GABAergic neurons intermingled with orexin and MCH neurons in the lateral hypothalamus discharge maximally during sleep

European Journal of Neuroscience

Volumn 32, Issue 3, 2010, Pages 448-457

  Hassani, Oum Kaltoum ^a   Henny, Pablo ^a,c   Lee, Maan Gee ^b   Jones, Barbara E ^a  

^a MCGILL UNIVERSITY   (Canada)

^b Kyungpook National University School of Medicine   (South Korea)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

arousal; paradoxical sleep; rapid eye movement sleep; rat; slow wave sleep; vesicular GABA transporter

Indexed keywords

4 AMINOBUTYRIC ACID; GLUTAMIC ACID; MELANIN CONCENTRATING HORMONE; OREXIN; VESICULAR INHIBITORY AMINO ACID TRANSPORTER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CORRELATION ANALYSIS; ELECTROENCEPHALOGRAPHY; GABAERGIC TRANSMISSION; IMMUNOHISTOCHEMISTRY; LATERAL HYPOTHALAMUS; MUSCLE ATONIA; NONHUMAN; PRIORITY JOURNAL; RAT; REM SLEEP; SLEEP; SLEEP WAKING CYCLE; SLOW WAVE SLEEP; VARICOSIS;

ANALYSIS OF VARIANCE; ANIMALS; AROUSAL; ELECTROENCEPHALOGRAPHY; ELECTROMYOGRAPHY; GAMMA-AMINOBUTYRIC ACID; HYPOTHALAMIC HORMONES; HYPOTHALAMUS; IMMUNOHISTOCHEMISTRY; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MELANINS; NEURONS; NEUROPEPTIDES; PITUITARY HORMONES; RATS; SLEEP; SYNAPTIC TRANSMISSION; VESICULAR INHIBITORY AMINO ACID TRANSPORT PROTEINS;

EID: 77955167922     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2010.07295.x     Document Type: Article

References (40)

