The cholinergic agonist carbachol increases the frequency of spontaneous GABAergic synaptic currents in dorsal raphe serotonergic neurons in the mouse

Neuroscience

Volumn 258, Issue , 2014, Pages 62-73

  Yang, C ^a   Brown, R E ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

GAD67 GFP knock in mice; Patch clamp; Presynaptic modulation; Sleep; Ventrolateral periaqueductal gray

Indexed keywords

CARBACHOL; SEROTONIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CHOLINERGIC NERVE CELL; CONTROLLED STUDY; DORSAL RAPHE NUCLEUS; FEMALE; GABAERGIC SYSTEM; IN VITRO STUDY; INHIBITORY POSTSYNAPTIC POTENTIAL; LATERAL RETICULAR NUCLEUS; MALE; MOUSE; NERVE CELL STIMULATION; NONHUMAN; PERIAQUEDUCTAL GRAY MATTER; PRIORITY JOURNAL; SEROTONINERGIC NERVE CELL; SYNAPSE;

(2R)-AMINO-5-PHOSPHONOVALERIC ACID; 4-(2-HYDROXYETHYL)PIPERAZINE-1-ETHANESULFONIC ACID; 5-HT; 6,7-DINITROQUINOXALINE-2,3-DIONE; ACSF; ACTION POTENTIAL; AFTERHYPERPOLARIZATION; AHP; ANALYSIS OF VARIANCE; ANOVA; AP; AP5; ARTIFICIAL CEREBROSPINAL FLUID; DECUSSATION OF THE SUPERIOR CEREBELLAR PEDUNCLE; DNQX; DORSAL RAPHE NUCLEUS; DRN; EGTA; ETHYLENE GLYCOL TETRAACETIC ACID; GAD67-GFP KNOCK-IN MICE; HEPES; LATERODORSAL TEGMENTUM; LDT; MINIATURE INHIBITORY POSTSYNAPTIC CURRENTS; MIPSCS; N-METHYL-D-ASPARTATE; NMDA; PATCH-CLAMP; PEDUNCULOPONTINE TEGMENTUM; PGO; PNO; PONTINE NUCLEUS, PARS ORALIS; PONTO-GENICULO-OCCIPITAL; PPT; PRESYNAPTIC MODULATION; RAPID-EYE-MOVEMENT; REM; RESTING MEMBRANE POTENTIAL; RMP; SEROTONIN; SIPSCS; SLEEP; SPONTANEOUS INHIBITORY POSTSYNAPTIC CURRENTS; SUBC; SUBCOERULEUS; TETRODOTOXIN; TTX; VENTROLATERAL PERIAQUEDUCTAL GRAY; VLPAG; XSCP;

ANIMALS; CARBACHOL; CHOLINERGIC AGONISTS; FEMALE; GABAERGIC NEURONS; GENE KNOCK-IN TECHNIQUES; INHIBITORY POSTSYNAPTIC POTENTIALS; MALE; MICE; MICE, TRANSGENIC; MUSCARINIC ANTAGONISTS; NICOTINIC ANTAGONISTS; PERIAQUEDUCTAL GRAY; RAPHE NUCLEI; RECEPTORS, MUSCARINIC; RECEPTORS, NICOTINIC; SEROTONERGIC NEURONS; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 84890303314     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2013.11.005     Document Type: Article

References (55)

