.1469-7580.2009.01121.x · Cited by 16 · see citing works
Lee, C. L., McFarland, D. J., & Wolpaw, J. R. (1988) · Neuroscience Letters · doi:10.1016/0304-3940(88)90559-9 · Cited by 15 · see citing works
Hernández, V. S., Ruiz‐Velasco, S., & Zhang, L. (2012) · Neuroscience Letters · doi:10.1016/j.neulet.2012.09.002 · Cited by 14 · see citing works
Chepkova, A. N., Kapai, N. A., & Skrebitskii, V. G. (2001) · Bulletin of Experimental Biology and Medicine · doi:10.1023/a:1017583626625 · Cited by 13 · see citing works
Neuroendocrine Regulation of Learning and Memory
Greidanus, T. B. V. W., Croiset, G., & de Wied, D. (2000) · Humana Press eBooks · doi:10.1007/978-1-59259-707-9_20 · Cited by 4 · see citing works
[The effect of neurohypophyseal peptides on the formation of conditioned active avoidance behavior].
Ibragimov, R. S. (1989) · PubMed · Cited by 2 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Rediscovering area CA2: unique properties and functions
Dudek, S. M., Alexander, G. M., & Farris, S. (2016) · Nature reviews. Neuroscience · doi:10.1038/nrn.2015.22 · Cited by 329 · see citing works
Targeted activation of the hippocampal CA2 area strongly enhances social memory
Smith, A. S., Williams Avram, S. K., Cymerblit-Sabba, A., Song, J., & Young, W. S. (2016) · Molecular Psychiatry · doi:10.1038/mp.2015.189 · Cited by 236 · see citing works
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
Ko, J. (2017) · Frontiers in Neural Circuits · doi:10.3389/fncir.2017.00041 · Cited by 212 · see citing works
Pagani, J. H., Zhao, M., Cui, Z., Williams Avram, S. K., Caruana, D. A., Dudek, S. M., & Young, W. S. (2015) · Molecular Psychiatry · doi:10.1038/mp.2014.47 · Cited by 204 · see citing works
Social and novel contexts modify hippocampal CA2 representations of space
Alexander, G. M., Farris, S., Pirone, J. R., Zheng, C., Colgin, L. L., & Dudek, S. M. (2016) · Nature Communications · doi:10.1038/ncomms10300 · Cited by 191 · see citing works
Oxytocin, Vasopressin, and Social Behavior: From Neural Circuits to Clinical Opportunities
Rigney, N., de Vries, G. J., Petrulis, A., & Young, L. J. (2022) · Endocrinology · doi:10.1210/endocr/bqac111 · Cited by 191 · see citing works
Lin, Y.-T., Hsieh, T.-Y., Tsai, T.-C., Chen, C.-C., Huang, C.-C., & Hsu, K.-S. (2018) · The Journal of Neuroscience · doi:10.1523/jneurosci.1896-17.2017 · Cited by 165 · see citing works
The Effect of Acute and Chronic Social Stress on the Hippocampal Transcriptome in Mice
Stankiewicz, A. M., Gościk, J., Majewska, A., Swiergiel, A. H., & Juszczak, G. R. (2015) · PLoS ONE · doi:10.1371/journal.pone.0142195 · Cited by 138 · see citing works
Social Memory and the Role of the Hippocampal CA2 Region
Tzakis, N., & Holahan, M. R. (2019) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2019.00233 · Cited by 122 · see citing works
Zhang, L., Hernández, V. S., Swinny, J. D., Verma, A. K., Giesecke, T., Emery, A. C., Mutig, K., García‐Segura, L. M., & Eiden, L. E. (2018) · Translational Psychiatry · doi:10.1038/s41398-018-0099-5 · Cited by 121 · see citing works
