Advertisement

Structural and functional connections between the median and the ventrolateral preoptic nucleus

  • Augustin Walter
  • Lorijn van der Spek
  • Eléonore Hardy
  • Alexis Pierre Bemelmans
  • Nathalie Rouach
  • Armelle RancillacEmail author
Original Article

Abstract

The median preoptic nucleus (MnPO) and the ventrolateral preoptic nucleus (VLPO) are two brain structures that contain neurons essential for promoting non-rapid eye movement (NREM) sleep. However, their connections are still largely unknown. Here, we describe for the first time a slice preparation with an oblique coronal slicing angle at 70° from the horizontal in which their connectivity is preserved. Using the in vivo iDISCO method following viral infection of the MnPO or ex vivo biocytin crystal deposition in the MnPO of mouse brain slices, we revealed a strong axonal pathway from the MnPO to the VLPO. Then, to further explore the functionality of these projections, acute 70° slices were placed on multielectrode arrays (MEAs) and electrical stimulations were performed near the MnPO. Recordings of the signals propagation throughout the slices revealed a preferential pathway from the MnPO to the VLPO. Finally, we performed an input–output curve of field responses evoked by stimulation of the MnPO and recorded in the VLPO. We found that field responses were inhibited by GABAA receptor antagonist, suggesting that afferent inputs from the MnPO activate VLPO neuronal networks by disinhibition.

Keywords

Sleep-promoting neuron Field recordings VLPO MnPO NREM sleep MEA 

Notes

Acknowledgements

This work was supported by grants from the Centre National de la Recherche Scientifique (CNRS), the Institut National de la Santé et de la Recherche Médicale (Inserm), Collège de France and the Marie Sklodowska-Curie Research and Innovation Programme EU-GliaPhD (722053) (N.R.). We thank all the members of the animal house facility and imaging platform from Collège de France, including Philippe Mailly in particular. We gratefully acknowledge Yves Dupraz for the design of the brain cutting angles and IT people including Aurélien Agneray, in particular, for excellent and prompt technical assistance.

Compliance with ethical standards

Conflict of interest

The authors have no conflicts of interest to declare.

Ethical approval

All animal procedures were carried out according to the guidelines of European Community Council Directives of January first 2013 (2010/63/EU) and followed our local guidelines for the ethical treatment of animal care [Center for Interdisciplinary Research in Biology in College de France (France)]. The number of animals in our study was kept to the necessary minimum.

