Abstract
Magnocellular neurosecretory cells (MNCs) clustered in the hypothalamic paraventricular nucleus (PVN) and supraoptic nucleus constitute a major source of oxytocin (OXT) and arginine vasopressin (AVP) peptides, and are among the best described peptidergic neurons in the brain. OXT and AVP are involved in a range of homeostatic processes, social behaviours, emotional processes, and learning. Notably, their actions can be sex-specific, and several sex differences in the anatomies of the OXT and AVP systems have been reported. Nonetheless, possible sex differences in the detailed distributions of MNCs and in their intrinsic electrical properties ex vivo have not been extensively examined. We addressed these issues utilizing immunostaining and patch-clamp ex vivo recordings. Here, we showed that Sprague-Dawley rat PVN AVP neurons are more numerous than OXT cells and that more neurons of both types are present in males. Furthermore, we identified several previously unreported differences between putative OXT and AVP MNC electrophysiology contributing to their partially unique profiles. Notably, elucidation of the highly specific action potential (AP) shapes, with AVP MNCs having a narrower AP and faster hyperpolarizing after-potential (HAP) kinetics than OXT MNCs, allowed unambiguous discrimination between OXT and AVP MNCs ex vivo for the first time. Moreover, the examined electrophysiological properties of male and female MNCs generally overlapped with the following exceptions: higher membrane resistance in male MNCs and HAP kinetics in putative OXT MNCs, which was slower in males. These reported observations constitute a thorough addition to the knowledge of MNC properties shaping their diverse physiological actions in both sexes.
Similar content being viewed by others
References
Abi-Gerges N, Small BG, Lawrence CL et al (2004) Evidence for gender differences in electrophysiological properties of canine Purkinje fibres. Br J Pharmacol 142:1255–1264. https://doi.org/10.1038/sj.bjp.0705880
Armstrong WE (1995) Morphological and electrophysiological classification of hypothalamic supraoptic neurons. Prog Neurobiol 47:291–339. https://doi.org/10.1016/0301-0082(95)80005-S
Armstrong WE (2015) Chapter 14. Hypothalamic supraoptic and paraventricular nuclei. In: Paxinos G (ed) The rat nervous system, 4th edn. Academic Press, Cambridge, pp 295–314
Armstrong WE, Tasker JG (eds) (2014) Neurophysiology of neuroendocrine neurons. Wiley, Chichester
Armstrong WE, Smith BN, Tian M (1994) Electrophysiological characteristics of immunochemically identified rat oxytocin and vasopressin neurones in vitro. J Physiol 475:115–128. https://doi.org/10.1113/jphysiol.1994.sp020053
Armstrong WE, Foehring RC, Kirchner MK, Sladek CD (2019) Electrophysiological properties of identified oxytocin and vasopressin neurones. J Neuroendocrinol. https://doi.org/10.1111/jne.12666
Aydın O, Lysaker PH, Balıkçı K et al (2018) Associations of oxytocin and vasopressin plasma levels with neurocognitive, social cognitive and meta cognitive function in schizophrenia. Psychiatry Res 270:1010–1016. https://doi.org/10.1016/j.psychres.2018.03.048
Bangasser DA, Wicks B (2017) Sex-specific mechanisms for responding to stress. J Neurosci Res 95:75–82. https://doi.org/10.1002/jnr.23812
Baribeau DA, Anagnostou E (2015) Oxytocin and vasopressin: linking pituitary neuropeptides and their receptors to social neurocircuits. Front Neurosci 9:335. https://doi.org/10.3389/fnins.2015.00335
Barna J, Dimén D, Puska G et al (2019) Complement component 1q subcomponent binding protein in the brain of the rat. Sci Rep 9:4597. https://doi.org/10.1038/s41598-019-40788-z