Kovac, S., & Walker, M. C. (2013) · Neuropeptides · doi:10.1016/j.npep.2013.10.015 · Cited by 112 · see citing works
Nolan, M., Roman, E., Nasa, A., Levins, K. J., O’Hanlon, E., O’Keane, V., & Willian Roddy, D. (2020) · Chronic Stress · doi:10.1177/2470547020944553 · Cited by 107 · see citing works
Hypothalamic Supraoptic and Paraventricular Nuclei
Armstrong, W. E. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-374245-2.00014-0 · Cited by 94 · see citing works
Multimodal mapping and analysis of the cyto- and receptorarchitecture of the human hippocampus
Palomero‐Gallagher, N., Kedo, O., Mohlberg, H., Zilles, K., & Amunts, K. (2020) · Brain Structure and Function · doi:10.1007/s00429-019-02022-4 · Cited by 90 · see citing works
Oxytocin and vasopressin in the rodent hippocampus
Cilz, N. I., Cymerblit‐Sabba, A., & Young, W. S. (2018) · Genes Brain & Behavior · doi:10.1111/gbb.12535 · Cited by 88 · see citing works
Stoop, R. (2014) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2014.09.012 · Cited by 84 · see citing works
Hernández, V. S., Hernández, O. R., de la Mora, M. P., Gómora, M. J., Fuxé, K., Eiden, L. E., & Zhang, L. (2016) · Frontiers in Neural Circuits · doi:10.3389/fncir.2016.00092 · Cited by 80 · see citing works
Hippocampal Area CA2: An Overlooked but Promising Therapeutic Target
Chevaleyre, V., & Piskorowski, R. A. (2016) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2016.06.007 · Cited by 80 · see citing works
Zhang, L., Hernández, V. S., Vázquez‐Juárez, E., Chay, F. K., & Barrio, R. A. (2016) · Frontiers in Neural Circuits · doi:10.3389/fncir.2016.00013 · Cited by 76 · see citing works
CA2 beyond social memory: Evidence for a fundamental role in hippocampal information processing
Lehr, A. B., Kumar, A., Tetzlaff, C., Hafting, T., Fyhn, M., & Stöber, T. M. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.03.020 · Cited by 74 · see citing works
ACE2 expression in rat brain: Implications for COVID-19 associated neurological manifestations
Hernández, V. S., Zetter, M. A., Guerra, E. C., Hernández‐Araiza, I., Karuzin, N., Hernández‐Pérez, O. R., Eiden, L. E., & Zhang, L. (2021) · Experimental Neurology · doi:10.1016/j.expneurol.2021.113837 · Cited by 76 · see citing works
Parallel social information processing circuits are differentially impacted in autism
Lewis, E. M., Stein-O’Brien, G. L., Patino, A. V., Nardou, R., Grossman, C. D., Brown, M., Bangamwabo, B., Ndiaye, N., Giovinazzo, D., Dardani, I., et al. (2020) · Neuron · doi:10.1016/j.neuron.2020.10.002 · Cited by 72 · see citing works
Whole-Brain Mapping the Direct Inputs of Dorsal and Ventral CA1 Projection Neurons
Tao, S., Wang, Y., Peng, J., Zhao, Y., He, X., Yu, X., Liu, Q., Jin, S., & Xu, F. (2021) · Frontiers in Neural Circuits · doi:10.3389/fncir.2021.643230 · Cited by 68 · see citing works
Connections of the juxtaventromedial region of the lateral hypothalamic area in the male rat
Hahn, J. D., & Swanson, L. W. (2015) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2015.00066 · Cited by 68 · see citing works
Oxytocin: Parallel Processing in the Social Brain?