1. Baraban J.M., Aghajanian G.K. Suppression of firing activity of 5-HT neurons in the dorsal raphe by alpha-adrenoceptor antagonists. Neuropharmacology 1980, 19:355-363.
2. Brown R.E., Sergeeva O.A., Eriksson K.S., Haas H.L. Convergent excitation of dorsal raphe serotonin neurons by multiple arousal systems (orexin/hypocretin, histamine and noradrenaline). J Neurosci 2002, 22:8850-8859.
3. Brown R.E., McKenna J.T., Winston S., Basheer R., Yanagawa Y., Thakkar M.M., McCarley R.W. Characterization of GABAergic neurons in rapid-eye-movement sleep controlling regions of the brainstem reticular formation in GAD67-green fluorescent protein knock-in mice. Eur J Neurosci 2008, 27:352-363.
4. Brown R.E., Basheer R., McKenna J.T., Strecker R.E., McCarley R.W. Control of sleep and wakefulness. Physiol Rev 2012, 92:1087-1187.
5. Chang B., Daniele C.A., Gallagher K., Madonia M., Mitchum R.D., Barrett L., Vezina P., McGehee D.S. Nicotinic excitation of serotonergic projections from dorsal raphe to the nucleus accumbens. J Neurophysiol 2011, 106:801-808.
6. Chen L., McKenna J.T., Leonard M.Z., Yanagawa Y., McCarley R.W. GAD67-GFP knock-in mice have normal sleep-wake patterns and sleep homeostasis. Neuroreport 2010, 21:216-220.
7. El Mansari M., Sakai K., Jouvet M. Unitary characteristics of presumptive cholinergic tegmental neurons during the sleep-waking cycle in freely moving cats. Exp Brain Res 1989, 76:519-529.
8. Franklin K.B.J., Paxinos G. The mouse brain in stereotaxic coordinates 2008, Academic Press, New York. third edition.
9. Galindo-Charles L., Hernandez-Lopez S., Galarraga E., Tapia D., Bargas J., Garduno J., Frias-Dominguez C., Drucker-Colin R., Mihailescu S. Serotoninergic dorsal raphe neurons possess functional postsynaptic nicotinic acetylcholine receptors. Synapse 2008, 62:601-615.
10. Garduño J., Galindo-Charles L., Jiménez-Rodríguez J., Galarraga E., Tapia D., Mihailescu S., Hernandez-Lopez S. Presynaptic α4β2 nicotinic acetylcholine receptors increase glutamate release and serotonin neuron excitability in the dorsal raphe nucleus. J Neurosci 2012, 32:15148-15157.
11. Gervasoni D., Peyron C., Rampon C., Barbagli B., Chouvet G., Urbain N., Fort P., Luppi P.H. Role and origin of the GABAergic innervations of dorsal raphe serotonergic neurons. J Neurosci 2000, 20:4217-4225.
12. Heym J., Trulson M.E., Jacobs B.L. Raphe unit activity in freely moving cats: effects of phasic auditory and visual stimuli. Brain Res 1982, 232:29-39.
13. Hobson J.A., McCarley R.W., Wyzinski P.W. Sleep cycle oscillation: reciprocal discharge by two brainstem neuronal groups. Science 1975, 189:55-58.
14. Hoshino K., Pompeiano O. Tonic inhibition of dorsal pontine neurons during the postural atonia produced by an anticholinesterase in the decerebrate cat. Arch Ital Biol 1976, 114:310-334.
15. Jacobs B.L., Azmitia E.C. Structure and function of the brain serotonin system. Physiol Rev 1992, 72:165-229.
16. Jouvet-Mounier D., Astic L. Study of the course of sleep in the young rat during the 1st postnatal month. C R Seances Soc Biol Fil 1968, 162:119-123.
17. Kohlmeier K.A., Vardar B., Christensen M.H. Γ-Hydroxybutyric acid induces actions via the GABAB receptor in arousal and motor control-related nuclei: Implications for therapeutic actions in behavioral state disorders. Neuroscience 2013, 248C:261-277.
18. Koyama Y., Jodo E., Kayama Y. Sensory responsiveness of "broad-spike" neurons in the laterodorsal tegmental nucleus, locus coeruleus and dorsal raphe of awake rats: implications for cholinergic and monoaminergic neuron-specific responses. Neuroscience 1994, 63:1021-1031.
