Cataplexy-active Neurons in the Hypothalamus: Implications for the Role of Histamine in Sleep and Waking Behavior

Overview

Journal Neuron

Publisher Cell Press

Specialty Neurology

Date 2004 May 26

PMID 15157423

Citations 100

Authors

Joshi John

Ming-Fung Wu

Lisa N Boehmer

Jerome M Siegel

Affiliations

Soon will be listed here.

Abstract

Noradrenergic, serotonergic, and histaminergic neurons are continuously active during waking, reduce discharge during NREM sleep, and cease discharge during REM sleep. Cataplexy, a symptom associated with narcolepsy, is a waking state in which muscle tone is lost, as it is in REM sleep, while environmental awareness continues, as in alert waking. In prior work, we reported that, during cataplexy, noradrenergic neurons cease discharge, and serotonergic neurons greatly reduce activity. We now report that, in contrast to these other monoaminergic "REM-off" cell groups, histamine neurons are active in cataplexy at a level similar to or greater than that in quiet waking. We hypothesize that the activity of histamine cells is linked to the maintenance of waking, in contrast to activity in noradrenergic and serotonergic neurons, which is more tightly coupled to the maintenance of muscle tone in waking and its loss in REM sleep and cataplexy.

Citing Articles

Histaminergic System Activity in the Central Nervous System: The Role in Neurodevelopmental and Neurodegenerative Disorders.

Szukiewicz D Int J Mol Sci. 2024; 25(18).

PMID: 39337347 PMC: 11432521. DOI: 10.3390/ijms25189859.

Homeostatic regulation of rapid eye movement sleep by the preoptic area of the hypothalamus.

Maurer J, Lin A, Jin X, Hong J, Sathi N, Cardis R Elife. 2024; 12.

PMID: 38884573 PMC: 11182646. DOI: 10.7554/eLife.92095.

Most dynorphin neurons in the zona incerta-perifornical area are active in waking relative to non-rapid-eye movement and rapid-eye movement sleep.

Shiromani P, Vidal-Ortiz A Sleep. 2024; 47(5).

PMID: 38447008 PMC: 11494376. DOI: 10.1093/sleep/zsae065.

Deficiency of orexin signaling during sleep is involved in abnormal REM sleep architecture in narcolepsy.

Ito H, Fukatsu N, Rahaman S, Mukai Y, Izawa S, Ono D Proc Natl Acad Sci U S A. 2023; 120(41):e2301951120.

PMID: 37796986 PMC: 10576136. DOI: 10.1073/pnas.2301951120.

Homeostatic regulation of REM sleep by the preoptic area of the hypothalamus.

Maurer J, Lin A, Jin X, Hong J, Sathi N, Cardis R bioRxiv. 2023; .

PMID: 37662417 PMC: 10473649. DOI: 10.1101/2023.08.22.554341.

References

Aston-Jones G, Bloom F . Activity of norepinephrine-containing locus coeruleus neurons in behaving rats anticipates fluctuations in the sleep-waking cycle. J Neurosci. 1981; 1(8):876-86. PMC: 6564235. View

Peyron C, Faraco J, Rogers W, Ripley B, Overeem S, Charnay Y . A mutation in a case of early onset narcolepsy and a generalized absence of hypocretin peptides in human narcoleptic brains. Nat Med. 2000; 6(9):991-7. DOI: 10.1038/79690. View

Gulyani S, Wu M, Nienhuis R, John J, Siegel J . Cataplexy-related neurons in the amygdala of the narcoleptic dog. Neuroscience. 2002; 112(2):355-65. PMC: 8789328. DOI: 10.1016/s0306-4522(02)00089-1. View

Lantos T, Gorcs T, Palkovits M . Immunohistochemical mapping of neuropeptides in the premamillary region of the hypothalamus in rats. Brain Res Brain Res Rev. 1995; 20(2):209-49. DOI: 10.1016/0165-0173(94)00013-f. View

Andre P, dAscanio P, Ioffe M, Pompeiano O . Microinjections of vasopressin in the locus coeruleus complex affect posture and vestibulospinal reflexes in decerebrate cats. Pflugers Arch. 1992; 420(3-4):376-88. DOI: 10.1007/BF00374473. View

