Abstract
The magnocellular neuroendocrine cells—located in the supraoptic and the paraventricular nuclei of the hypothalamus—project their axons to the posterior pituitary, where they secrete the neurohormones vasopressin or oxytocin into the systemic circulation. Vasopressin regulates water–salt balance and blood pressure, whereas oxytocin controls key steps in lactation and parturition. These neuroendocrine cells interact with surrounding astrocytes, and this relationship plays an important role in synaptic and circuit plasticity, thereby regulating neuroendocrine output. Noradrenergic and glutamatergic inputs to the magnocellular neurons are essential drivers of neurohormone release, yet there is a surprising reliance on the recruitment of astrocyte-derived ATP in this excitation process. ATP release from these glia scales the strength of excitatory synapses on the magnocellular neurons, effectively increasing their ability to respond to many different afferent glutamate inputs when neurohormone release is needed. This system represents a unique example of how astrocyte–neuron interactions can shape the activity-level of homeostatic neural networks to meet physiological demands.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Similar content being viewed by others
References
Armstrong WE, Gallagher MJ, Sladek CD (1986) Noradrenergic stimulation of supraoptic neuronal activity and vasopressin release in vitro: mediation by an alpha 1-receptor. Brain Res 365(1):192–197. https://doi.org/10.1016/0006-8993(86)90739-0
Arnauld E, Vincent JD, Dreifuss JJ (1974) Firing patterns of hypothalamic supraoptic neurons during water deprivation in monkeys. Science (New York, NY) 185(4150):535–537. https://doi.org/10.1126/science.185.4150.535
Buller KM, Khanna S, Sibbald JR, Day TA (1996) Central noradrenergic neurons signal via ATP to elicit vasopressin responses to haemorrhage. Neuroscience 73(3):637–642. https://doi.org/10.1016/0306-4522(96)00156-x
Cunningham ET, Sawchenko PE (1988) Anatomical specificity of noradrenergic inputs to the paraventricular and supraoptic nuclei of the rat hypothalamus. J Comp Neurol 274(1):60–76. https://doi.org/10.1002/cne.902740107
Daftary SS, Boudaba C, Szabó K, Tasker JG (1998) Noradrenergic excitation of magnocellular neurons in the rat hypothalamic paraventricular nucleus via intranuclear glutamatergic circuits. J Neurosci 18(24):10619–10628
Day TA, Ferguson AV, Renaud LP (1984) Facilitatory influence of noradrenergic afferents on the excitability of rat paraventricular nucleus neurosecretory cells. J Physiol 355(October):237–249. https://doi.org/10.1113/jphysiol.1984.sp015416
Day TA, Renaud LP, Sibbald JR (1990) Excitation of supraoptic vasopressin cells by stimulation of the A1 noradrenaline cell group: failure to demonstrate role for established adrenergic or amino acid receptors. Brain Res 516(1):91–98. https://doi.org/10.1016/0006-8993(90)90901-m
Day TA, Sibbald JR, Khanna S (1993) ATP mediates an excitatory noradrenergic neuron input to supraoptic vasopressin cells. Brain Res 607(1–2):341–344. https://doi.org/10.1016/0006-8993(93)91528-z
Gordon GRJ, Baimoukhametova DV, Hewitt SA, Kosala WRA, Rajapaksha JS, Fisher TE, Bains JS (2005) Norepinephrine triggers release of glial ATP to increase postsynaptic efficacy. Nat Neurosci 8(8):1078–1086. https://doi.org/10.1038/nn1498
Gordon GRJ, Iremonger KJ, Kantevari S, Ellis-Davies GCR, MacVicar BA, Bains JS (2009) Astrocyte-mediated distributed plasticity at hypothalamic glutamate synapses. Neuron 64(3):391–403. https://doi.org/10.1016/j.neuron.2009.10.021
Gourine AV, Kasymov V, Marina N, Tang F, Figueiredo MF, Lane S, Teschemacher AG, Spyer KM, Deisseroth K, Kasparov S (2010) Astrocytes control breathing through pH-dependent release of ATP. Science (New York, NY) 329(5991):571–575. https://doi.org/10.1126/science.1190721
Guthrie PB, Knappenberger J, Segal M, Bennett MV, Charles AC, Kater SB (1999) ATP released from astrocytes mediates glial calcium waves. J Neurosci 19(2):520–528
Hatton GI, Tweedle CD (1982) Magnocellular neuropeptidergic neurons in hypothalamus: increases in membrane apposition and number of specialized synapses from pregnancy to lactation. Brain Res Bull 8(2):197–204. https://doi.org/10.1016/0361-9230(82)90046-6
Hiruma H, Bourque CW (1995) P2 purinoceptor-mediated depolarization of rat supraoptic neurosecretory cells in vitro. J Physiol 489 (Pt 3):805–811
Huckstepp RT, id Bihi R, Eason R, Spyer KM, Dicke N, Willecke K, Marina N, Gourine AV, Dale N (2010) Connexin hemichannel-mediated CO2-dependent release of ATP in the medulla oblongata contributes to central respiratory chemosensitivity. J Physiol 588(Pt 20):3901–3920. https://doi.org/10.1113/jphysiol.2010.192088. Epub 2010 Aug 24
