Vasopressin cells in the medial amygdala of the rat project to the lateral septum and ventral hippocampus

Caffé, A. R.; van Leeuwen, F. W.; Luiten, P. G. M.

doi:10.1002/cne.902610206

Cited by 287Neuroendocrine regulation and behaviorNeuropeptides and Animal PhysiologyMemory and Neural Mechanisms

Vasopressin cells in the medial amygdala of the rat project to the lateral septum and ventral hippocampus

Caffé, A. R., van Leeuwen, F. W., Luiten, P. G. M.·1987·Journal of Comparative Neurology

DOI 10.1002/cne.902610206

Open this paper in CoChat — free account

Abstract

The rat brain contains a large number of vasopressin (VP) immunoreactive fibers, the sites of origin of which have not yet been established completely. For instance, the sources of VP fiber systems in the amygdala, ventral hippocampus (VH), mediodorsal thalamic nucleus, ventral tegmental area, and dorsal raphe yet remain obscure. These VP fibers may originate in any of the recently described extrahypothalamic VP cell groups, viz., medial amygdaloid nucleus (AME), dorsomedial hypothalamic nucleus, or locus coeruleus, since VP efferents from these cells still remain to be demonstrated. In search of AME VP efferents three approaches were followed: (1) the Phaseolus vulgaris anterograde tracing method, (2) immunocytochemistry after AME lesioning, and (3) retrograde transport of a fluorescent dye in combination with immunofluorescence. The results demonstrate that VP cells in the AME project to (1) the lateral septum (LS) by the ventral amygdalofugal pathway and (2) the VH via the amygdalohippocampal transition zone. In addition, the VP projection from the bed nucleus of the stria terminalis (BST) to the LS was confirmed. There was no indication that VP cells in the AME project through the amygdalotegmental pathway to the medulla oblongata and spinal cord. The results support the possibility that the BST and AME are an anatomical entity that may be part of the central loci controlling sexual processes in the rat.

Integrity signals

Registry

Crossref · 10.1002/cne.902610206

Cites

40 of 40 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

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?

The LS receives vasopressinergic inputs directly from the MeA and the bed nucleus of the stria terminalis (BNST).
“It receives vasopressinergic inputs directly from the MeA (Caffe et al., 1987) and the bed nucleus of the stria terminalis (BNST) (De Vries & Buijs, 1983).”
From Developmental origins of sex differences in the neural circuitry of play (2020) · cites this paper as Caffe et al., 1987
In Callithrix marmosets, there was low but detectable AVP immunoreactivity in the LS, but fibers did not form a dense plexus as in several rodent species.
“In Callithrix marmosets, there was low, but detectable, AVP immunoreactivity in the LS (confirmed by in situ hybridization; Wang et al., 1997b), but the fibers did not form a dense plexus as found in several rodent species (Caffé et al., 1987; de Vries and Ruijs, 1983).”
From Neuropeptide diversity and the regulation of social behavior in New World primates (2016) · cites this paper as Caffé et al., 1987