Bean BP (2007) The action potential in mammalian central neurons. Nat Rev Neurosci 8:451–465. https://doi.org/10.1038/nrn2148
Beery AK, Zucker I (2011) Sex bias in neuroscience and biomedical research. Neurosci Biobehav Rev 35:565–572. https://doi.org/10.1016/j.neubiorev.2010.07.002
Bendesky A, Kwon Y-M, Lassance J-M et al (2017) The genetic basis of parental care evolution in monogamous mice. Nature 544:434–439. https://doi.org/10.1038/nature22074
Bosch OJ, Neumann ID (2012) Both oxytocin and vasopressin are mediators of maternal care and aggression in rodents: from central release to sites of action. Horm Behav 61:293–303. https://doi.org/10.1016/j.yhbeh.2011.11.002
Boudaba C, Szabó K, Tasker JG (1996) Physiological mapping of local inhibitory inputs to the hypothalamic paraventricular nucleus. J Neurosci 16:7151–7160. https://doi.org/10.1523/JNEUROSCI.16-22-07151.1996
Bourque CW (1988) Transient calcium-dependent potassium current in magnocellular neurosecretory cells of the rat supraoptic nucleus. J Physiol 397:331–347. https://doi.org/10.1113/jphysiol.1988.sp017004
Bourque CW, Randle JC, Renaud LP (1985) Calcium-dependent potassium conductance in rat supraoptic nucleus neurosecretory neurons. J Neurophysiol 54:1375–1382. https://doi.org/10.1152/jn.1985.54.6.1375
Bredewold R, Veenema AH (2018) Sex differences in the regulation of social and anxiety-related behaviors: insights from vasopressin and oxytocin brain systems. Curr Opin Neurobiol 49:132–140. https://doi.org/10.1016/j.conb.2018.02.011
Brown CH, Bains JS, Ludwig M, Stern JE (2013) Physiological regulation of magnocellular neurosecretory cell activity: integration of intrinsic, local and afferent mechanisms. J Neuroendocrinol 25:678–710. https://doi.org/10.1111/jne.12051
Caldwell HK (2017) Oxytocin and vasopressin: powerful regulators of social behavior. Neuroscientist 23:517–528. https://doi.org/10.1177/1073858417708284
Cao J, Willett JA, Dorris DM, Meitzen J (2018) Sex differences in medium spiny neuron excitability and glutamatergic synaptic input: heterogeneity across striatal regions and evidence for estradiol-dependent sexual differentiation. Front Endocrinol (Lausanne) 9:173. https://doi.org/10.3389/fendo.2018.00173
Choe KY, Trudel E, Bourque CW (2016) Effects of salt loading on the regulation of rat hypothalamic magnocellular neurosecretory cells by ionotropic GABA and glycine receptors. J Neuroendocrinol. https://doi.org/10.1111/jne.12372
Cobbett P, Legendre P, Mason WT (1989) Characterization of three types of potassium current in cultured neurones of rat supraoptic nucleus area. J Physiol 410:443–462. https://doi.org/10.1113/jphysiol.1989.sp017543
da Silva MP, Merino RM, Mecawi AS et al (2015) In vitro differentiation between oxytocin- and vasopressin-secreting magnocellular neurons requires more than one experimental criterion. Mol Cell Endocrinol 400:102–111. https://doi.org/10.1016/j.mce.2014.11.004
de Vries GJ (2008) Sex differences in vasopressin and oxytocin innervation of the brain. Prog Brain Res 170:17–27. https://doi.org/10.1016/S0079-6123(08)00402-0
De Vries GJ, Panzica GC (2006) Sexual differentiation of central vasopressin and vasotocin systems in vertebrates: different mechanisms, similar endpoints. Neuroscience 138:947–955. https://doi.org/10.1016/j.neuroscience.2005.07.050
Dopico AM, Widmer H, Wang G et al (1999) Rat supraoptic magnocellular neurones show distinct large conductance, Ca2+-activated K+ channel subtypes in cell bodies versus nerve endings. J Physiol 519(Pt 1):101–114. https://doi.org/10.1111/j.1469-7793.1999.0101o.x
Dumais KM, Veenema AH (2016) Vasopressin and oxytocin receptor systems in the brain: sex differences and sex-specific regulation of social behavior. Front Neuroendocrinol 40:1–23. https://doi.org/10.1016/j.yfrne.2015.04.003