Dölen, G. (2015) · Journal of Neuroendocrinology · doi:10.1111/jne.12284 · Cited by 65 · see citing works
Lesse, A., Rether, K., Gröger, N., Braun, K., & Bock, J. (2016) · Molecular Neurobiology · doi:10.1007/s12035-016-0043-8 · Cited by 66 · see citing works
Windows into stress: a glimpse at emerging roles for CRH <sup>PVN</sup> neurons
Rasiah, N. P., Loewen, S. P., & Bains, J. S. (2023) · Physiological Reviews · doi:10.1152/physrev.00056.2021 · Cited by 62 · see citing works
Spoljaric, A., Seja, P., Spoljaric, I., Virtanen, M. A., Lindfors, J., Uvarov, P., Summanen, M., Crow, A., Hsueh, B., Puskarjov, M., et al. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1717337114 · Cited by 60 · see citing works
Hippocampal area CA2: an emerging modulatory gateway in the hippocampal circuit
Benoy, A., Dasgupta, A., & Sajikumar, S. (2018) · Experimental Brain Research · doi:10.1007/s00221-018-5187-5 · Cited by 57 · see citing works
Hernández, V. S., Vázquez‐Juárez, E., Márquez, M. M., Jáuregui-Huerta, F., Barrio, R. A., & Zhang, L. (2015) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2015.00130 · Cited by 57 · see citing works
Zhang, L., Hernández, V. S., Gerfen, C. R., Jiang, S. Z., Zavala, L., Barrio, R. A., & Eiden, L. E. (2021) · eLife · doi:10.7554/elife.61718 · Cited by 54 · see citing works
Regulation of synaptic plasticity in hippocampal area CA2
Carstens, K. E., & Dudek, S. M. (2019) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2018.07.008 · Cited by 55 · see citing works
The Role of Serotonin, Vasopressin, and Serotonin/Vasopressin Interactions in Aggressive Behavior
Morrison, T. R., & Melloni, R. H. (2014) · Current topics in behavioral neurosciences · doi:10.1007/7854_2014_283 · Cited by 51 · see citing works
Harden, S. W., & Frazier, C. J. (2016) · Hippocampus · doi:10.1002/hipo.22595 · Cited by 40 · see citing works
Neuropeptides and small-molecule amine transmitters: cooperative signaling in the nervous system
Eiden, L. E., Hernández, V. S., Jiang, S. Z., & Zhang, L. (2022) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-022-04451-7 · Cited by 36 · see citing works
Yang, C., Zhang, X., Gao, J., Wang, M., & Yang, Z. R. (2017) · Translational Psychiatry · doi:10.1038/tp.2017.121 · Cited by 36 · see citing works
Randesi, M., Zhou, Y., Mazid, S., Odell, S. C., Gray, J. D., da Rosa, J. C., McEwen, B. S., Milner, T. A., & Kreek, M. J. (2018) · Neurobiology of Stress · doi:10.1016/j.ynstr.2018.01.001 · Cited by 32 · see citing works
Dynamic Hippocampal CA2 Responses to Contextual Spatial Novelty
Bhasin, G., & Nair, I. R. (2022) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2022.923911 · Cited by 31 · see citing works
Corbani, M., Marir, R., Trueba, M., Chafaï, M., Vincent, A., Borie, A. M., Desarménien, M. G., Ueta, Y., Corbani, M., Olma, A., et al. (2017) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2017.10.011 · Cited by 31 · see citing works
Hernández‐Pérez, O. R., Hernández, V. S., Nava-Kopp, A. T., Barrio, R. A., Seifi, M., Swinny, J. D., Eiden, L. E., & Zhang, L. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.00196 · Cited by 30 · see citing works
Female HPA axis displays heightened sensitivity to pre-pubertal stress
Brydges, N. M., Best, C., & Thomas, K. L. (2019) · Stress · doi:10.1080/10253890.2019.1658738 · Cited by 30 · see citing works
Vasopressin Receptor Antagonists
Palmer, B. F. (2015) · Current Hypertension Reports · doi:10.1007/s11906-014-0510-4 · Cited by 28 · see citing works
Lajud, N., Gonzalez-Zapien, R., Roque, A., Tinajero, E., Valdez, J. J., Clapp, C., & Torner, L. (2013) · Hormones and Behavior · doi:10.1016/j.yhbeh.2013.10.005 · Cited by 27 · see citing works