Memory deficits associated with senescence: A neurophysiological and behavioral study in the rat.
Barnes, C. A. (1979) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0077579 · Cited by 2,088 · see citing works
Atlas of estradiol‐concentrating cells in the central nervous system of the female rat
Pfaff, D. W., & Keiner, M. (1973) · The Journal of Comparative Neurology · doi:10.1002/cne.901510204 · Cited by 1,494 · see citing works
WITHDRAWN: References
Paxinos, G., & WATSON, C. R. R. (1982) · Elsevier eBooks · doi:10.1016/b978-0-12-547620-1.50007-2 · Cited by 824 · see citing works
The origin of the vasopressinergic and oxytocinergic innervation of the rat brain with special reference to the lateral septum
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 vasopressinergic innervation of the brain in normal and castrated rats
DeVries, G. J., Buijs, R. M., van Leeuwen, F. W., Caffé, A. R., & Swaab, D. F. (1985) · Journal of Comparative Neurology · doi:10.1002/cne.902330206 · Cited by 522 · see citing works
Projections of the bed nucleus of the stria terminalis to the mesencephalon, pons, and medulla oblongata in the cat
Holstege, G., Meiners, L. C., & Tan, K. (1985) · Experimental Brain Research · doi:10.1007/bf00235319 · Cited by 342 · see citing works
Immunofluorescence of vasopressin and oxytocin in the rat hypothalamo-neurohypophyseal system
Swaab, D. F., Pool, C. W., & Nijveldt, F. (1975) · Journal of Neural Transmission · doi:10.1007/bf01253126 · Cited by 323 · see citing works
Ontogeny of the vasopressinergic neurons of the suprachiasmatic nucleus and their extrahypothalamic projections in the rat brain–presence of a sex difference in the lateral septum
De Vries, G. J., Buds, R. M., & Swaab, D. F. (1981) · Brain Research · doi:10.1016/0006-8993(81)90989-6 · Cited by 319 · see citing works
The Amygdaloid Projection Field in the Rat as Studied with the Cupric-Silver Method
de Olmos, J. S. (1972) · Advances in behavioral biology · doi:10.1007/978-1-4615-8987-7_7 · Cited by 294 · see citing works
Medial Nucleus of the Amygdala Mediates Chemosensory Control of Male Hamster Sexual Behavior
Lehman, M. N., Winans, S. S., & Powers, J. B. (1980) · Science · doi:10.1126/science.7423209 · Cited by 282 · see citing works
Immuno-electron microscopical demonstration of vasopressin and oxytocin synapses in the limbic system of the rat
Buijs, R. M., & Swaab, D. F. (1979) · Cell and Tissue Research · doi:10.1007/bf00233648 · Cited by 262 · see citing works
Vasopressin cells in the bed nucleus of the stria terminalis of the rat: sex differences and the influence of androgens
van Leeuwen, F. W., Caffe, A. R., & Vries, G. J. D. (1985) · Brain Research · doi:10.1016/0006-8993(85)90348-8 · Cited by 248 · see citing works
Evidence for a direct projection from oxytocin and vasopressin neurons in the hypothalamic paraventricular nucleus to the medulla oblongata: Immunohistochemical visualization of both the horseradish peroxidase transported and the peptide produced by the same neurons
Sofroniew, M. V., & Schrell, U. (1981) · Neuroscience Letters · doi:10.1016/0304-3940(81)90108-7 · Cited by 224 · see citing works
Sexually dimorphic regions in the medial preoptic area and the bed nucleus of the stria terminalis of the guinea pig brain: a description and an investigation of their relationship to gonadal steroids in adulthood
Hines, M., Davis, F., Coquelin, A., Rw, G., & Gorski, R. (1985) · Journal of Neuroscience · doi:10.1523/jneurosci.05-01-00040.1985 · Cited by 220 · see citing works
Vasopressin fiber pathways in the rat brain following suprachiasmatic nucleus lesioning
Hoorneman, E. M. D., & Buijs, R. M. (1982) · Brain Research · doi:10.1016/0006-8993(82)90246-3 · Cited by 211 · see citing works
Vasopressin-immunoreactive cell bodies in the bed nucleus of the stria terminalis of the rat
van Leeuwen, F., & Caffé, R. (1983) · Cell and Tissue Research · doi:10.1007/bf00211473 · Cited by 206 · see citing works
Vasopressin-immunoreactive cells in the dorsomedial hypothalamic region, medial amygdaloid nucleus and locus coeruleus of the rat
Caffe´, A. R., & van Leeuwen, F. W. (1983) · Cell and Tissue Research · doi:10.1007/bf00222229 · Cited by 199 · see citing works
Characteristics of sex behaviour in male rats following castration
Davidson, J. M. (1966) · Animal Behaviour · doi:10.1016/s0003-3472(66)80082-9 · Cited by 194 · see citing works
Sexual difference in nuclear volume and its ontogeny in the rat amygdala
Mizukami, S., Nishizuka, M., & Arai, Y. (1983) · Experimental Neurology · doi:10.1016/0014-4886(83)90235-2 · Cited by 178 · see citing works
Vasopressin and oxytocin: distribution and putative functions in the brain
Buijs, R. M., De Vries, G. J., Van Leeuwen, F. W., & Swaab, D. F. (1983) · Progress in Brain Research · doi:10.1016/s0079-6123(08)64379-4 · Cited by 167 · see citing works
Copulatory behavior in male rats with lesions in the bed nucleus of the stria terminalis
Emery, D. E., & Sachs, B. D. (1976) · Physiology & Behavior · doi:10.1016/0031-9384(76)90044-5 · Cited by 151 · see citing works
Amygdalotegmental projections in the rat, cat and rhesus monkey
Hopkins, D. A. (1975) · Neuroscience Letters · doi:10.1016/0304-3940(75)90041-5 · Cited by 143 · see citing works
The cortico-medial amygdala in the central nervous system organization of agonistic behavior
Luiten, P. G. M., Koolhaas, J. M., de Boer, S. F., & Koopmans, S. J. (1985) · Brain Research · doi:10.1016/0006-8993(85)90597-9 · Cited by 137 · see citing works
Self-citation
Vasopressin alters female sexual behaviour by acting on the brain independently of alterations in blood pressure
Södersten, P., Henning, M., Melin, P., & Ludin, S. M. (1983) · Nature · doi:10.1038/301608a0 · Cited by 134 · see citing works
Ontogeny of vasopressin and oxytocin in the fetal rat: Early vasopressinergic innervation of the fetal brain
Buijs, R. M., Velis, D. N., & Swaab, D. F. (1980) · Peptides · doi:10.1016/0196-9781(80)90009-1 · Cited by 121 · see citing works
Vasopressin- and neurophysin-immunoreactive neurons in the septal region, medial amygdala and locus coeruleus in colchicine-treated rats
Sofroniew, M. V. (1985) · Neuroscience · doi:10.1016/0306-4522(85)90217-9 · Cited by 112 · see citing works
Central Nervous System Distribution of Vasopressin, Oxytocin, and Neurophysin
Sofroniew, M. V., & Weindl, A. (1981) · Elsevier eBooks · doi:10.1016/b978-0-12-474980-1.50022-2 · Cited by 110 · see citing works
Facilitatory and inhibitory effects of electrochemical stimulation of the amygdala on the release of luteinizing hormone
Beltramino, C. A., & Taleisnik, S. (1978) · Brain Research · doi:10.1016/0006-8993(78)90437-7 · Cited by 107 · see citing works
A [14C]2-deoxyglucose analysis of the functional neural pathways of the limbic forebrain in the rat. I. The amygdala
Watson, R. E., Troiano, R. A., Poulakos, J. J., Weiner, S., Block, C. H., & Siegel, A. (1983) · Brain Research Reviews · doi:10.1016/0165-0173(83)90020-6 · Cited by 92 · see citing works
Central Actions of Neurohypophysial Hormones
de Wied, D. (1983) · Progress in brain research · doi:10.1016/s0079-6123(08)64383-6 · Cited by 75 · see citing works
Phaseolus vulgaris leuco-agglutinin immunohistochemistry. A comparison between autoradiographic and lectin tracing of neuronal efferents
Horst, G. J. T., Groenewegen, H. J., Karst, H., & Luiten, P. G. M. (1984) · Brain Research · doi:10.1016/0006-8993(84)90500-6 · Cited by 75 · see citing works
Self-citation
Changes with aging in the vasopressin and oxytocin innervation of the rat brain
Fliers, E., Vries, G. J. D., & Swaab, D. F. (1985) · Brain Research · doi:10.1016/0006-8993(85)90351-8 · Cited by 74 · see citing works
The distribution of hypothalamic and extrahypothalamic vasotocinergic cells and fibers in the brain of a lizard, Gekko gecko: Presence of a sex difference
Stoll, C., & Voorn, P. (1985) · The Journal of Comparative Neurology · doi:10.1002/cne.902390206 · Cited by 74 · see citing works
Facilitation of avoidance behavior by vasopressin fragments microinjected into limbic-midbrain structures
Kovács, G. L., Veldhuis, H. D., Versteeg, D. H. G., & de Wied, D. (1986) · Brain Research · doi:10.1016/0006-8993(86)90805-x · Cited by 72 · see citing works
Testosterone and the decline of sexual behavior in aging male rats
Chambers, K. C., & Phoenix, C. H. (1984) · Behavioral and Neural Biology · doi:10.1016/s0163-1047(84)90194-8 · Cited by 49 · see citing works
Solitary magnocellular neurons in the homozygous Brattleboro rat have vasopressin and glycopeptide immunoreactivity
Richards, S.-J., Morris, R. J., & Raisman, G. (1985) · Neuroscience · doi:10.1016/0306-4522(85)90196-4 · Cited by 42 · see citing works
Pathways conducting amygdaloid influence on feminine sexual behavior in the rat
Mascó, D. H., & Carrer, H. F. (1984) · Behavioural Brain Research · doi:10.1016/0166-4328(84)90212-2 · Cited by 33 · see citing works
Study on the Bed Nucleus of Stria Terminalis in Relation to Gonadotropin Control
KAWAKAMI, M., & Kimura, F. (1974) · Endocrinologia Japonica · doi:10.1507/endocrj1954.21.125 · Cited by 24 · see citing works
Propressophysin is present in neurones at multiple sites in wistar and homozygous brattleboro rat brain
van Leeuwen, F. W., Caffé, R., van der Sluis, P. J., Sluiter, A. A., van der Woude, T. P., Seidah, N. G., & Chrétien, M. (1986) · Brain Research · doi:10.1016/0006-8993(86)90272-6 · Cited by 21 · see citing works
Intrinsic connections in the medial amygdala as revealed by complete deafferentation
Nishizuka, M., & Arai, Y. (1983) · Neuroscience Letters · doi:10.1016/0304-3940(83)90325-7 · Cited by 9 · see citing works