1. Alam, M.N., Gong, H., Alam, T., Jaganath, R., McGinty, D. Szymusiak, R. (2002) Sleep-waking discharge patterns of neurons recorded in the rat perifornical lateral hypothalamic area. J. Physiol., 538, 619 631.
2. Alam, M.N., Kumar, S., Bashir, T., Suntsova, N., Methippara, M.M., Szymusiak, R. McGinty, D. (2005) GABA-mediated control of hypocretin- but not melanin-concentrating hormone-immunoreactive neurones during sleep in rats. J. Physiol., 563, 569 582.
3. Boissard, R., Fort, P., Gervasoni, D., Barbagli, B. Luppi, P.H. (2003) Localization of the GABAergic and non-GABAergic neurons projecting to the sublaterodorsal nucleus and potentially gating paradoxical sleep onset. Eur. J. Neurosci., 18, 1627 1639.
4. Broberger, C., De Lecea, L., Sutcliffe, J.G. Hokfelt, T. (1998) Hypocretin/orexin- and melanin-concentrating hormone-expressing cells form distinct populations in the rodent lateral hypothalamus: relationship to the neuropeptide Y and agouti gene-related protein systems. J. Comp. Neurol., 402, 460 474.
5. Chaudhry, F.A., Reimer, R.J., Bellocchio, E.E., Danbolt, N.C., Osen, K.K., Edwards, R.H. Storm-Mathisen, J. (1998) The vesicular GABA transporter, VGAT, localizes to synaptic vesicles in sets of glycinergic as well as GABAergic neurons. J. Neurosci., 18, 9733 9750.
6. Chemelli, R.M., Willie, J.T., Sinton, C.M., Elmquist, J.K., Scammell, T., Lee, C., Richardson, J.A., Williams, S.C., Xiong, Y., Kisanuki, Y., Fitch, T.E., Nakazato, M., Hammer, R.E., Saper, C.B. Yanagisawa, M. (1999) Narcolepsy in orexin knockout mice: molecular genetics of sleep regulation. Cell, 98, 437 451.
7. Decavel, C. Van den Pol, A.N. (1990) GABA: a dominant neurotransmitter in the hypothalamus. J. Comp. Neurol., 302, 1019 1037.
8. von Economo, C. (1930) Sleep as a problem of localization. J. Nerv. Ment. Dis., 71, 249 259.
9. Eggermann, E., Bayer, L., Serafin, M., Saint-Mleux, B., Bernheim, L., Machard, D., Jones, B.E. Muhlethaler, M. (2003) The wake-promoting hypocretin-orexin neurons are in an intrinsic state of membrane depolarization. J. Neurosci., 23, 1557 1562.
10. Fremeau, R.T. Jr., Troyer, M.D., Pahner, I., Nygaard, G.O., Tran, C.H., Reimer, R.J., Bellocchio, E.E., Fortin, D., Storm-Mathisen, J. Edwards, R.H. (2001) The expression of vesicular glutamate transporters defines two classes of excitatory synapse. Neuron, 31, 247 260.
11. Gervasoni, D., Darracq, L., Fort, P., Souliere, F., Chouvet, G. Luppi, P.H. (1998) Electrophysiological evidence that noradrenergic neurons of the rat locus coeruleus are tonically inhibited by GABA during sleep. Eur. J. Neurosci., 10, 964 970.
12. Hassani, O.K., Lee, M.G., Henny, P. Jones, B.E. (2009a) Discharge profiles of identified GABAergic in comparison to cholinergic and putative glutamatergic basal forebrain neurons across the sleep-wake cycle. J. Neurosci., 29, 11828 11840.
13. Hassani, O.K., Lee, M.G. Jones, B.E. (2009b) Melanin-concentrating hormone neurons discharge in a reciprocal manner to orexin neurons across the sleep-wake cycle. Proc. Natl. Acad. Sci. USA, 106, 2418 2422.
14. Henny, P. Jones, B.E. (2006a) Innervation of orexin/hypocretin neurons by GABAergic, glutamatergic or cholinergic basal forebrain terminals evidenced by immunostaining for presynaptic vesicular transporter and postsynaptic scaffolding proteins. J. Comp. Neurol., 499, 645 661.
15. Henny, P. Jones, B.E. (2006b) Vesicular glutamate (VGluT), GABA (VGAT), and acetylcholine (VAChT) transporters in basal forebrain axon terminals innervating the lateral hypothalamus. J. Comp. Neurol., 496, 453 467.
16. Jones, B.E. (2005) Basic mechanisms of sleep-wake states. In Kryger, M.H., Roth, T. Dement, W.C. (Eds Principles and Practice of Sleep Medicine. Elsevier Saunders, Philadelphia, pp. 136 153.
17. Koyama, Y. Hayaishi, O. (1994) Firing of neurons in the preoptic/anterior hypothalamic areas in rat: its possible involvement in slow wave sleep and paradoxical sleep. Neurosci. Res., 19, 31 38.
18. Koyama, Y., Takahashi, K., Kodama, T. Kayama, Y. (2003) State-dependent activity of neurons in the perifornical hypothalamic area during sleep and waking. Neuroscience, 119, 1209 1219.
19. Lee, M.G., Manns, I.D., Alonso, A. Jones, B.E. (2004) Sleep-wake related discharge properties of basal forebrain neurons recorded with micropipettes in head-fixed rats. J. Neurophysiol., 92, 1182 1198.
20. Lee, M.G., Hassani, O.K., Alonso, A. Jones, B.E. (2005a) Cholinergic basal forebrain neurons burst with theta during waking and paradoxical sleep. J. Neurosci., 25, 4365 4369.