Long term effects of early life stress on HPA circuit in rodent models
Babicola, L., Ventura, R., D’Addario, S. L., Ielpo, D., Andolina, D., & Segni, M. D. (2020) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2020.111125 · Cited by 27 · see citing works
Lopes‐Azevedo, S., Fortaleza, E. A. T., Busnardo, C., Scopinho, A. A., Matthiesen, M., Antunes‐Rodrigues, J., & Corrêa, F. M. D. A. (2019) · Neuroendocrinology · doi:10.1159/000500160 · Cited by 25 · see citing works
Bilateral lesions of the paraventricular hypothalamic nucleus disrupt nursing behavior in rabbits
Domínguez, M., Aguilar‐Roblero, R. A., & González‐Mariscal, G. (2017) · European Journal of Neuroscience · doi:10.1111/ejn.13656 · Cited by 22 · see citing works
The CA2 hippocampal subfield in humans: A review
Insausti, R., Muñoz, M., & Serrano, A. M. I. (2023) · Hippocampus · doi:10.1002/hipo.23547 · Cited by 23 · see citing works
Immunohistochemical field parcellation of the human hippocampus along its antero-posterior axis
González‐Arnay, E., Pérez-Santos, I., Sánchez, L. J., Cid, E., Gal, B., de la Prida, L. M., & Cavada, C. (2024) · Brain Structure and Function · doi:10.1007/s00429-023-02725-9 · Cited by 25 · see citing works
Stöber, T. M., Lehr, A. B., Hafting, T., Kumar, A., & Fyhn, M. (2020) · Hippocampus · doi:10.1002/hipo.23256 · Cited by 20 · see citing works
Zhou, M., Cui, S., Wang, K., Wu, S.-B., Zhu, G., Cao, J., & Zhou, Y. (2018) · Neural Regeneration Research · doi:10.4103/1673-5374.237124 · Cited by 21 · see citing works
Dynamic Modulation of Mouse Locus Coeruleus Neurons by Vasopressin 1a and 1b Receptors
Campos‐Lira, E., Kelly, L., Seifi, M., Jackson, T., Giesecke, T., Mutig, K., Koshimizu, T., Hernández, V. S., Zhang, L., & Swinny, J. D. (2018) · Frontiers in Neuroscience · doi:10.3389/fnins.2018.00919 · Cited by 21 · see citing works
Zimmermann-Peruzatto, J. M., Lazzari, V. M., Agnes, G., Becker, R. O., de Moura, A. C., Guedes, R. P., Lucion, A. B., Almeida, S., & Giovenardi, M. (2016) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-016-0419-3 · Cited by 21 · see citing works
Zhang, L., & Eiden, L. E. (2018) · Cell and Tissue Research · doi:10.1007/s00441-018-2958-z · Cited by 21 · see citing works
Zhang, L., Hernández, V. S., Zetter, M. A., & Eiden, L. E. (2020) · Journal of Neuroendocrinology · doi:10.1111/jne.12831 · Cited by 19 · see citing works
Oxytocin and vasopressin in the hippocampus
Zăgrean, A., Georgescu, I.-A., Ieșanu, M. I., Ionescu, R.-B., Haret, R. M., Panaitescu, A. M., & Zăgrean, L. (2022) · Vitamins and hormones · doi:10.1016/bs.vh.2021.11.002 · Cited by 20 · 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
Differential Effects of Dietary MSG on Hippocampal Dependent Memory Are Mediated by Diet
Holton, K. F., Hargrave, S. L., & Davidson, T. L. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.00968 · Cited by 15 · see citing works
Li, C.-Y., Zhang, L., Li, J., Qi, C., Li, D.-Y., Liu, X., & Xian, Q. (2017) · BioMed Research International · doi:10.1155/2017/3214918 · Cited by 15 · see citing works
Vasopressin as Possible Treatment Option in Autism Spectrum Disorder
László, K., Vörös, D., Correia, P., Fazekas, C. L., Török, B., Plangár, I., & Zelena, D. (2023) · Biomedicines · doi:10.3390/biomedicines11102603 · Cited by 13 · see citing works
Neural mechanisms of AVPR1A RS3-RS1 haplotypes that impact verbal learning and memory
Zhang, Y., Zhu, D., Zhang, P., Li, W., Qin, W., Liu, F., Xu, J., Xu, Q., Wang, J., Ye, Z., et al. (2020) · NeuroImage · doi:10.1016/j.neuroimage.2020.117283 · Cited by 13 · see citing works