Flagged first, then by citations

Sorted by citations

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
Vasopressin and oxytocin release within the brain: a dynamic concept of multiple and variable modes of neuropeptide communication
Landgraf, R., & Neumann, I. D. (2004) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2004.05.001 · Cited by 1,059 · see citing works
The Vertebrate mesolimbic reward system and social behavior network: A comparative synthesis
O'Connell, L. A., & Hofmann, H. A. (2011) · Journal of Comparative Neurology · doi:10.1002/cne.22735 · Cited by 986 · see citing works
Organization of projections from the medial nucleus of the amygdala: A PHAL study in the rat
Canteras, N. S., Simerly, R. B., & Swanson, L. W. (1995) · The Journal of Comparative Neurology · doi:10.1002/cne.903600203 · Cited by 884 · see citing works
Comparison of spatial firing characteristics of units in dorsal and ventral hippocampus of the rat
Jung, M. W., Wiener, S. I., & McNaughton, B. L. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-12-07347.1994 · Cited by 818 · see citing works
Connections of the rat lateral septal complex 1Published on the World Wide Web on 2 June 1997. 1
Risold, P. Y., & Swanson, L. W. (1997) · Brain Research Reviews · doi:10.1016/s0165-0173(97)00009-x · Cited by 671 · see citing works
Combinatorial amygdalar inputs to hippocampal domains and hypothalamic behavior systems.
Petrovich, G., Canteras, N., & Swanson, L. (2001) · Brain research. Brain research reviews · doi:10.1016/s0165-0173(01)00080-7 · Cited by 628 · see citing works
Regulation of affect by the lateral septum: implications for neuropsychiatry
Sheehan, T. P., Chambers, R. A., & Russell, D. S. (2004) · Brain Research Reviews · doi:10.1016/j.brainresrev.2004.04.009 · Cited by 514 · see citing works
Vasopressin and oxytocin receptor systems in the brain: Sex differences and sex-specific regulation of social behavior
Dumais, K. M., & Veenema, A. H. (2016) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2015.04.003 · Cited by 520 · see citing works
“VP-ir fibers Macaques Medial septum, BNST, amygdala, hippocampus VTA, peraquaductal gray, raphe, LC, NTS, parabrachial nuclei, diagonal band Caffé et al. (1989)”
BackgroundInfluential
Neuromodulation by Oxytocin and Vasopressin
Stoop, R. (2012) · Neuron · doi:10.1016/j.neuron.2012.09.025 · Cited by 506 · 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
Oxytocin, vasopressin, and social recognition in mammals
Bielsky, I. F., & Young, L. J. (2004) · Peptides · doi:10.1016/j.peptides.2004.05.019 · Cited by 460 · see citing works
The hypothalamic-neurohypophysial system regulates the hypothalamic–pituitary–adrenal axis under stress: an old concept revisited
Engelmann, M., Landgraf, R., & Wotjak, C. T. (2004) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2004.09.001 · Cited by 450 · see citing works
Genomic anatomy of the hippocampus
Thompson, C. L., Pathak, S. D., Jeromin, A., Ng, L. L., MacPherson, C. R., Mortrud, M. T., Cusick, A., Riley, Z. L., Sunkin, S. M., Bernard, A., et al. (2008) · Neuron · doi:10.1016/j.neuron.2008.12.008 · Cited by 403 · see citing works
Neuropeptide systems as novel therapeutic targets for depression and anxiety disorders
Holmes, A., Heilig, M. A., Rupniak, N. M. J., Steckler, T., & Griebel, G. (2003) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2003.09.011 · Cited by 401 · see citing works
Role of septal vasopressin innervation in paternal behavior in prairie voles (Microtus ochrogaster).
Wang, Z., Ferris, C. F., & De Vries, G. J. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.1.400 · Cited by 381 · see citing works
Sexual differentiation of central vasopressin and vasotocin systems in vertebrates: different mechanisms, similar endpoints
De Vries, G. J., & Panzica, G. C. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2005.07.050 · Cited by 346 · see citing works
Immunohistochemical Localization of the Vasopressin V1b Receptor in the Rat Brain and Pituitary Gland: Anatomical Support for Its Involvement in the Central Effects of Vasopressin
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
Chronic ethanol ingestion decreases vasopressin mRNA in hypothalamic and extrahypothalamic nuclei of mouse brain
Gulya, K., Dave, J. R., & Hoffman, P. L. (1991) · Brain Research · doi:10.1016/0006-8993(91)90125-f · Cited by 265 · see citing works
Chemoarchitecture of the rat lateral septal nucleus 1Published on the World Wide Web on 2 June 1997. 1
Risold, P. Y., & Swanson, L. W. (1997) · Brain Research Reviews · doi:10.1016/s0165-0173(97)00008-8 · Cited by 263 · see citing works
HPA axis responsiveness to stress: implications for healthy aging
Aguilera, G. (2011) · Experimental Gerontology · doi:10.1016/j.exger.2010.08.023 · Cited by 250 · 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
The vasopressin 1b receptor is prominent in the hippocampal area CA2 where it is unaffected by restraint stress or adrenalectomy
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
Anatomy, Development, and Function of Sexually Dimorphic Neural Circuits in the Mammalian Brain
Vries, G. J. D., & Simerly, R. B. (2002) · Elsevier eBooks · doi:10.1016/b978-012532104-4/50066-4 · Cited by 218 · see citing works
Sexual dimorphism in the mammalian limbic system
Madeira, M. D., & Lieberman, A. R. (1995) · Progress in Neurobiology · doi:10.1016/0301-0082(94)00052-j · Cited by 202 · see citing works
Species, sex and individual differences in the vasotocin/vasopressin system: relationship to neurochemical signaling in the social behavior neural network
Albers, H. E. (2015) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2014.07.001 · Cited by 200 · see citing works
Neuropeptide receptor ligands as drugs for psychiatric diseases: the end of the beginning?
Griebel, G., & Holsboer, F. (2012) · Nature Reviews Drug Discovery · doi:10.1038/nrd3702 · Cited by 194 · see citing works
Chapter 1.1 Anatomy and function of extrahypothalamic vasopressin systems in the brain