References

  1. Abbott SBG, Saper CB (2017) Median preoptic glutamatergic neurons promote thermoregulatory heat loss and water consumption in mice. J Physiol 595:6569–6583.  https://doi.org/10.1113/JP274667 CrossRefGoogle Scholar
  2. Abbott SBG, Machado NLS, Geerling JC, Saper CB (2016) Reciprocal control of drinking behavior by median preoptic neurons in mice. J Neurosci 36:8228–8237.  https://doi.org/10.1523/jneurosci.1244-16.2016 CrossRefGoogle Scholar
  3. Alam MA, Kumar S, McGinty D et al (2014) Neuronal activity in the preoptic hypothalamus during sleep deprivation and recovery sleep. J Neurophysiol 111:287–299.  https://doi.org/10.1152/jn.00504.2013 CrossRefGoogle Scholar
  4. Anaclet C, Ferrari L, Arrigoni E et al (2014) The GABAergic parafacial zone is a medullary slow wave sleep-promoting center. Nat Neurosci 17:1217–1224.  https://doi.org/10.1038/nn.3789 CrossRefGoogle Scholar
  5. Chever O, Dossi E, Pannasch U et al (2016) Astroglial networks promote neuronal coordination. Sci Signal 9:1–9.  https://doi.org/10.1126/scisignal.aad3066 CrossRefGoogle Scholar
  6. Chou TC, Bjorkum AA, Gaus SE et al (2002) Afferents to the ventrolateral preoptic nucleus. J Neurosci 22:977–990CrossRefGoogle Scholar
  7. Economo CV (1930) Sleep as a problem of localization. J Nerv Ment Dis 71:249–259.  https://doi.org/10.1097/00005053-193003000-00001 CrossRefGoogle Scholar
  8. Franklin KBJ, Paxinos G (2007) The mouse brain in stereotaxic coordinates, 3rd edn. Academic Press, San DiegoGoogle Scholar
  9. Gaus SE, Strecker RE, Tate BA et al (2002) Ventrolateral preoptic nucleus contains sleep-active, galaninergic neurons in multiple mammalian species. Neuroscience 115:285–294CrossRefGoogle Scholar
  10. Gong S, Zheng C, Doughty ML et al (2003) A gene expression atlas of the central nervous system based on bacterial artificial chromosomes. Nature 425:917–925.  https://doi.org/10.1038/nature02033 CrossRefGoogle Scholar
  11. Gong H, McGinty D, Guzman-Marin R et al (2004) Activation of c-Fos in GABAergic neurones in the preoptic area during sleep and in response to sleep deprivation. J Physiol 556:935–946CrossRefGoogle Scholar
  12. Gvilia I, Xu F, McGinty D, Szymusiak R (2006) Homeostatic regulation of sleep: a role for preoptic area neurons. J Neurosci 26:9426–9433.  https://doi.org/10.1523/JNEUROSCI.2012-06.2006 CrossRefGoogle Scholar
  13. Kroeger D, Absi G, Gagliardi C et al (2018) Galanin neurons in the ventrolateral preoptic area promote sleep and heat loss in mice. Nat Commun.  https://doi.org/10.1038/s41467-018-06590-7 Google Scholar
  14. MacLean JN, Fenstermaker V, Watson BO, Yuste R (2006) A visual thalamocortical slice. Nat Methods 3:129–134.  https://doi.org/10.1038/nmeth849 CrossRefGoogle Scholar
  15. McKinley MJ, Yao ST, Uschakov A et al (2015) The median preoptic nucleus: front and centre for the regulation of body fluid, sodium, temperature, sleep and cardiovascular homeostasis. Acta Physiol (Oxf) 214:8–32.  https://doi.org/10.1111/apha.12487 CrossRefGoogle Scholar
  16. Pannasch U, Freche D, Dallérac G et al (2014) Connexin 30 sets synaptic strength by controlling astroglial synapse invasion. Nat Neurosci 17:549–558.  https://doi.org/10.1038/nn.3662 CrossRefGoogle Scholar
  17. Renier N, Wu Z, Simon DJ et al (2014) IDISCO: a simple, rapid method to immunolabel large tissue samples for volume imaging. Cell 159:896–910.  https://doi.org/10.1016/j.cell.2014.10.010 CrossRefGoogle Scholar
  18. Ross FM, Cassidy J, Wilson M, Davies SN (2000) Developmental regulation of hippocampal excitatory synaptic transmission by metabotropic glutamate receptors. Br J Pharmacol 131:453–464.  https://doi.org/10.1038/sj.bjp.0703610 CrossRefGoogle Scholar
  19. Sakai K, Crochet S (2001) Differentiation of presumed serotonergic dorsal raphe neurons in relation to behavior and wake–sleep states. Neuroscience 104:1141–1155CrossRefGoogle Scholar
  20. Saper CB, Scammell TE, Lu J (2005) Hypothalamic regulation of sleep and circadian rhythms. Nature 437:1257–1263CrossRefGoogle Scholar
  21. Saper CB, Fuller PM, Pedersen NP et al (2010) Sleep state switching. Neuron 68:1023–1042CrossRefGoogle Scholar
  22. Scammell TE, Arrigoni E, Lipton JO (2017) Neural circuitry of wakefulness and sleep. Neuron 93:747–765.  https://doi.org/10.1016/j.neuron.2017.01.014 CrossRefGoogle Scholar
  23. Scharbarg E, Daenens M, Lemaître F et al (2016) Astrocyte-derived adenosine is central to the hypnogenic effect of glucose. Sci Rep 6:19107CrossRefGoogle Scholar
  24. Sherin JE, Shiromani PJ, McCarley RW, Saper CB (1996) Activation of ventrolateral preoptic neurons during sleep. Science 271:216–219CrossRefGoogle Scholar
  25. Sherin JE, Elmquist JK, Torrealba F, Saper CB (1998) Innervation of histaminergic tuberomammillary neurons by GABAergic and galaninergic neurons in the ventrolateral preoptic nucleus of the rat. J Neurosci 18:4705–4721CrossRefGoogle Scholar
  26. Suntsova N, Szymusiak R, Alam MN et al (2002) Sleep-waking discharge patterns of median preoptic nucleus neurons in rats. J Physiol 543:665–677.  https://doi.org/10.1113/jphysiol.2002.023085 CrossRefGoogle Scholar
  27. Szymusiak R, Alam N, Steininger TL, McGinty D (1998) Sleep-waking discharge patterns of ventrolateral preoptic/anterior hypothalamic neurons in rats. Brain Res 803:178–188CrossRefGoogle Scholar
  28. Takahashi K, Lin J-S, Sakai K (2009) Characterization and mapping of sleep-waking specific neurons in the basal forebrain and preoptic hypothalamus in mice. Neuroscience 161:269–292.  https://doi.org/10.1016/j.neuroscience.2009.02.075 CrossRefGoogle Scholar
  29. Thompson RH, Swanson LW (2003) Structural characterization of a hypothalamic visceromotor pattern generator network. Brain Res Brain Res Rev 41:153–202CrossRefGoogle Scholar
  30. Uschakov A, Gong H, McGinty D, Szymusiak R (2006) Sleep-active neurons in the preoptic area project to the hypothalamic paraventricular nucleus and perifornical lateral hypothalamus. Eur J Neurosci 23:3284–3296CrossRefGoogle Scholar
  31. Uschakov A, Gong H, McGinty D, Szymusiak R (2007) Efferent projections from the median preoptic nucleus to sleep- and arousal-regulatory nuclei in the rat brain. Neuroscience 150:104–120CrossRefGoogle Scholar
  32. Williams RH, Chee MJS, Kroeger D et al (2014) Optogenetic-mediated release of histamine reveals distal and autoregulatory mechanisms for controlling arousal. J Neurosci 34:6023–6029.  https://doi.org/10.1523/JNEUROSCI.4838-13.2014 CrossRefGoogle Scholar
  33. Zhang W, Zhou Q, Chen W et al (2017) A hypothalamic circuit that controls body temperature. Proc Natl Acad Sci 114:E1755.  https://doi.org/10.1073/pnas.1701881114 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Neuroglial Interactions in Cerebral Physiopathology, Center for Interdisciplinary Research in BiologyCentre National de la Recherche Scientifique UMR 7241, Institut National de la Santé et de la Recherche Médicale U1050, Collège de France, Labex Memolife, PSL-UniversityParisFrance
  2. 2.Commissariat à l’Energie Atomique et aux Energies Alternatives, Département de la Recherche Fondamentale, Institut de biologie François JacobMolecular Imaging Research Center and Centre National de la Recherche Scientifique UMR9199, Université Paris-Sud, Neurodegenerative Diseases LaboratoryFontenay-aux-RosesFrance

Personalised recommendations