Abstract
The adult hypothalamo-neurohypophysial system (HNS) comprises the cell bodies of the magnocellular neurons of the hypothalamus, located in the supraoptic and paraventricular nuclei, and their axons that project onto the neurohypophysis, where they release oxytocin and vasopressin directly in the bloodstream. Oxytocin governs parturition and lactation, while vasopressin is the antidiuretic hormone and a vasopressor. The HNS undergoes a remarkable reversible, activity-dependent morphological neuroglial plasticity during lactation and dehydration. Here we summarize how this made it a seminal model to study the physiological contribution of the astrocytic environment to synaptic signaling. We show first that reduction in glial processes modifies local glutamate level at the synapse by reducing its uptake, and thus affects homosynaptic strength. Second, it also changes neurotransmitter diffusion, and as a result contributes to inter-synaptic crosstalk between glutamate and GABAergic inputs through metabotropic and kainate receptors. Finally it hampers the contribution of astrocytes to glutamatergic synaptic communication through d-serine gliotransmission. Astrocytes thus dynamically dictate the tenor of brain signaling.
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References
Armstrong WE (2015) Hypothalamic supraoptic and paraventricular nuclei. In: Paxinos G (ed) The rat nervous system, 4th edn. Elsevier, Sydney, pp 295–314
Bonfardin VD, Fossat P, Theodosis DT et al (2010) Glia-dependent switch of kainate receptor presynaptic action. J Neurosci 30:985–995
Boudaba C, Linn DM, Halmos KC et al (2003) Increased tonic activation of presynaptic metabotropic glutamate receptors in the rat supraoptic nucleus following chronic dehydration. J Physiol 551:815–823
Bourque CW (2008) Central mechanisms of osmosensation and systemic osmoregulation. Nat Rev Neurosci 9:519–531
Brown CH, Bains JS, Ludwig M et al (2013) Physiological regulation of magnocellular neurosecretory cell activity: integration of intrinsic, local and afferent mechanisms. J Neuroendocrinol 25:678–710
Catheline G, Touquet B, Lombard MC et al (2006) A study of the role of neuro-glial remodeling in the oxytocin system at lactation. Neuroscience 137:309–316
Choe KY, Olson JE, Bourque CW (2012) Taurine release by astrocytes modulates osmosensitive glycine receptor tone and excitability in the adult supraoptic nucleus. J Neurosci 32:12518–12527
Deleuze C, Alonso G, Lefevre IA et al (2005) Extrasynaptic localization of glycine receptors in the rat supraoptic nucleus: further evidence for their involvement in glia-to-neuron communication. Neuroscience 133:175–183
Di S, Popescu IR, Tasker JG (2013) Glial control of endocannabinoid heterosynaptic modulation in hypothalamic magnocellular neuroendocrine cells. J Neurosci 33:18331–18342
Fiacco TA, McCarthy KD (2018) Multiple lines of evidence indicate that gliotransmission does not occur under physiological conditions. J Neurosci 38:3–13
Gordon GR, Baimoukhametova DV, Hewitt SA et al (2005) Norepinephrine triggers release of glial ATP to increase postsynaptic efficacy. Nat Neurosci 8:1078–1086
Hussy N, Deleuze C, Desarmenien MG et al (2000) Osmotic regulation of neuronal activity: a new role for taurine and glial cells in a hypothalamic neuroendocrine structure. Prog Neurobiol 62:113–134
Jourdain P, Israel JM, Dupouy B et al (1998) Evidence for a hypothalamic oxytocin-sensitive pattern-generating network governing oxytocin neurons in vitro. J Neurosci 18:6641–6649
Ludwig M, Stern J (2015) Multiple signalling modalities mediated by dendritic exocytosis of oxytocin and vasopressin. Philos Trans R Soc B Biol Sci 370:1672
Miyata S, Hatton GI (2002) Activity-related, dynamic neuron-glial interactions in the hypothalamo-neurohypophysial system. Microsc Res Tech 56:143–157
Oliet SH, Piet R, Poulain DA (2001) Control of glutamate clearance and synaptic efficacy by glial coverage of neurons. Science 292:923–926
Panatier A, Theodosis DT, Mothet JP et al (2006) Glia-derived d-serine controls NMDA receptor activity and synaptic memory. Cell 125:775–784
Panatier A, Vallée J, Haber M et al (2011) Astrocytes are endogenous regulators of basal transmission at central synapses. Cell 146:785–798
Papouin T, Henneberger C, Rusakov DA et al (2017) Astroglial versus neuronal d-serine: fact checking. Trends Neurosci 40:517–520
Piet R, Bonhomme R, Theodosis DT et al (2003) Modulation of GABAergic transmission by endogenous glutamate in the rat supraoptic nucleus. Eur J Neurosci 17:1777–1785
Piet R, Vargová L, Syková E et al (2004) Physiological contribution of the astrocytic environment of neurons to intersynaptic crosstalk. Proc Natl Acad Sci U S A 101:2151–2155
Poulain DA, Wakerley JB (1982) Electrophysiology of hypothalamic magnocellular neurons secreting oxytocin and vasopressin. Neuroscience 7:773–808
Salm AK (2000) Mechanisms of glial retraction in the hypothalamo-neurohypophysial system of the rat. Exp Physiol 85 Spec No:197S–202S
Savtchouk I, Volterra A (2018) Gliotransmission: beyond black-and-white. J Neurosci 38:14–25
Theodosis DT, Piet R, Poulain DA et al (2004) Neuronal, glial and synaptic remodeling in the adult hypothalamus: functional consequences and role of cell surface and extracellular matrix adhesion molecules. Neurochem Int 45:491–501
Wolosker H, Balu DT, Coyle JT (2016) The rise and fall of the d-serine -mediated gliotransmission hypothesis. Trends Neurosci 39:712–721
Further Recommended Reading
Tasker JG, Voisin DL, Armstrong WE (2017) The cell biology of oxytocin and vasopressin cells. In: Pfaff DW, Joëls M (eds) Hormones, brain, and behavior, 3rd edn. Academic, Oxford, pp 305–336
Theodosis DT, Poulain DA, Oliet SH (2008) Activity-dependent structural and functional plasticity of astrocyte-neuron interactions. Physiol Rev 88:983–1008
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Voisin, D.L., Panatier, A., Oliet, S.H.R. (2021). Functional Consequences of Morphological Plasticity in the Adult Hypothalamo-Neurohypophysial System. 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_2
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