Vries, G. J. D., & MILLER, M. A. (1999) · Progress in brain research · doi:10.1016/s0079-6123(08)61558-7 · Cited by 183 · see citing works
Differential projections of the anterior and posterior regions of the medial amygdaloid nucleus in the Syrian hamster
Gomez, D. M., & Newman, S. W. (1992) · Journal of Comparative Neurology · doi:10.1002/cne.903170208 · Cited by 185 · see citing works
Distinct correlations of vasopressin release within the lateral septum and the bed nucleus of the stria terminalis with the display of intermale aggression
Veenema, A. H., Beiderbeck, D. I., Lukas, M., & Neumann, I. D. (2010) · Hormones and Behavior · doi:10.1016/j.yhbeh.2010.03.006 · Cited by 180 · see citing works
Sex and Species Differences in the Vasopressin Innervation of Sexually Naive and Parental Prairie Voles, Microtus ochrogaster and Meadow Voles, Microtus pennsylvanicus
Bamshad, M., Novak, M. A., & De Vries, G. J. (1993) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.1993.tb00480.x · Cited by 175 · see citing works
Sex differences in vasopressin and oxytocin innervation of the brain
DEVRIES, G. (2008) · Progress in Brain Research · doi:10.1016/s0079-6123(08)00402-0 · Cited by 169 · see citing works
Sex-specific modulation of juvenile social play by vasopressin
Veenema, A. H., Bredewold, R., & De Vries, G. J. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.06.002 · Cited by 166 · see citing works
“To test whether AVP projections of the BNST or MeA modulate social play, we targeted the LS because this area receives projections from AVP-expressing neurons in the BNST and MeA that are denser in males than in females (De Vries & Buijs, 1983; Van Leeuwen et al., 1985; Caffe et al., 1987).”
Background
Toward understanding how early-life social experiences alter oxytocin- and vasopressin-regulated social behaviors
Veenema, A. H. (2011) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.12.002 · Cited by 157 · see citing works
Innovative Approaches for the Treatment of Depression: Targeting the HPA Axis
THOMSON, F. J., & Craighead, M. W. (2007) · Neurochemical Research · doi:10.1007/s11064-007-9518-3 · Cited by 155 · see citing works
Topographical projection from the hippocampal formation to the amygdala: A combined anterograde and retrograde tracing study in the rat
Kishi, T., Tsumori, T., Yokota, S., & Yasui, Y. (2006) · The Journal of Comparative Neurology · doi:10.1002/cne.20919 · Cited by 150 · see citing works
Differential modulation of lateral septal vasopressin receptor blockade in spatial learning, social recognition, and anxiety-related behaviors in rats
Everts, H. G. J., & Koolhaas, J. M. (1999) · Behavioural Brain Research · doi:10.1016/s0166-4328(98)00004-7 · Cited by 148 · see citing works
Sex differences in the regulation of social and anxiety-related behaviors: insights from vasopressin and oxytocin brain systems
Bredewold, R., & Veenema, A. H. (2018) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2018.02.011 · Cited by 144 · see citing works
Age and sex differences in oxytocin and vasopressin V1a receptor binding densities in the rat brain: focus on the social decision-making network
Smith, 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
Differences in intermale aggression are accompanied by opposite vasopressin release patterns within the septum in rats bred for low and high anxiety
Beiderbeck, D. I., Neumann, I. D., & Veenema, A. H. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05974.x · Cited by 142 · see citing works
The Central Vasopressinergic System: Examining the Opportunities for Psychiatric Drug Development
Ring, R. H. (2005) · Current Pharmaceutical Design · doi:10.2174/1381612053382241 · Cited by 141 · see citing works
Species differences in vasopressin receptor binding are evident early in development: Comparative anatomic studies in prairie and montane voles
Wang, Z., Young, L. J., Liu, Y., & Insel, T. R. (1997) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19970224)378:4 · Cited by 135 · see citing works
Dissociating the anti-fear effects of septal and amygdaloid lesions using two pharmacologically validated models of rat anxiety.
Treit, D., Pesold, C., & Rotzinger, S. (1993) · Behavioral Neuroscience · doi:10.1037//0735-7044.107.5.770 · Cited by 137 · see citing works
Longitudinal axis of the hippocampus: Both septal and temporal poles of the hippocampus support water maze spatial learning depending on the training protocol
de Hoz, L., Knox, J., & Morris, R. (2003) · Hippocampus · doi:10.1002/hipo.10079 · Cited by 135 · see citing works
Vasopressin innervation of the mouse ( Mus musculus ) 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
Oxytocin and vasopressin in rodent behaviors related to social dysfunctions in autism spectrum disorders
Lukas, M., & Neumann, I. D. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.08.011 · Cited by 136 · see citing works
Vasopressin regulates social recognition in juvenile and adult rats of both sexes, but in sex- and age-specific ways
Veenema, A. H., Bredewold, R., & De Vries, G. J. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.10.002 · Cited by 129 · see citing works
A single social defeat experience selectively stimulates the release of oxytocin, but not vasopressin, within the septal brain area of male rats
Ebner, K., Wotjak, C. T., Landgraf, R., & Engelmann, M. (2000) · Brain Research · doi:10.1016/s0006-8993(00)02464-1 · Cited by 129 · see citing works
Sex differences in hormonal responses of vasopressin pathways in the rat brain
De Vries, G. J., & Al‐Shamma, H. A. (1990) · Journal of Neurobiology · doi:10.1002/neu.480210503 · Cited by 129 · see citing works
Vasopressin and oxytocin systems in the brain and upper spinal cord of Macaca fascicularis
Caffé, A. R., Van Ryen, P. C., Van Der Woude, T. P., & Van Leeuwen, F. W. (1989) · Journal of Comparative Neurology · doi:10.1002/cne.902870304 · Cited by 128 · see citing works
The human basal forebrain. Part II