Eliava M, Melchior M, Knobloch-Bollmann HS et al (2016) A new population of parvocellular oxytocin neurons controlling magnocellular neuron activity and inflammatory pain processing. Neuron 89:1291–1304. https://doi.org/10.1016/j.neuron.2016.01.041
Erickson KR, Ronnekleiv OK, Kelly MJ (1990) Inward rectification (I) in immunocytochemically-ldentified vasopressin and oxytocin neurons of guinea-pig supraoptic nucleus. J Neuroendocrinol 2:261–265. https://doi.org/10.1111/j.1365-2826.1990.tb00402.x
Erickson KR, Ronnekleiv OK, Kelly MJ (1993) Electrophysiology of guinea-pig supraoptic neurones: role of a hyperpolarization-activated cation current in phasic firing. J Physiol 460:407–425. https://doi.org/10.1113/jphysiol.1993.sp019478
Fisher TE, Voisin DL, Bourque CW (1998) Density of transient K+ current influences excitability in acutely isolated vasopressin and oxytocin neurones of rat hypothalamus. J Physiol 511(Pt 2):423–432. https://doi.org/10.1111/j.1469-7793.1998.423bh.x
Haam J, Popescu IR, Morton LA et al (2012) GABA is excitatory in adult vasopressinergic neuroendocrine cells. J Neurosci 32:572–582. https://doi.org/10.1523/JNEUROSCI.3826-11.2012
Hatton GI, Wang Y-F (2008) Neural mechanisms underlying the milk ejection burst and reflex. Prog Brain Res 170:155–166. https://doi.org/10.1016/S0079-6123(08)00414-7
Hazell GGJ, Hindmarch CC, Pope GR et al (2012) G protein-coupled receptors in the hypothalamic paraventricular and supraoptic nuclei–serpentine gateways to neuroendocrine homeostasis. Front Neuroendocrinol 33:45–66. https://doi.org/10.1016/j.yfrne.2011.07.002
Hernández VS, Vázquez-Juárez E, Márquez MM et al (2015) Extra-neurohypophyseal axonal projections from individual vasopressin-containing magnocellular neurons in rat hypothalamus. Front Neuroanat 9:130. https://doi.org/10.3389/fnana.2015.00130
Hirasawa M, Mouginot D, Kozoriz MG et al (2003) Vasopressin differentially modulates non-NMDA receptors in vasopressin and oxytocin neurons in the supraoptic nucleus. J Neurosci 23:4270–4277. https://doi.org/10.1523/JNEUROSCI.23-10-04270.2003
Hlubek MD, Cobbett P (1997) Outward potassium currents of supraoptic magnocellular neurosecretory cells isolated from the adult guinea-pig. J Physiol 502(Pt 1):61–74. https://doi.org/10.1111/j.1469-7793.1997.061bl.x
Hlubek MD, Cobbett P (2000) Differential effects of K(+) channel blockers on frequency-dependent action potential broadening in supraoptic neurons. Brain Res Bull 53:203–209. https://doi.org/10.1016/S0361-9230(00)00335-X
Hoffman NW, Tasker JG, Dudek FE (1991) Immunohistochemical differentiation of electrophysiologically defined neuronal populations in the region of the rat hypothalamic paraventricular nucleus. J Comp Neurol 307:405–416. https://doi.org/10.1002/cne.903070306
Horn JP, Swanson LW (2013) Chapter 47: the autonomic motor system and the hypothalamus. In: Kandel EK, Schwartz JH, Jessell TM et al (eds) Principles of neural science, 5th edn. McGraw-Hill Medical, New York, pp 1056–1078
Hou-Yu A, Lamme AT, Zimmerman EA, Silverman AJ (1986) Comparative distribution of vasopressin and oxytocin neurons in the rat brain using a double-label procedure. Neuroendocrinology 44:235–246. https://doi.org/10.1159/000124651
Ishunina TA, Swaab DF (1999) Vasopressin and oxytocin neurons of the human supraoptic and paraventricular nucleus: size changes in relation to age and sex. J Clin Endocrinol Metab 84:4637–4644. https://doi.org/10.1210/jcem.84.12.6187
Jobst A, Dehning S, Ruf S et al (2014) Oxytocin and vasopressin levels are decreased in the plasma of male schizophrenia patients. Acta Neuropsychiatr 26:347–355. https://doi.org/10.1017/neu.2014.20