Imaging the Hypothalamo-Neurohypophysial System
Bárez‐López, S., Scanlon, L., Murphy, D., & Greenwood, M. P. (2021) · Neuroendocrinology · doi:10.1159/000519233 · Cited by 13 · see citing works
Montañez‐Miranda, C., Bramlett, S. N., & Hepler, J. R. (2022) · Hippocampus · doi:10.1002/hipo.23492 · Cited by 12 · see citing works
Zetter, M. A., Roque, A., Hernández, V. S., Hernández‐Pérez, O. R., Gómora, M. J., Ruiz‐Velasco, S., Eiden, L. E., & Zhang, L. (2021) · Journal of Neuroendocrinology · doi:10.1111/jne.12969 · Cited by 12 · see citing works
Peptide-Liganded G Protein-Coupled Receptors as Neurotherapeutics
Eiden, L. E., Goosens, K. A., Jacobson, K. A., Leggio, L., & Zhang, L. (2020) · ACS Pharmacology & Translational Science · doi:10.1021/acsptsci.0c00017 · Cited by 11 · 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
Zhang, L., Hernández, V. S., Estrada, F. S., & Luján, R. (2014) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2014.02.002 · Cited by 9 · see citing works
Schatz, K. C., Brown, L. M., Barrett, A., Roth, L. C., Grinevich, V., & Paul, M. J. (2019) · Scientific Reports · doi:10.1038/s41598-019-44776-1 · Cited by 9 · see citing works
Zhang, L., Hernández, V. S., Zetter, M. A., Hernández‐Pérez, O. R., González, R. H., Camacho‐Arroyo, I., Eiden, L. E., & Millar, R. P. (2025) · Journal of Neuroendocrinology · doi:10.1111/jne.70007 · Cited by 7 · see citing works
Role of the hypothalamic paraventricular nucleus in anxiety disorders
Chen, W., & Zetter, M. A. (2022) · Stress and Brain · doi:10.26599/sab.2022.9060019 · Cited by 7 · see citing works
Social odors drive hippocampal CA2 place cell responses to social stimuli
Robson, E., Donahue, M. M., Mably, A. J., Demetrovich, P. G., Hewitt, L. T., & Colgin, L. L. (2024) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2024.102708 · Cited by 8 · see citing works
The Central Inflammatory Network: A Hypothalamic fMRI Study of Experimental Endotoxemia in Humans
Färber, N., Manuel, J., May, M., Foadi, N., & Beißner, F. (2021) · NeuroImmunoModulation · doi:10.1159/000519061 · Cited by 7 · see citing works
Jiang, S., Wang, Y.-Q., Tang, Y., Lu, X., & Guo, D. (2022) · Journal of Inflammation Research · doi:10.2147/jir.s345108 · Cited by 7 · see citing works
Progress in regulatory peptide research
Zhang, L., & Eiden, L. E. (2019) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.14260 · Cited by 7 · see citing works
Zhang, L., Zetter, M. A., Hernández, V. S., Hernández‐Pérez, O. R., Jáuregui-Huerta, F., Krabichler, Q., & Grinevich, V. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25136988 · Cited by 6 · see citing works
Vasopressin acts as a synapse organizer in limbic regions by boosting PSD95 and GluA1 expression
Zhang, L., Padilla‐Flores, T., Hernández, V. S., Zetter, M. A., Campos‐Lira, E., Escobar, L. I., Millar, R. P., & Eiden, L. E. (2022) · Journal of Neuroendocrinology · doi:10.1111/jne.13164 · Cited by 5 · see citing works
Zhao, F., & Behnisch, T. (2023) · Biomedicines · doi:10.3390/biomedicines11071996 · Cited by 6 · see citing works
Arakawa, H., Tokashiki, M., Higuchi, Y., & Konno, T. (2024) · Peptides · doi:10.1016/j.peptides.2024.171178 · Cited by 4 · see citing works
Vasopressin: Roles in Modulating Social Behaviors
Williams, S. K., & Cymerblit‐Sabba, A. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-803592-4.00057-2 · Cited by 5 · see citing works
Hernández‐Pérez, O. R., Hernández, V. S., Zetter, M. A., Eiden, L. E., & Zhang, L. (2022) · Journal of Neuroendocrinology · doi:10.1111/jne.13202 · Cited by 4 · see citing works