Heimer, L., de Olmos, J. S., Alheid, G. F., Pearson, J., Sakamoto, N., Shinoda, K., Marksteiner, J., & Switzer, R. C. (1999) · Handbook of Chemical Neuroanatomy · doi:10.1016/s0924-8196(99)80024-4 · Cited by 125 · see citing works
Early life stress impairs social recognition due to a blunted response of vasopressin release within the septum of adult male rats
Lukas, M., Bredewold, R., Landgraf, R., Neumann, I. D., & Veenema, A. H. (2011) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2010.11.007 · Cited by 122 · see citing works
Sexual differentiation of vasopressin projections of the bed nucleus of the stria terminals and medial amygdaloid nucleus in rats.
Wang, Z., Bullock, N. A., & De Vries, G. J. (1993) · Endocrinology · doi:10.1210/endo.132.6.8504734 · Cited by 123 · see citing works
Site of origin of and sex differences in the vasopressin innervation of the mouse ( Mus musculus ) brain
Rood, B. D., Stott, R. T., You, S., Smith, C. J. W., Woodbury, M. E., & De Vries, G. J. (2013) · Journal of Comparative Neurology · doi:10.1002/cne.23288 · Cited by 120 · see citing works
Vasopressin- and oxytocin-induced activity in the central nervous system: electrophysiological studies using in-vitro systems
Raggenbass, M. (2001) · Progress in Neurobiology · doi:10.1016/s0301-0082(00)00064-2 · Cited by 120 · see citing works
Oxytocin and Vasopressin: Genetics and Behavioral Implications
Caldwell, H. K., & Young, W. S. (2006) · Springer eBooks · doi:10.1007/0-387-30395-2_25 · Cited by 113 · see citing works
Oxytocin and vasopressin: genetics and behavioral implications
Caldwell, H. K., & Young, W. S. (2006) · Handbook of Neurochemistry and Molecular Neurobiology · doi:10.1007/978-0-387-30381-9_25 · Cited by 113 · see citing works
Evidence that the lateral septum is involved in the antidepressant-like effects of the vasopressin V1b receptor antagonist, SSR149415
Stemmelin, J., Lukovic, L., Salome, N., & Griebel, G. (2005) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300562 · Cited by 112 · see citing works
Vasopressin, oxytocin, and social odor recognition
Wacker, D. W., & Ludwig, M. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.08.014 · Cited by 112 · see citing works
Oxytocin in learning and addiction: From early discoveries to the present
Sarnyai, Z., & Kovács, G. L. (2013) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2013.11.019 · Cited by 106 · see citing works
Neural Substrates of Psychostimulant Withdrawal-Induced Anhedonia
D’Souza, M. S., & Markou, A. (2009) · Current topics in behavioral neurosciences · doi:10.1007/7854_2009_20 · Cited by 107 · see citing works
Modulation of Hippocampal Long-Term Potentiation by the Amygdala: A Synaptic Mechanism Linking Emotion and Memory
Abe, K. (2001) · The Japanese Journal of Pharmacology · doi:10.1254/jjp.86.18 · Cited by 106 · see citing works
Top-down regulation of motivated behaviors via lateral septum sub-circuits
Besnard, A., & Leroy, F. (2022) · Molecular Psychiatry · doi:10.1038/s41380-022-01599-3 · Cited by 108 · see citing works
Isoflurane exposure in newborn rats induces long-term cognitive dysfunction in males but not females
Lee, B. H., Chan, J. T., Kraeva, E., Peterson, K., & Sall, J. W. (2014) · Neuropharmacology · doi:10.1016/j.neuropharm.2014.03.011 · Cited by 105 · see citing works
Forced swimming triggers vasopressin release within the amygdala to modulate stress‐coping strategies in rats
Ebner, K., Wotjak, C. T., Landgraf, R., & Engelmann, M. (2002) · European Journal of Neuroscience · doi:10.1046/j.0953-816x.2001.01869.x · Cited by 104 · see citing works
Overview of cellular electrophysiological actions of vasopressin
Raggenbass, M. (2008) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2007.11.074 · Cited by 102 · see citing works
Stress Responsiveness of the Hypothalamic–Pituitary–Adrenal Axis: Age-Related Features of the Vasopressinergic Regulation
Goncharova, N. D. (2013) · Frontiers in Endocrinology · doi:10.3389/fendo.2013.00026 · Cited by 99 · see citing works
Coping with stress in rats and mice: Differential peptidergic modulation of the amygdala-lateral septum complex
Koolhaas, J. M., Everts, H., de Ruiter, A. J. H., de Boer, S. F., & Bohus, B. (1999) · Progress in Brain Research · doi:10.1016/s0079-6123(08)61586-1 · Cited by 100 · see citing works
Synaptic innervation to rat hippocampus by vasopressin-immuno-positive fibres from the hypothalamic supraoptic and paraventricular nuclei
Zhang, L., & Hernández, V. S. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2012.10.010 · Cited by 96 · see citing works
Behavioural impact of intraseptally released vasopressin and oxytocin in rats
Englemann, M., Wotjak, C. T., Ebner, K., & Landgraf, R. (2000) · Experimental Physiology · doi:10.1111/j.1469-445x.2000.tb00015.x · Cited by 94 · see citing works
Sexual dimorphism in the vasotocin system of the bullfrog (Rana catesbeiana)
Boyd, S. K., Tyler, C. J., & Vries, G. J. D. (1992) · The Journal of Comparative Neurology · doi:10.1002/cne.903250213 · Cited by 93 · see citing works
Variation in maternal and anxiety-like behavior associated with discrete patterns of oxytocin and vasopressin 1a receptor density in the lateral septum
Curley, J. P., Jensen, C. L., Franks, B., & Champagne, F. A. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2012.01.013 · Cited by 90 · see citing works
Amygdalar Lesions Block Discriminative Avoidance Learning and Cingulothalamic Training-Induced Neuronal Plasticity in Rabbits
Poremba, A., & Gabriel, M. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-13-05237.1997 · Cited by 92 · see citing works
Effects of chronic social defeat on behavioral and neural correlates of sociality: Vasopressin, oxytocin and the vasopressinergic V1b receptor
Litvin, Y., Murakami, G., & Pfaff, D. W. (2011) · Physiology & Behavior · doi:10.1016/j.physbeh.2011.03.007 · Cited by 90 · see citing works
Differential roles of amygdaloid nuclei in the anxiolytic- and antidepressant-like effects of the V1b receptor antagonist, SSR149415, in rats
Salomé, N., Stemmelin, J., Cohen, C., & Griebel, G. (2006) · Psychopharmacology · doi:10.1007/s00213-006-0424-1 · Cited by 89 · see citing works