Jourdain P, Poulain DA, Theodosis DT, Israel JM (1996) Electrical properties of oxytocin neurons in organotypic cultures from postnatal rat hypothalamus. J Neurophysiol 76:2772–2785. https://doi.org/10.1152/jn.1996.76.4.2772
Jurek B, Neumann ID (2018) The oxytocin receptor: from intracellular signaling to behavior. Physiol Rev 98:1805–1908. https://doi.org/10.1152/physrev.00031.2017
Kania A, Gugula A, Grabowiecka A et al (2017) Inhibition of oxytocin and vasopressin neuron activity in rat hypothalamic paraventricular nucleus by relaxin-3-RXFP3 signalling. J Physiol 595:3425–3447. https://doi.org/10.1113/JP273787
Karim MA, Sloper JC (1980) Histogenesis of the supraoptic and paraventricular neurosecretory cells of the mouse hypothalamus. J Anat 130:341–347
Kastman HE, Blasiak A, Walker L et al (2016) Nucleus incertus Orexin2 receptors mediate alcohol seeking in rats. Neuropharmacology 110:82–91. https://doi.org/10.1016/j.neuropharm.2016.07.006
Kawata M, Sano Y (1982) Immunohistochemical identification of the oxytocin and vasopressin neurons in the hypothalamus of the monkey (Macaca fuscata). Anat Embryol (Berl) 165:151–167. https://doi.org/10.1007/BF00305474
Knigge KM, Joseph SA (1982) Relationship of the central ACTH-immunoreactive opiocortin system to the supraoptic and paraventricular nuclei of the hypothalamus of the rat. Brain Res 239:655–658. https://doi.org/10.1016/0006-8993(82)90545-5
Knobloch HS, Grinevich V (2014) Evolution of oxytocin pathways in the brain of vertebrates. Front Behav Neurosci 8:31. https://doi.org/10.3389/fnbeh.2014.00031
Knobloch HS, Charlet A, Hoffmann LC et al (2012) Evoked axonal oxytocin release in the central amygdala attenuates fear response. Neuron 73:553–566. https://doi.org/10.1016/j.neuron.2011.11.030
Komendantov AO, Trayanova NA, Tasker JG (2007) Somato-dendritic mechanisms underlying the electrophysiological properties of hypothalamic magnocellular neuroendocrine cells: a multicompartmental model study. J Comput Neurosci 23:143–168. https://doi.org/10.1007/s10827-007-0024-z
Koshimizu T, Nakamura K, Egashira N et al (2012) Vasopressin V1a and V1b receptors: from molecules to physiological systems. Physiol Rev 92:1813–1864. https://doi.org/10.1152/physrev.00035.2011
Kramer KM, Cushing BS, Carter CS et al (2004) Sex and species differences in plasma oxytocin using an enzyme immunoassay. Can J Zool 82:1194–1200. https://doi.org/10.1139/z04-098
Lazcano MA, Bentura ML, Toledano A (1990) Morphometric study on the development of magnocellular neurons of the supraoptic nucleus utilising immunohistochemical methods. J Anat 168:1–11
Leng G, Pineda R, Sabatier N, Ludwig M (2015) 60 years of neuroendocrinology: the posterior pituitary, from Geoffrey Harris to our present understanding. J Endocrinol 226:T173–T185. https://doi.org/10.1530/JOE-15-0087
Li Z, Ferguson AV (1996) Electrophysiological properties of paraventricular magnocellular neurons in rat brain slices: modulation of IA by angiotensin II. Neuroscience 71:133–145. https://doi.org/10.1016/0306-4522(95)00434-3
Li C, Tripathi PK, Armstrong WE (2007) Differences in spike train variability in rat vasopressin and oxytocin neurons and their relationship to synaptic activity. J Physiol 581:221–240. https://doi.org/10.1113/jphysiol.2006.123810
LoParo D, Waldman ID (2015) The oxytocin receptor gene (OXTR) is associated with autism spectrum disorder: a meta-analysis. Mol Psychiatry 20:640–646. https://doi.org/10.1038/mp.2014.77
Ludwig M, Leng G (2006) Dendritic peptide release and peptide-dependent behaviours. Nat Rev Neurosci 7:126–136. https://doi.org/10.1038/nrn1845
Ludwig M, Sabatier N, Bull PM et al (2002) Intracellular calcium stores regulate activity-dependent neuropeptide release from dendrites. Nature 418:85–89. https://doi.org/10.1038/nature00822