19. Kumar A. Carbachol-induced long-term synaptic depression is enhanced during senescence at hippocampal CA3-CA1 synapses. J Neurophysiol 2010, 104:607-616.
20. Kumari A., Sreetama S., Mohanakumar K.P. Atropine, a muscarinic cholinergic receptor antagonist increases serotonin, but not dopamine levels in discrete brain regions of mice. Neurosci Lett 2007, 423:100-103.
21. Leonard C.S., Llinás R. Serotonergic and cholinergic inhibition of mesopontine cholinergic neurons controlling REM sleep: an in vitro electrophysiological study. Neuroscience 1994, 59:309-330.
22. Li X., Rainnie D.G., McCarley R.W., Greene R.W. Presynaptic nicotinic receptors facilitate monoaminergic transmission. J Neurosci 1998, 18:1904-1912.
23. Liu R.J., van den Pol A.N., Aghajanian G.K. Hypocretins (orexins) regulate serotonin neurons in the dorsal raphe nucleus by excitatory direct and inhibitory indirect actions. J Neurosci 2002, 22:9453-9464.
24. Luebke J.I., Greene R.W., Semba K., Kamondi A., McCarley R.W., Reiner P.B. Serotonin hyperpolarizes cholinergic low-threshold burst neurons in the rat laterodorsal tegmental nucleus in vitro. Proc Natl Acad Sci U S A 1992, 89:743-747.
25. Luppi P.H., Gervasoni D., Verret L., Goutagny R., Peyron C., Salvert D., Leger L., Fort P. Paradoxical (REM) sleep genesis: the switch from an aminergic-cholinergic to a GABAergic-glutamatergic hypothesis. J Physiol Paris 2006, 100:271-283.
26. Lydic R., McCarley R.W., Hobson J.A. The time-course of dorsal raphe discharge, PGO waves, and muscle tone averaged across multiple sleep cycles. Brain Res 1983, 274:365-370.
27. Mallick B.N., Singh A., Khanday M.A. Activation of inactivation process initiates rapid eye movement sleep. Prog Neurobiol 2012, 97:259-276.
28. Maloney K.J., Mainville L., Jones B.E. C-Fos expression in GABAergic, serotonergic, and other neurons of the pontomedullary reticular formation and raphe after paradoxical sleep deprivation and recovery. J Neurosci 2000, 20:4669-4679.
29. McCarley R.W. Neurobiology of REM and NREM sleep. Sleep Med 2007, 8:302-330.
30. McCarley R.W., Hobson J.A. Neuronal excitability modulation over the sleep cycle: a structural and mathematical model. Science 1975, 189:58-60.
31. McGinty D.J., Harper R.M. Dorsal raphe neurons: depression of firing during sleep in cats. Brain Res 1976, 101:569-575.
32. McKenna JT, Albu SM, Winston S, Yanagawa Y, McCarley RW, Brown RE (2010) Investigation of GABAergic brainstem projections to the dorsal raphe nucleus in GAD67-GFP knock-in mice: possible implications for REM sleep regulation. Associated Professional Sleep Societies 24th Annual Meeting, Abs:0136.
33. McKenna J.T., Yang C., Franciosi S., Winston S., Abarr K.K., Rigby M.S., Yanagawa Y., McCarley R.W., Brown R.E. Distribution and intrinsic membrane properties of basal forebrain GABAergic and parvalbumin neurons in the mouse. J Comp Neurol 2013, 521:1225-1250.
34. McNally J.M., McCarley R.W., McKenna J.T., Yanagawa Y., Brown R.E. Complex receptor mediation of acute ketamine application on in vitro gamma oscillations in mouse prefrontal cortex: modeling gamma band oscillation abnormalities in schizophrenia. Neuroscience 2011, 199:51-63.
35. Mihailescu S., Palomero-Rivero M., Meade-Huerta P., Maza-Flores A., Drucker-Colín R. Effects of nicotine and mecamylamine on rat dorsal raphe neurons. Eur J Pharmacol 1998, 360:31-36.
36. Mihailescu S., Guzmán-Marín R., Drucker-Colín R. Nicotine stimulation of dorsal raphe neurons: effects on laterodorsal and pedunculopontine neurons. Eur Neuropsychopharmacol 2001, 11:359-366.