Multiple telencephalic and extratelencephalic embryonic domains contribute neurons to the medial extended amygdala
Bupesh, M., Legáz, I., Abellán, A., & Medina, L. M. (2010) · The Journal of Comparative Neurology · doi:10.1002/cne.22581 · Cited by 89 · 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
First exposure to an alive conspecific activates septal and amygdaloid nuclei in visually-naïve domestic chicks (Gallus gallus)
Mayer, U., Salva, O. R., & Vallortígara, G. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2016.09.031 · Cited by 80 · see citing works
Anatomic heterogeneity of the rat amygdaloid complex.
Pitkänen, A., Jolkkonen, E., & Kemppainen, S. (2000) · PubMed · Cited by 85 · see citing works
Neuromodulation by oxytocin and vasopressin in the central nervous system as a basis for their rapid behavioral effects
Stoop, R. (2014) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2014.09.012 · Cited by 84 · see citing works
BDNF restricted knockout mice as an animal model for aggression
Ito, W., Chehab, M., Thakur, S., Li, J., & Morozov, A. (2011) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2010.00676.x · Cited by 87 · see citing works
Non-Peptide Vasopressin V1b Receptor Antagonists as Potential Drugs for the Treatment of Stress-Related Disorders
Griebel, G., Stemmelin, J., Gal, C. S., & Soubrié, P. (2005) · Current Pharmaceutical Design · doi:10.2174/1381612053764797 · Cited by 84 · see citing works
The Vasopressin V1bReceptor Antagonist SSR149415 in the Treatment of Major Depressive and Generalized Anxiety Disorders: Results From 4 Randomized, Double-Blind, Placebo-Controlled Studies
Griebel, G., Beeské, S., & Stahl, S. M. (2012) · The Journal of Clinical Psychiatry · doi:10.4088/jcp.12m07804 · Cited by 81 · see citing works
Histoautoradiographic detection of oxytocin‐ and vasopressin‐binding sites in the telencephalon of the rat
Krémarik, P., Freund‐Mercier, M. J., & Stoeckel, M. E. (1993) · The Journal of Comparative Neurology · doi:10.1002/cne.903330304 · Cited by 80 · see citing works
Lateral septal vasopressin in rats: role in social and object recognition?
Everts, H. G. J., & Koolhaas, J. M. (1997) · Brain Research · doi:10.1016/s0006-8993(97)00269-2 · Cited by 98 · see citing works
Differential Modulation of Changes in Hippocampal–Septal Synaptic Excitability by the Amygdala as a Function of Either Elemental or Contextual Fear Conditioning in Mice
Desmedt, A., Garcia, R., & Jaffard, R. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-01-00480.1998 · Cited by 77 · 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
Neuromodulation of memory in the hippocampus by vasopressin
Alescio‐Lautier, B., Paban, V., & Soumireu-Mourat, B. (2000) · European Journal of Pharmacology · doi:10.1016/s0014-2999(00)00542-2 · Cited by 76 · see citing works
Vasopressin in the forebrain of common marmosets (Callithrix jacchus): studies with in situ hybridization, immunocytochemistry and receptor autoradiography
Wang, Z., Toloczko, D., Young, L. J., Moody, K., Newman, J. D., & Insel, T. R. (1997) · Brain Research · doi:10.1016/s0006-8993(97)00636-7 · Cited by 75 · see citing works
Role of Vasopressin in Aggressive and Dominant/Subordinate Behaviors
Ferris, C. F. (1992) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1992.tb34357.x · Cited by 75 · see citing works
Differential roles of the dorsal and ventral hippocampus in predator odor contextual fear conditioning
Wang, M. E., Fraize, N., Yin, L. X., Yuan, R. K., Petsagourakis, D., Wann, E. G., & Muzzio, I. A. (2013) · Hippocampus · doi:10.1002/hipo.22105 · Cited by 68 · see citing works
Pattern of afferents to the lateral septum in the guinea pig
Staiger, J. F., & N�rnberger, F. (1989) · Cell and Tissue Research · doi:10.1007/bf00221457 · Cited by 67 · see citing works
Neuropeptide diversity and the regulation of social behavior in New World primates
French, J. A., Taylor, J. H., Mustoe, A. C., & Cavanaugh, J. (2016) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2016.03.004 · Cited by 66 · see citing works
Changes in the Arginine‐Vasopressin Immunoreactive Systems in Male Mice Lacking a Functional Aromatase Gene
Plumari, L., Viglietti‐Panzica, C., Allieri, F., Honda, S., Harada, N., Absil, P., Balthazart, J., & Panzica, G. C. (2002) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2002.00866.x · Cited by 66 · see citing works
Interaction of Stress, Corticotropin-Releasing Factor, Arginine Vasopressin and Behaviour
Beurel, E., & Nemeroff, C. B. (2014) · Current Topics in Behavioral Neurosciences · doi:10.1007/7854_2014_306 · Cited by 64 · see citing works
Neural systems that facilitate the representation of social rank
Dwortz, M. F., Curley, J. P., Tye, K. M., & Padilla-Coreano, N. (2022) · Philosophical Transactions of the Royal Society B · doi:10.1098/rstb.2020.0444 · Cited by 64 · see citing works
Modulation of social behavior by distinct vasopressin sources
Rigney, N., Vries, G. J. D., & Petrulis, A. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1127792 · Cited by 61 · see citing works
Psychiatric Comorbidities in Temporal Lobe Epilepsy: Possible Relationships between Psychotic Disorders and Involvement of Limbic Circuits
Kandratavicius, L., Lopes‐Aguiar, C., Bueno-Júnior, L. S., Romcy-Pereira, R. N., Hallak, J. E. C., & Leite, J. P. (2012) · Brazilian Journal of Psychiatry · doi:10.1016/j.rbp.2012.04.007 · Cited by 58 · see citing works
Comparing vasopressin and oxytocin fiber and receptor density patterns in the social behavior neural network: implications for cross-system signaling
Smith, C. J. W., DiBenedictis, B. T., & Veenema, A. H. (2019) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2019.02.001 · Cited by 59 · see citing works
Vasopressin innervation of sexually dimorphic structures of the gerbil forebrain under various hormonal conditions
Crenshaw, B. J., Vries, G. J. D., & Yahr, P. (1992) · The Journal of Comparative Neurology · doi:10.1002/cne.903220412 · Cited by 59 · see citing works