21. Lee, M.G., Hassani, O.K. Jones, B.E. (2005b) Discharge of identified orexin/hypocretin neurons across the sleep-waking cycle. J. Neurosci., 25, 6716 6720.
22. Lin, L., Faraco, J., Li, R., Kadotani, H., Rogers, W., Lin, X., Qiu, X., de Jong, P.J., Nishino, S. Mignot, E. (1999) The sleep disorder canine narcolepsy is caused by a mutation in the hypocretin (orexin) receptor 2 gene. Cell, 98, 365 376.
23. Maloney, K.J., Cape, E.G., Gotman, J. Jones, B.E. (1997) High-frequency gamma electroencephalogram activity in association with sleep-wake states and spontaneous behaviors in the rat. Neuroscience, 76, 541 555.
24. Maloney, K.J., Mainville, L. Jones, B.E. (1999) Differential c-Fos expression in cholinergic, monoaminergic and GABAergic cell groups of the pontomesencephalic tegmentum after paradoxical sleep deprivation and recovery. J. Neurosci., 19, 3057 3072.
25. Maloney, K.J., Mainville, L. Jones, B.E. (2000) c-Fos expression in GABAergic, serotonergic and other neurons of the pontomedullary reticular formation and raphe after paradoxical sleep deprivation and recovery. J. Neurosci., 20, 4669 4679.
26. Manns, I.D., Alonso, A. Jones, B.E. (2000) Discharge profiles of juxtacellularly labeled and immunohistochemically identified GABAergic basal forebrain neurons recorded in association with the electroencephalogram in anesthetized rats. J. Neurosci., 20, 9252 9263. (Pubitemid 32042928)
27. McGinty, D. Szymusiak, R. (2005) Sleep-promoting mechanisms in mammals. In Kryger, M.H., Roth, T. Dement, W. (Eds Principles and Practice of Sleep Medicine. Elsevier Saunders, Philadelphia, pp. 169 184.
28. Mileykovskiy, B.Y., Kiyashchenko, L.I. Siegel, J.M. (2005) Behavioral correlates of activity in identified hypocretin/orexin neurons. Neuron, 46, 787 798.
29. Modirrousta, M., Mainville, L. Jones, B.E. (2005) Orexin and MCH neurons express c-Fos differently after sleep deprivation vs. recovery and bear different adrenergic receptors. Eur. J. Neurosci., 21, 2807 2816.
30. Nitz, D. Siegel, J.M. (1997) GABA release in the locus coeruleus as a function of sleep/wake state. Neuroscience, 78, 795 801.
31. Peyron, C., Faraco, J., Rogers, W., Ripley, B., Overeem, S., Charnay, Y., Nevsimalova, S., Aldrich, M., Reynolds, D., Albin, R., Li, R., Hungs, M., Pedrazzoli, M., Padigaru, M., Kucherlapati, M., Fan, J., Maki, R., Lammers, G.J., Bouras, C., Kucherlapati, R., Nishino, S. Mignot, E. (2000) A mutation in a case of early onset narcolepsy and a generalized absence of hypocretin peptides in human narcoleptic brains. Nat. Med., 6, 991 997.
32. Rodrigo-Angulo, M.L., Heredero, S., Rodriguez-Veiga, E. Reinoso-Suarez, F. (2008) GABAergic and non-GABAergic thalamic, hypothalamic and basal forebrain projections to the ventral oral pontine reticular nucleus: their implication in REM sleep modulation. Brain Res., 1210, 116 125.
33. Saper, C.B., Chou, T.C. Scammell, T.E. (2001) The sleep switch: hypothalamic control of sleep and wakefulness. Trends Neurosci., 24, 726 731.
34. Sapin, E., Leger, L., Berod, A., Herman, P., Luppi, P.-H. Peyron, C. (2009) Localization of hypothalamic GABAergic neurons implicated in Paradoxical (REM) Sleep regulation and their relationship with MCH neurons. Program No. 375.22. 2009 Neuroscience Meeting Planner : Chicago, IL, Society for Neuroscience, 2009. Online.
35. Thannickal, T.C., Moore, R.Y., Nienhuis, R., Ramanathan, L., Gulyani, S., Aldrich, M., Cornford, M. Siegel, J.M. (2000) Reduced number of hypocretin neurons in human narcolepsy. Neuron, 27, 469 474.
36. Verret, L., Goutagny, R., Fort, P., Cagnon, L., Salvert, D., Leger, L., Boissard, R., Salin, P., Peyron, C. Luppi, P.H. (2003) A role of melanin-concentrating hormone producing neurons in the central regulation of paradoxical sleep. BMC Neurosci., 4, 19.
37. Verret, L., Fort, P., Gervasoni, D., Leger, L. Luppi, P.H. (2006) Localization of the neurons active during paradoxical (REM) sleep and projecting to the locus coeruleus noradrenergic neurons in the rat. J. Comp. Neurol., 495, 573 586.
38. Vincent, S.R., Hokfelt, T., Skirboll, L.R. Wu, J.-Y. (1983) Hypothalamic gamma-aminobutyric acid neurons project to the neocortex. Science, 220, 1309 1311.
39. Xie, X., Crowder, T.L., Yamanaka, A., Morairty, S.R., Lewinter, R.D., Sakurai, T. Kilduff, T.S. (2006) GABA(B) receptor-mediated modulation of hypocretin/orexin neurones in mouse hypothalamus. J. Physiol., 574, 399 414.
40. Yoshida, K., McCormack, S., Espana, R.A., Crocker, A. Scammell, T.E. (2006) Afferents to the orexin neurons of the rat brain. J. Comp. Neurol., 494, 845 861.