Steininger T, Alam M, Gong H, Szymusiak R, McGinty D . Sleep-waking discharge of neurons in the posterior lateral hypothalamus of the albino rat. Brain Res. 1999; 840(1-2):138-47. DOI: 10.1016/s0006-8993(99)01648-0. View

Bourgin P, Huitron-Resendiz S, Spier A, Fabre V, Morte B, Criado J . Hypocretin-1 modulates rapid eye movement sleep through activation of locus coeruleus neurons. J Neurosci. 2000; 20(20):7760-5. PMC: 6772862. View

Vanni-Mercier G, Gigout S, Debilly G, Lin J . Waking selective neurons in the posterior hypothalamus and their response to histamine H3-receptor ligands: an electrophysiological study in freely moving cats. Behav Brain Res. 2003; 144(1-2):227-41. DOI: 10.1016/s0166-4328(03)00091-3. View

Wu M, Gulyani S, Yau E, Mignot E, Phan B, Siegel J . Locus coeruleus neurons: cessation of activity during cataplexy. Neuroscience. 1999; 91(4):1389-99. PMC: 8848839. DOI: 10.1016/s0306-4522(98)00600-9. View

10.

Horvath T, Peyron C, Diano S, Ivanov A, Aston-Jones G, Kilduff T . Hypocretin (orexin) activation and synaptic innervation of the locus coeruleus noradrenergic system. J Comp Neurol. 1999; 415(2):145-59. View

11.

Kushida C, Baker T, Dement W . Electroencephalographic correlates of cataplectic attacks in narcoleptic canines. Electroencephalogr Clin Neurophysiol. 1985; 61(1):61-70. DOI: 10.1016/0013-4694(85)91073-9. View

12.

Kohyama J, Lai Y, Siegel J . Inactivation of the pons blocks medullary-induced muscle tone suppression in the decerebrate cat. Sleep. 2001; 21(7):695-9. PMC: 8848857. DOI: 10.1093/sleep/21.7.695. View

13.

Boehmer L, Wu M, John J, Siegel J . Treatment with immunosuppressive and anti-inflammatory agents delays onset of canine genetic narcolepsy and reduces symptom severity. Exp Neurol. 2004; 188(2):292-9. PMC: 8788643. DOI: 10.1016/j.expneurol.2004.04.006. View

14.

Aldrich M . Diagnostic aspects of narcolepsy. Neurology. 1998; 50(2 Suppl 1):S2-7. DOI: 10.1212/wnl.50.2_suppl_1.s2. View

15.

Siegel J, Nienhuis R, Fahringer H, Paul R, Shiromani P, Dement W . Neuronal activity in narcolepsy: identification of cataplexy-related cells in the medial medulla. Science. 1991; 252(5010):1315-8. PMC: 8784798. DOI: 10.1126/science.1925546. View

16.

Nishino S, Sakurai E, Nevsimalova S, Yoshida Y, Watanabe T, Yanai K . Decreased CSF histamine in narcolepsy with and without low CSF hypocretin-1 in comparison to healthy controls. Sleep. 2009; 32(2):175-80. PMC: 2635581. DOI: 10.1093/sleep/32.2.175. View

17.

Lin J, Sakai K, Jouvet M . Hypothalamo-preoptic histaminergic projections in sleep-wake control in the cat. Eur J Neurosci. 1994; 6(4):618-25. DOI: 10.1111/j.1460-9568.1994.tb00306.x. View

18.

Kodama T, Lai Y, Siegel J . Changes in inhibitory amino acid release linked to pontine-induced atonia: an in vivo microdialysis study. J Neurosci. 2003; 23(4):1548-54. PMC: 6742274. View

19.

Siegel J, Nienhuis R, Fahringer H, Chiu C, Dement W, Mignot E . Activity of medial mesopontine units during cataplexy and sleep-waking states in the narcoleptic dog. J Neurosci. 1992; 12(5):1640-6. PMC: 6575889. View

20.

Wu M, John J, Boehmer L, Yau D, Nguyen G, Siegel J . Activity of dorsal raphe cells across the sleep-waking cycle and during cataplexy in narcoleptic dogs. J Physiol. 2003; 554(Pt 1):202-15. PMC: 1664742. DOI: 10.1113/jphysiol.2003.052134. View