Luther JA, Tasker JG (2000) Voltage-gated currents distinguish parvocellular from magnocellular neurones in the rat hypothalamic paraventricular nucleus. J Physiol 523(Pt 1):193–209. https://doi.org/10.1111/j.1469-7793.2000.t01-1-00193.x
Massey SH, Backes KA, Schuette SA (2016) Plasma oxytocin concentration and depressive symptoms: a review of current evidence and directions for future research. Depress Anxiety 33:316–322. https://doi.org/10.1002/da.22467
McCutcheon JE, Marinelli M (2009) Age matters. Eur J Neurosci 29:997–1014. https://doi.org/10.1111/j.1460-9568.2009.06648.x
Meyer-Lindenberg A, Domes G, Kirsch P, Heinrichs M (2011) Oxytocin and vasopressin in the human brain: social neuropeptides for translational medicine. Nat Rev Neurosci 12:524–538. https://doi.org/10.1038/nrn3044
Morton LA, Popescu IR, Haam J, Tasker JG (2014) Short-term potentiation of GABAergic synaptic inputs to vasopressin and oxytocin neurones. J Physiol 592:4221–4233. https://doi.org/10.1113/jphysiol.2014.277293
Nephew BC (2012) Behavioral roles of oxytocin and vasopressin. In: Sumiyoshi T (ed) Neuroendocrinology and behavior. InTech, London, pp 49–82
Ohno A, Ohya S, Yamamura H, Imaizumi Y (2009) Gender difference in BK channel expression in amygdala complex of rat brain. Biochem Biophys Res Commun 378:867–871. https://doi.org/10.1016/j.bbrc.2008.12.004
Oliet SH, Bourque CW (1992) Properties of supraoptic magnocellular neurones isolated from the adult rat. J Physiol 455:291–306. https://doi.org/10.1113/jphysiol.1992.sp019302
Paxinos G, Watson C (2007) The rat brain in stereotaxic coordinates, 6th edn. Academic Press, San Diego
Piekut DT (2003) Relationship of ACTH1-39-immunostained fibers and magnocellular neurons in the paraventricular nucleus of rat hypothalamus. Peptides 6:883–890. https://doi.org/10.1016/0196-9781(85)90319-5
Poulain DA, Wakerley JB (1982) Electrophysiology of hypothalamic magnocellular neurones secreting oxytocin and vasopressin. Neuroscience 7:773–808. https://doi.org/10.1016/0306-4522(82)90044-6
Poulain DA, Wakerley JB, Dyball RE (1977) Electrophysiological differentiation of oxytocin- and vasopressin-secreting neurones. Proc R Soc Lond Ser B Biol Sci 196:367–384. https://doi.org/10.1098/rspb.1977.0046
Pranzatelli MR (1994) On the molecular mechanism of adrenocorticotrophic hormone in the CNS: neurotransmitters and receptors. Exp Neurol 125:142–161. https://doi.org/10.1006/exnr.1994.1018
Raggenbass M (2001) Vasopressin- and oxytocin-induced activity in the central nervous system: electrophysiological studies using in vitro systems. Prog Neurobiol 64:307–326. https://doi.org/10.1016/S0301-0082(00)00064-2
R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/
Renaud LP, Bourque CW (1991) Neurophysiology and neuropharmacology of hypothalamic magnocellular neurons secreting vasopressin and oxytocin. Prog Neurobiol 36:131–169. https://doi.org/10.1016/0301-0082(91)90020-2
Rhodes CH, Morrell JI, Pfaff DW (1981) Immunohistochemical analysis of magnocellular elements in rat hypothalamus: distribution and numbers of cells containing neurophysin, oxytocin, and vasopressin. J Comp Neurol 198:45–64. https://doi.org/10.1002/cne.901980106
Roper P, Callaway J, Shevchenko T et al (2003) AHP’s, HAP’s and DAP’s: how potassium currents regulate the excitability of rat supraoptic neurones. J Comput Neurosci 15:367–389. https://doi.org/10.1023/A:1027424128972
Roy RK, Augustine RA, Brown CH, Schwenke DO (2018) Activation of oxytocin neurons in the paraventricular nucleus drives cardiac sympathetic nerve activation following myocardial infarction in rats. Commun Biol 1:160. https://doi.org/10.1038/s42003-018-0169-5
