Skip to main content
Log in

Multiparametric characterization of neuronal subpopulations in the ventrolateral preoptic nucleus

  • Original Article
  • Published:
Brain Structure and Function Aims and scope Submit manuscript

Abstract

The characterization of neuronal properties is a necessary first step toward understanding how the ventrolateral preoptic nucleus (VLPO) neuronal network regulates slow-wave sleep (SWS). Indeed, the electrophysiological heterogeneity of VLPO neurons suggests the existence of subtypes that could differently contribute in SWS induction and maintenance. The aim of the present study was to define cell classes in the VLPO using an unsupervised clustering classification method. Electrophysiological features extracted from 289 neurons recorded in whole-cell patch-clamp allowed the identification of three main classes of VLPO neurons subdivided into five distinct subpopulations (cluster 1, 2a, 2b, 3a and 3b). The high occurrence of a low-threshold calcium spike (LTS) was one of the most distinctive features of cluster 1 and 3. Since sleep-promoting neurons are generally identified by their ability to generate an LTS and by their inhibitory response to noradrenaline (NA), 189 neurons from our dataset were also tested for this neurotransmitter. Neurons from cluster 3 were the most frequently inhibited by NA. Biocytin labeling and Neurolucida reconstructions of 112 neurons furthermore revealed a small dendritic arbor of cluster 3b neurons compared, in particular, to cluster 2b neurons. Altogether, we performed an exhaustive characterization of VLPO neuronal subtypes that is a crucial step toward a better understanding of the neuronal network within the VLPO and thereby sleep physiology.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Ascoli GA, Onso-Nanclares L, Anderson SA et al (2008) Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex. Nat Rev Neurosci 9:557–568

    Article  CAS  PubMed  Google Scholar 

  • Cauli B, Audinat E, Lambolez B et al (1997) Molecular and physiological diversity of cortical nonpyramidal cells. J Neurosci 17:3894–3906

    CAS  PubMed  Google Scholar 

  • Fort P, Bassetti CL, Luppi PH (2009) Alternating vigilance states: new insights regarding neuronal networks and mechanisms. Eur J Neurosci 29:1741–1753

    Article  CAS  PubMed  Google Scholar 

  • Gallopin T, Fort P, Eggermann E et al (2000) Identication of sleep-promoting neurons in vitro. Nature 404:3–6

    Google Scholar 

  • Gallopin T, Luppi PH, Rambert FA et al (2004) Effect of the wake-promoting agent modafinil on sleep-promoting neurons from the ventrolateral preoptic nucleus: an in vitro pharmacologic study. Sleep 27:19–25

    PubMed  Google Scholar 

  • Gallopin T, Luppi PH, Cauli B et al (2005) The endogenous somnogen adenosine excites a subset of sleep-promoting neurons via A2A receptors in the ventrolateral preoptic nucleus. Neuroscience 134:1377–1390

    Article  CAS  PubMed  Google Scholar 

  • Karagiannis A, Gallopin T, David C et al (2009) Classification of NPY-expressing neocortical interneurons. J Neurosci 29:3642–3659

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khateb A, Fort P, Alonso A et al (1993) Pharmacological and immunohistochemical evidence for serotonergic modulation of cholinergic nucleus basalis neurons. Eur J Neurosci 5:541–547

    Article  CAS  PubMed  Google Scholar 

  • Liu Y-W, Li J, Ye J-H (2010) Histamine regulates activities of neurons in the ventrolateral preoptic nucleus. J Physiol 588:4103–4116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Y-W, Zuo W, Ye J-H (2013) Propofol stimulates noradrenalin-inhibited neurons in the ventrolateral preoptic nucleus by reducing GABAergic inhibition. Anesth Analg 117:358–363

    Article  CAS  PubMed  Google Scholar 

  • Lu J, Greco MA, Shiromani P, Saper CB (2000) Effect of lesions of the ventrolateral preoptic nucleus on NREM and REM sleep. J Neurosci 20:3830–3842

    CAS  PubMed  Google Scholar 

  • Matsuo S-I, Jang I-S, Nabekura J, Akaike N (2003) alpha 2-Adrenoceptor-mediated presynaptic modulation of GABAergic transmission in mechanically dissociated rat ventrolateral preoptic neurons. J Neurophysiol 89:1640–1648

    Article  CAS  PubMed  Google Scholar 

  • McCarren HS, Chalifoux MR, Han B et al (2014) 2-adrenergic stimulation of the ventrolateral preoptic nucleus destabilizes the anesthetic state. J Neurosci 34:16385–16396. doi:10.1523/JNEUROSCI.1135-14.2014