Kapoor JR, Sladek CD (2000) Purinergic and adrenergic agonists synergize in stimulating vasopressin and oxytocin release. J Neurosci 20(23):8868–8875
Kendrick KM, Leng G (1988) Haemorrhage-induced release of noradrenaline, 5-hydroxytryptamine and uric acid in the supraoptic nucleus of the rat, measured by microdialysis. Brain Res 440:402–406
Kronschläger MT, Drdla-Schutting R, Gassner M, Honsek SD, Teuchmann HL, Sandkühler J (2016) Gliogenic LTP spreads widely in nociceptive pathways. Science (New York, NY) 354(6316):1144–1148. https://doi.org/10.1126/science.aah5715
Lincoln DW, Wakerley JB (1974) Electrophysiological evidence for the activation of supraoptic neurones during the release of oxytocin. J Physiol 242(2):533–554. https://doi.org/10.1113/jphysiol.1974.sp010722. PMID: 4616998, PMCID: PMC1330682
Mori M, Tsushima H, Matsuda T (1992) Antidiuretic effects of purinoceptor agonists injected into the hypothalamic paraventricular nucleus of water-loaded, ethanol-anesthetized rats. Neuropharmacology 31(6):585–592. https://doi.org/10.1016/0028-3908(92)90191-q
Oliet SH, Piet R, Poulain DA (2001) Control of glutamate clearance and synaptic efficacy by glial coverage of neurons. Science (New York, NY) 292(5518):923–926. https://doi.org/10.1126/science.1059162
Panatier A, Theodosis DT, Mothet J-P, Touquet B, Pollegioni L, Poulain DA, Oliet SHR (2006) Glia-derived D-serine controls NMDA receptor activity and synaptic memory. Cell 125(4):775–784. https://doi.org/10.1016/j.cell.2006.02.051
Pascual O, Casper KB, Kubera C, Zhang J, Revilla-Sanchez R, Sul JY, Takano H, Moss SJ, McCarthy K, Haydon PG (2005) Astrocytic purinergic signaling coordinates synaptic networks. Science 310(5745):113–116
Renaud LP (1994) Hypothalamic magnocellular neurosecretory neurons: intrinsic membrane properties and synaptic connections. Prog Brain Res 100:133–137
Sawchenko PE, Swanson LW (1981) Central noradrenergic pathways for the integration of hypothalamic neuroendocrine and autonomic responses. Science (New York, NY) 214(4521):685–687. https://doi.org/10.1126/science.7292008
Shibuya I, Tanaka K, Hattori Y, Uezono Y, Harayama N, Noguchi J, Ueta Y, Izumi F, Yamashita H (1999) Evidence that multiple P2X purinoceptors are functionally expressed in rat supraoptic neurones. J Physiol 514(Pt 2):351–367
Shioda S, Nakai Y (1992) Noradrenergic innervation of vasopressin-containing neurons in the rat hypothalamic supraoptic nucleus. Neurosci Lett 140(2):215–218. https://doi.org/10.1016/0304-3940(92)90106-h
Shioda S, Yada T, Muroya S, Takigawa M, Nakai Y (1997) Noradrenaline activates vasopressin neurons via alpha1-receptor-mediated Ca2+ signaling pathway. Neurosci Lett 226(3):210–212. https://doi.org/10.1016/s0304-3940(97)00275-9
Theodosis DT, Poulain DA, Vincent JD (1981) Possible morphological bases for synchronisation of neuronal firing in the rat supraoptic nucleus during lactation. Neuroscience 6(5):919–929. https://doi.org/10.1016/0306-4522(81)90173-1
Tweedle CD, Hatton GI (1977) Ultrastructural changes in rat hypothalamic neurosecretory cells and their associated glia during minimal dehydration and rehydration. Cell Tissue Res 181(1):59–72. https://doi.org/10.1007/bf00222774
Vizi ES, Sperlagh B, Baranyi M (1992) Evidence that ATP released from the postsynaptic site by noradrenaline, is involved in mechanical responses of guineapig vas deferens: cascade transmission. Neuroscience 50:455–465
Von Kügelgen I, Allgaier C, Schobert A, Starke K (1994) Co-release of noradrenaline and ATP from cultured sympathetic neurons. Neuroscience 61(2):199–202
Yamashita H, Inenaga K, Kannan H (1987) Depolarizing effect of noradrenaline on neurons of the rat supraoptic nucleus in vitro. Brain Res 405(2):348–352. https://doi.org/10.1016/0006-8993(87)90304-0
Further Recommended Reading
Kronschläger MT, Drdla-Schutting R, Gassner M, Honsek SD, Teuchmann HL, Sandkühler J (2016) Gliogenic LTP spreads widely in nociceptive pathways. Science 354(6316):1144–1148
This paper describes a type of glial mediated LTP in the spinal cord that is similar to that described by Gordon et al. in the PVN, which relies on ATP, P2X7 receptors and d-serine
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2021 Springer Nature Switzerland AG
About this chapter
Cite this chapter
Gordon, G.R., Dayas, C.V., Bains, J.S. (2021). Astrocyte–Magnocellular Neuron Interactions in Hypothalamic Memory. In: Tasker, J.G., Bains, J.S., Chowen, J.A. (eds) Glial-Neuronal Signaling in Neuroendocrine Systems. Masterclass in Neuroendocrinology, vol 11. Springer, Cham. https://doi.org/10.1007/978-3-030-62383-8_4
Download citation
DOI: https://doi.org/10.1007/978-3-030-62383-8_4
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-62382-1
Online ISBN: 978-3-030-62383-8
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)