Schimchowitsch S, Moreau C, Laurent F, Stoeckel M-E (1989) Distribution and morphometric characteristics of oxytocin- and vasopressin-immunoreactive neurons in the rabbit hypothalamus. J Comp Neurol 285:304–324. https://doi.org/10.1002/cne.902850303
Scroggs R, Wang L, Teruyama R, Armstrong WE (2013) Variation in sodium current amplitude between vasopressin and oxytocin hypothalamic supraoptic neurons. J Neurophysiol 109:1017–1024. https://doi.org/10.1152/jn.00812.2012
Share L, Crofton JT, Ouchi Y (1988) Vasopressin: sexual dimorphism in secretion, cardiovascular actions and hypertension. Am J Med Sci 295:314–319. https://doi.org/10.1097/00000441-198804000-00017
Shevchenko T, Teruyama R, Armstrong WE (2004) High-threshold, Kv3-like potassium currents in magnocellular neurosecretory neurons and their role in spike repolarization. J Neurophysiol 92:3043–3055. https://doi.org/10.1152/jn.00431.2004
Silverman AJ, Zimmerman EA (1983) Magnocellular neurosecretory system. Annu Rev Neurosci 6:357–380. https://doi.org/10.1146/annurev.ne.06.030183.002041
Steinman MQ, Laredo SA, Lopez EM et al (2015) Hypothalamic vasopressin systems are more sensitive to the long term effects of social defeat in males versus females. Psychoneuroendocrinology 51:122–134. https://doi.org/10.1016/j.psyneuen.2014.09.009
Stern JE, Armstrong WE (1995) Electrophysiological differences between oxytocin and vasopressin neurones recorded from female rats in vitro. J Physiol 488(Pt 3):701–708. https://doi.org/10.1113/jphysiol.1995.sp021001
Stern JE, Armstrong WE (1996) Changes in the electrical properties of supraoptic nucleus oxytocin and vasopressin neurons during lactation. J Neurosci 16:4861–4871. https://doi.org/10.1523/jneurosci.16-16-04861.1996
Stern JE, Armstrong WE (1997) Sustained outward rectification of oxytocinergic neurones in the rat supraoptic nucleus: ionic dependence and pharmacology. J Physiol 500(Pt 2):497–508. https://doi.org/10.1113/jphysiol.1997.sp022036
Stern JE, Galarreta M, Foehring RC et al (1999) Differences in the properties of ionotropic glutamate synaptic currents in oxytocin and vasopressin neuroendocrine neurons. J Neurosci 19:3367–3375. https://doi.org/10.1523/JNEUROSCI.19-09-03367.1999
Stoop R (2012) Neuromodulation by oxytocin and vasopressin. Neuron 76:142–159. https://doi.org/10.1016/j.neuron.2012.09.025
Swaab DF, Pool CW, Nijveldt F (1975) Immunofluorescence of vasopressin and oxytocin in the rat hypothalamo-neurohypophypopseal system. J Neural Transm 36:195–215
Swanson LW, Sawchenko PE (1983) Hypothalamic integration: organization of the paraventricular and supraoptic nuclei. Annu Rev Neurosci 6:269–324. https://doi.org/10.1146/annurev.ne.06.030183.001413
Tasker JG, Dudek FE (1991) Electrophysiological properties of neurones in the region of the paraventricular nucleus in slices of rat hypothalamus. J Physiol 434:271–293. https://doi.org/10.1113/jphysiol.1991.sp018469
Tasker JG, Dudek FE (1993) Local inhibitory synaptic inputs to neurones of the paraventricular nucleus in slices of rat hypothalamus. J Physiol 469:179–192. https://doi.org/10.1113/jphysiol.1993.sp019810
Terranova JI, Song Z, Larkin TE et al (2016) Serotonin and arginine-vasopressin mediate sex differences in the regulation of dominance and aggression by the social brain. Proc Natl Acad Sci USA 113:13233–13238. https://doi.org/10.1073/pnas.1610446113
Teruyama R, Armstrong WE (2002) Changes in the active membrane properties of rat supraoptic neurones during pregnancy and lactation. J Neuroendocrinol 14:933–944. https://doi.org/10.1046/j.1365-2826.2002.00844.x