37. Mihailescu S., Guzmán-Marín R., Domínguez Mdel C., Drucker-Colín R. Mechanisms of nicotine actions on dorsal raphe serotoninergic neurons. Eur J Pharmacol 2002, 452(1):77-82.
38. Monti J.M. The structure of the dorsal raphe nucleus and its relevance to the regulation of sleep and wakefulness. Sleep Med Rev 2010, 14:307-317.
39. Nitz D.A., Siegel J.M. Inhibitory amino acid neurotransmission in the dorsal raphe nucleus during sleep/wake states. Am J Physiol 1997, 273:R451-R454.
40. Peyron C., Petit J.M., Rampon C., Jouvet M., Luppi P.H. Forebrain afferents to the rat dorsal raphe nucleus demonstrated by retrograde and anterograde tracing methods. Neuroscience 1998, 82:443-468.
41. Rye D.B., Saper C.B., Lee H.J., Wainer B.H. Pedunculopontine tegmental nucleus of the rat: cytoarchitecture, cytochemistry, and some extrapyramidal connections of the mesopontine tegmentum. J Comp Neurol 1987, 259:483-528.
42. Sakai K. Discharge properties of presumed cholinergic and noncholinergic laterodorsal tegmental neurons related to cortical activation in non-anesthetized mice. Neuroscience 2012, 224:172-190.
43. Sakai K., Crochet S. Serotonergic dorsal raphe neurons cease firing by disfacilitation during paradoxical sleep. Neuroreport 2000, 11:3237-3241.
44. Sakai K., Crochet S. Differentiation of presumed serotonergic dorsal raphe neurons in relation to behavior and wake-sleep states. Neuroscience 2001, 104:1141-1155.
45. Sapin E., Lapray D., Bérod A., Goutagny R., Léger L., Ravassard P., Clément O., Hanriot L., Fort P., Luppi P.H. Localization of the brainstem GABAergic neurons controlling paradoxical (REM) sleep. PLoS One 2009, 4:e4272.
46. Simon C., Kezunovic N., Williams D.K., Urbano F.J., Garcia-Rill E. Cholinergic and glutamatergic agonists induce gamma frequency activity in dorsal subcoeruleus nucleus neurons. Am J Physiol Cell Physiol 2011, 301:C327-C335.
47. Stamp J.A., Semba K. Extent of colocalization of serotonin and GABA in the neurons of the rat raphe nuclei. Brain Res 1995, 677:39-49.
48. Steriade M., Datta S., Paré D., Oakson G., Curró Dossi R.C. Neuronal activities in brain-stem cholinergic nuclei related to tonic activation processes in thalamocortical systems. J Neurosci 1990, 10:2541-2559.
49. Tamamaki N., Yanagawa Y., Tomioka R., Miyazaki J., Obata K., Kaneko T. Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67-GFP knock-in mouse. J Comp Neurol 2003, 467:60-79.
50. Thakkar M.M., Strecker R.E., McCarley R.W. Behavioral state control through differential serotonergic inhibition in the mesopontine cholinergic nuclei: a simultaneous unit recording and microdialysis study. J Neurosci 1998, 18:5490-5497.
51. Trulson M.E., Jacobs B.L. Raphe unit activity in freely moving cats: correlation with level of behavioral arousal. Brain Res 1979, 163:135-150.
52. Trulson M.E., Jacobs B.L., Morrison A.R. Raphe unit activity during REM sleep in normal cats and in pontine lesioned cats displaying REM sleep without atonia. Brain Res 1981, 226:75-91.
53. Williams J.A., Comisarow J., Day J., Fibiger H.C., Reiner P.B. State-dependent release of acetylcholine in rat thalamus measured by in vivo microdialysis. J Neurosci 1994, 14:5236-5242.
54. Woolf N.J., Butcher L.L. Cholinergic systems in the rat brain: IV. Descending projections of the pontomesencephalic tegmentum. Brain Res Bull 1989, 23:519-540.
55. Xi M.C., Morales F.R., Chase M.H. Evidence that wakefulness and REM sleep are controlled by a GABAergic pontine mechanism. J Neurophysiol 1999, 82:2015-2019.