Zhang, L., Hernández, V. S., Murphy, D., Young, W. S., & Eiden, L. E. (2021) · Masterclass in neuroendocrinology · doi:10.1007/978-3-030-86630-3_7 · Cited by 4 · see citing works
Effects of estrogen on social recognition and oxytocin regulating synaptic plasticity
Gao, T., Ying, Z., Yang, Y., & Xu, X. (2025) · Physiology & Behavior · doi:10.1016/j.physbeh.2025.114843 · Cited by 3 · see citing works
Melino, S., & Mormone, E. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.745138 · Cited by 1 · see citing works
Barrera-Conde, M., Ramon‐Duaso, C., González-Parra, J. A., Veza-Estévez, E., Chevaleyre, V., Piskorowski, R. A., de la Torre, R., Busquets-García, A., & Robledo, P. (2024) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2024.102652 · Cited by 1 · see citing works
Imaging Phenotypes of Stress Based on Functional MRI
Kapoor, A. (2023) · Journal of Clinical and Medical Research · doi:10.37191/mapsci-2582-4333-5(1)-127 · Cited by 1 · see citing works
Lawford‐Smith, H. (2015)
Zhang, H. B., Marquez-Machorro, M., Hernández, V. S., Molina, A., Zhang, L., Govezensky, T., & Barrio, R. A. (2020) · arXiv (Cornell University) · doi:10.48550/arxiv.2011.04040
PERINEURONAL NETS IN HIPPOCAMPAL AREA CA2: REGULATION BY ACTIVITY AND DISEASE
Carstens, K. E. (2020) · Carolina Digital Repository (University of North Carolina at Chapel Hill) · doi:10.17615/khgn-dw13
Brown, J. P., Marshall, S., Walker, R. M., Campbell, A. I., Hayward, C., McIntosh, A. M., Evans, K. L., & Thomson, P. A. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.11.13.566835
The role of hippocampal subregions in learning and memory
Shin, J., Lee, J. W., & Jung, M. W. (2025) · Elsevier eBooks · doi:10.1016/b978-0-443-15754-7.00079-1
Effects of bisphenol-a on vasopressin regulating synaptic plasticity of hippocampus
Xu, X., Wang, J., & Yang, Y. (2025) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2025.107531
Lopes‐Azevedo, S., Suzuki, G. M. F., Busnardo, C., Scopinho, A. A., Matthiesen, M., Antunes‐Rodrigues, J., & Corrêa, F. M. D. A. (2025) · Behavioural Brain Research · doi:10.1016/j.bbr.2025.115802
New regulators in oxytocin and vasopressin release : role of the endolysosomal two-pore channels
Martucci, L. L. (2021) · theses.fr (ABES) · doi:10.70675/027d1ae2zd2ebz4677za019ze6ccd94cafe9
Hypothalamic supraoptic and paraventricular nuclei
Krabichler, Q., & Grinevich, V. (2026) · Elsevier eBooks · doi:10.1016/b978-0-443-24078-2.00012-7
- Authors
- Zhang, L., & Hernández, V. S.
- Affiliations
- Universidad Nacional Autónoma de México (MX)
- Corresponding author
- Zhang, L.
- Venue
- Neuroscience
- Publisher
- Elsevier BV
- Published
- 2013-01
- Volume
- 228
- Pages
- 139-162
- ISSN
- 0306-4522 (ISSN-L)
- OpenAlex
- W2024418933
- Cited by
- 96
- References
- 70
- Citations by year
- 2026: 1 · 2025: 7 · 2024: 6 · 2023: 6 · 2022: 11 · 2021: 9 · 2020: 10 · 2019: 7 · 2018: 8 · 2017: 7 · 2016: 10 · 2015: 6 · 2014: 5 · 2013: 2 · 2012: 1
- FWCI
- 6.74
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Funders
- CONACYT (79641, 127777)
- PAPIIT-UNAM (IN218111)
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Keywords
- vasopressin, hippocampus, supraoptic nucleus, paraventricular nucleus, magnocellular neurons, synaptic innervation, varicose axons, interneurons, pyramidal neurons, amygdala, bed nucleus of the stria terminalis, fimbria-fornix, retrograde tracing
- MeSH terms
- Animals, Arginine Vasopressin, Hippocampus, Hypothalamus, Anterior, Male, Nerve Fibers, Myelinated, Neural Pathways, Paraventricular Hypothalamic Nucleus, Synapses, Rats, Wistar, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