Teruyama R, Armstrong WE (2005) Enhancement of calcium-dependent afterpotentials in oxytocin neurons of the rat supraoptic nucleus during lactation. J Physiol 566:505–518. https://doi.org/10.1113/jphysiol.2005.085985
Vandesande F, Dierickx K (1975) Identification of the vasopressin producing and of the oxytocin producing neurons in the hypothalamic magnocellular neurosecretroy system of the rat. Cell Tissue Res 164:153–162
Veening JG, de Jong TR, Waldinger MD et al (2015) The role of oxytocin in male and female reproductive behavior. Eur J Pharmacol 753:209–228. https://doi.org/10.1016/j.ejphar.2014.07.045
Wakerley JB, Lincoln DW (1973) The milk-ejection reflex of the rat: a 20- to 40-fold acceleration in the firing of paraventricular neurones during oxytocin release. J Endocrinol 57:477–493
Wang Y-F, Hatton GI (2005) Burst firing of oxytocin neurons in male rat hypothalamic slices. Brain Res 1032:36–43. https://doi.org/10.1016/j.brainres.2004.10.046
Windle RJ, Forsling ML (1993) Variations in oxytocin secretion during the 4-day oestrous cycle of the rat. J Endocrinol 136:305–311. https://doi.org/10.1677/joe.0.1360305
Xu X-J, Shou X-J, Li J et al (2013) Mothers of autistic children: lower plasma levels of oxytocin and Arg-vasopressin and a higher level of testosterone. PLoS One. https://doi.org/10.1371/journal.pone.0074849
Yuen KW, Garner JP, Carson DS et al (2014) Plasma oxytocin concentrations are lower in depressed vs. healthy control women and are independent of cortisol. J Psychiatr Res 51:30–36. https://doi.org/10.1016/j.jpsychires.2013.12.012
Zampronio AR, Kuzmiski JB, Florence CM et al (2010) Opposing actions of endothelin-1 on glutamatergic transmission onto vasopressin and oxytocin neurons in the supraoptic nucleus. J Neurosci 30:16855–16863. https://doi.org/10.1523/JNEUROSCI.5079-10.2010
Zhao Z, Wang L, Gao W et al (2017) A central catecholaminergic circuit controls blood glucose levels during stress. Neuron 95:138–152. https://doi.org/10.1016/j.neuron.2017.05.031
Funding
This study was funded by research grants from the Ministry of Science and Higher Education (MSHE Poland 0020/DIA/2014/43 to A.K.), the National Science Centre (NSC Poland, DEC-2012/05/D/NZ4/02984 to A.B.), and the Institute of Zoology and Biomedical Research of the Jagiellonian University in Krakow (DS/MND/WBiNoZ/IZ/20/2016, K/DSC/003960 and DS/MND/WBiNoZ/IZ/16/2017, K/DSC/004650). A.K. obtained founding from the National Science Centre’s Ph.D. scholarship programme ETIUDA V (NSC Poland, UMO-2017/24/T/NZ4/00225).
Author information
Authors and Affiliations
Contributions
AK and AB conceived the project; AK, AB, PS, AG, AS, ZS, TB, GH, and ZR contributed to the data acquisition and interpretation of the results; AK performed, analysed, and interpreted the ex vivo electrophysiology data; PS and AS performed and analysed the ex vivo electrophysiology data; AK and AG performed the immunostaining and analysed and interpreted the resultant microscopy data; TB created the analysis tools; and AK and AB wrote the article. All authors provided comments and corrections and approved the final version of the manuscript.
Corresponding author
Ethics declarations
Conflicts of interest
The authors have no conflicts of interest to declare.
Human and animal participants right statement
This article does not contain any studies involving human participants that were performed by any of the authors.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Kania, A., Sambak, P., Gugula, A. et al. Electrophysiology and distribution of oxytocin and vasopressin neurons in the hypothalamic paraventricular nucleus: a study in male and female rats. Brain Struct Funct 225, 285–304 (2020). https://doi.org/10.1007/s00429-019-01989-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00429-019-01989-4