    Article  PubMed  PubMed Central  Google Scholar 

  • Moore JT, Chen J, Han B et al (2012) Direct activation of sleep-promoting VLPO neurons by volatile anesthetics contributes to anesthetic hypnosis. Curr Biol 22:2008–2016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morairty S, Rainnie D, McCarley R, Greene R (2004) Disinhibition of ventrolateral preoptic area sleep-active neurons by adenosine: a new mechanism for sleep promotion. Neuroscience 123:451–457

    Article  CAS  PubMed  Google Scholar 

  • Perrenoud Q, Geoffroy H, Gauthier B et al (2012) Characterization of Type I and Type II nNOS-expressing interneurons in the barrel cortex of mouse. Front Neural Circuits 6:1–17

    Google Scholar 

  • Saint-Mleux B, Eggermann E, Bisetti A et al (2004) Nicotinic enhancement of the noradrenergic inhibition of sleep-promoting neurons in the ventrolateral preoptic area. J Neurosci 24:63–67

    Article  CAS  PubMed  Google Scholar 

  • Saint-Mleux B, Bayer L, Eggermann E et al (2007) Suprachiasmatic modulation of noradrenaline release in the ventrolateral preoptic nucleus. J Neurosci 27:6412–6416

    Article  CAS  PubMed  Google Scholar 

  • Sangare A, Dubourget R, Geoffroy H, Gallopin T, Rancillac A (2016) Serotonin differentially modulates excitatory and inhibitory synaptic inputs to putative sleep-promoting neurons of the ventrolateral preoptic nucleus. Neuropharmacology 109:29–40. doi:10.1016/j.neuropharm.2016.05.015

    Article  CAS  PubMed  Google Scholar 

  • Saper CB, Scammell TE, Lu J (2005) Hypothalamic regulation of sleep and circadian rhythms. Nature 437:1257–1263

    Article  CAS  PubMed  Google Scholar 

  • Saper CB, Fuller PM, Pedersen NP et al (2010) Sleep state switching. Neuron 68:1023–1042

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scharbarg E, Daenens M, Lemaître F et al (2016) Astrocyte-derived adenosine is central to the hypnogenic effect of glucose. Sci Rep 6:19107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sherin JE, Shiromani PJ, McCarley RW, Saper CB (1996) Activation of ventrolateral preoptic neurons during sleep. Science 271:216–219

    Article  CAS  PubMed  Google Scholar 

  • 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 18:4705–4721

    CAS  PubMed  Google Scholar 

  • Sholl DA (1953) Dendritic organization in the neurons of the visual and motor cortices of the cat. J Anat 87:387–406

    CAS  PubMed  PubMed Central  Google Scholar 

  • Unal CT, Golowasch JP, Zaborszky L (2012) Adult mouse basal forebrain harbors two distinct cholinergic populations defined by their electrophysiology. Front Behav Neurosci 6:21

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Varin C, Rancillac A, Geoffroy H et al (2015) Glucose induces slow-wave sleep by exciting the sleep-promoting neurons in the ventrolateral preoptic nucleus: a new link between sleep and metabolism. J Neurosci 35:9900–9911

    Article  CAS  PubMed  Google Scholar 

  • Von Economo C (1930) Sleep as a problem of localization. J Nerv Ment Dis 71:249–259

    Article  Google Scholar 

  • Wang Q, Yue X-F, Qu W-M, et al (2012) Morphine inhibits sleep-promoting neurons in the ventrolateral preoptic area via mu receptors and induces wakefulness in rats. Neuropsychopharmacology 1–11

  • Ward JH (1963) Hierarchical grouping to optimize an objective function. J Am Stat Assoc 58:236–244

    Article  Google Scholar 

Download references

Acknowledgments

This work was supported by a Grant from ANR-12-JSV4-001-01, the Centre National de la Recherche Scientifique (CNRS), the French Institute of Health and Medical Research (Inserm) and ESPCI ParisTech. We are grateful to Judith Pineau and Aude Duhamel for technical support. The authors declare no competing financial interests.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Armelle Rancillac.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dubourget, R., Sangare, A., Geoffroy, H. et al. Multiparametric characterization of neuronal subpopulations in the ventrolateral preoptic nucleus. Brain Struct Funct 222, 1153–1167 (2017). https://doi.org/10.1007/s00429-016-1265-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00429-016-1265-2

Keywords

Navigation