Immunocytochemical demonstration of vasopressin and oxytocin in the rat brain by light and electron microscopy.
Buijs, R. M. (1980) · Journal of Histochemistry & Cytochemistry · doi:10.1177/28.4.6989899 · Cited by 81 · see citing works
Efferent projections from the lateral septal nucleus to the anterior hypothalamus in the rat: A study combining Phaseolus vulgaris-leucoagglutinin tracing with vasopressin immunocytochemistry
Staiger, J. F., & Wouterlood, F. G. (1990) · Cell and Tissue Research · doi:10.1007/bf00329434 · Cited by 50 · see citing works
Extrahypothalamic vasopressin and oxytocin in the human brain; presence of vasopressin cells in the bed nucleus of the stria terminalis
Fliers, E., Guldenaar, S. E. F., Wal, N. V. D., & Swaab, D. F. (1986) · Brain Research · doi:10.1016/0006-8993(86)90759-6 · Cited by 114 · see citing works
Vasopressin-immunoreactive cells in the dorsomedial hypothalamic region, medial amygdaloid nucleus and locus coeruleus of the rat
Caffe´, A. R., & van Leeuwen, F. W. (1983) · Cell and Tissue Research · doi:10.1007/bf00222229 · Cited by 199 · see citing works
The origin of the vasopressinergic and oxytocinergic innervation of the rat brain with special reference to the lateral septum
de Vries, G. J., & Buijs, R. M. (1983) · Brain Research · doi:10.1016/0006-8993(83)90855-7 · Cited by 524 · see citing works

Authors: Caffé, A. R., van Leeuwen, F. W., & Luiten, P. G. M.
Affiliations: University of Groningen (NL)
Venue: Journal of Comparative Neurology
Publisher: Wiley
Published: 1987-07-08
Volume: 261
Issue: 2
Pages: 237-252
ISSN: 0021-9967 (ISSN-L)
1096-9861
DOI: 10.1002/cne.902610206
OpenAlex: W2162632863
Cited by: 286
References: 40
Citations by year: 2025: 2 · 2024: 1 · 2023: 3 · 2022: 6 · 2021: 8 · 2020: 3 · 2019: 5 · 2018: 9 · 2017: 2 · 2016: 6 · 2015: 5 · 2014: 11 · 2013: 10 · 2012: 12
FWCI: 15.51
Type: journal article
Language: en
Open access: closed
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor, 6303 d)
Locations: The Journal of Comparative Neurology (publishedVersion)
PubMed (publishedVersion)
University of Groningen research database (University of Groningen / Centre for Information Technology) (publishedVersion)
University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion)
Funders: National Institutes of Health (5r01am016166-12)
Topics: Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Keywords: vasopressin, medial amygdala, lateral septum, ventral hippocampus, bed nucleus of the stria terminalis, anterograde tracing, retrograde tracing, sexual behavior
MeSH terms: Amygdala, Animals, Fluorescent Antibody Technique, Hippocampus, Immunoenzyme Techniques, Male, Neural Pathways, Rats, Inbred Strains, Septum Pellucidum, Vasopressins, 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

Vasopressin cells in the medial amygdala of the rat project to the lateral septum and ventral hippocampus

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Cites

Cited by

Related

Record

About these checks