Intrinsic and extrinsic cues regulate the daily profile of mouse lateral habenula neuronal activity

Journal of Physiology

Volumn 592, Issue 22, 2014, Pages 5025-5045

  Sakhi, Kanwal ^a   Wegner, Sven ^a   Belle, Mino D C ^a   Howarth, Michael ^a   Delagrange, Philippe ^b   Brown, Timothy M ^a   Piggins, Hugh D ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b INSTITUT DE RECHERCHES SERVIER   (France)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; CRY1 PROTEIN, MOUSE; CRY2 PROTEIN, MOUSE; CRYPTOCHROME; GASTROINTESTINAL HORMONE; NEUROPEPTIDE; PROK2 PROTEIN, MOUSE;

4 AMINOBUTYRIC ACID RELEASE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASSOCIATION; BRAIN SLICE; CIRCADIAN RHYTHM; CONTROLLED STUDY; EPITHALAMUS; FEMALE; ILLUMINATION; IN VITRO STUDY; IN VIVO STUDY; LATERAL HABENULA; MALE; MOLECULAR CLOCK; MOUSE; NERVE CELL; NERVE POTENTIAL; NONHUMAN; POLYSYNAPTIC REFLEX; PRIORITY JOURNAL; RETINA; SUPRACHIASMATIC NUCLEUS; VISUAL STIMULATION; ACTION POTENTIAL; ANIMAL; CYTOLOGY; GENETICS; HABENULA; METABOLISM; PHYSIOLOGY;

ACTION POTENTIALS; ANIMALS; CIRCADIAN RHYTHM; CRYPTOCHROMES; CUES; GAMMA-AMINOBUTYRIC ACID; GASTROINTESTINAL HORMONES; HABENULA; MICE; NEURONS; NEUROPEPTIDES;

EID: 84925379702     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2014.280065     Document Type: Article

References (71)

1. Abe M, Herzog ED, Yamazaki S, Straume M, Tei H, Sakaki Y, Menaker M & Block GD (2002). Circadian rhythms in isolated brain regions. J Neurosci 22, 350-356.
2. Aizawa H, Cui W, Tanaka K & Okamoto H (2013). Hyperactivation of the habenula as a link between depression and sleep disturbance. Front Hum Neurosci 7, 826.
3. Aizawa H, Kobayashi M, Tanaka S, Fukai T & Okamoto H (2012). Molecular characterization of the subnuclei in rat habenula. J Comp Neurol 520, 4051-4066.
4. Albrecht U (2013). Circadian clocks and mood-related behaviors. Hndbk Exp Pharmacol 217, 227-239.
5. Andres KH, von During M & Veh RW (1999). Subnuclear organization of the rat habenular complexes. J Comp Neurol 407, 130-150.
6. Barrot M, Sesack SR, Georges F, Pistis M, Hong S & Jhou TC (2012). Braking dopamine systems: a new GABA master structure for mesolimbic and nigrostriatal functions. J Neurosci 32, 14094-14101.
7. Belle MD, Diekman CO, Forger DB & Piggins HD (2009). Daily electrical silencing in the mammalian circadian clock. Science 326, 281-284.
8. Belle MD, Hughes AT, Bechtold DA, Cunningham P, Pierucci M, Burdakov D & Piggins HD (2014). Acute suppressive and long-term phase modulation actions of orexin on the mammalian circadian clock. J Neurosci 34, 3607-3621.
9. Bernard R & Veh RW (2012). Individual neurons in the rat lateral habenular complex project mostly to the dopaminergic ventral tegmental area or to the serotonergic raphe nuclei. J Comp Neurol 520, 2545-2558.
10. Bianco IH & Wilson SW(2009). The habenular nuclei: a conserved asymmetric relay station in the vertebrate brain. Phil Trans R Soc Lond B Biol Sci 364, 1005-1020.
11. Brinschwitz K, Dittgen A, Madai VI, Lommel R, Geisler S & Veh RW (2010). Glutamatergic axons from the lateral habenula mainly terminate on GABAergic neurons of the ventral midbrain. Neuroscience 168, 463-476.
12. Brown TM, Allen AE,Wynne J, Paul DL, Piggins HD & Lucas RJ (2011b). Visual responses in the lateral geniculate evoked by Cx36-independent rod pathways. Vision Res 51, 280-287.
13. Brown TM, Banks JR & Piggins HD (2006). A novel suction electrode recording technique for monitoring circadian rhythms in single and multiunit discharge from brain slices. J Neurosci Methods 156, 173-181.
14. Brown TM & Piggins HD (2007). Electrophysiology of the suprachiasmatic circadian clock. Prog Neurobiol 82, 229-255.
15. Brown TM, Wynne J, Piggins HD & Lucas RJ (2011b). Multiple hypothalamic cell populations encoding distinct visual information. J Physiol 589, 1173-1194.
16. Chang SY & Kim U (2004). Ionic mechanism of long-lasting discharges of action potentials triggered by membrane hyperpolarization in the medial lateral habenula. J Neurosci 24, 2172-2181.
17. Cheng MY, Bullock CM, Li C, Lee AG, Bermak JC, Belluzzi J, Weaver DR, Leslie FM & Zhou QY (2002). Prokineticin 2 transmits the behavioural circadian rhythm of the suprachiasmatic nucleus. Nature 417, 405-410.
18. Cottrell GT, Zhou QY & Ferguson AV (2004). Prokineticin 2 modulates the excitability of subfornical organ neurons. J Neurosci 24, 2375-2379.
19. Cutler DJ, Haraura M, Reed HE, Shen S, Sheward WJ, Morrison CF, Marston HM, Harmar AJ & Piggins HD (2003). The mouse VPAC2 receptor confers suprachiasmatic nuclei cellular rhythmicity and responsiveness to vasoactive intestinal polypeptide in vitro. Eur J Neurosci 17, 197-204.
20. Dibner C, Schibler U & Albrecht U (2010). The mammalian circadian timing system: organization and coordination of central and peripheral clocks. Ann Rev Physiol 72, 517-549.
21. Diekman CO, Belle MD, Irwin RP, Allen CN, Piggins HD & Forger DB (2013). Causes and consequences of hyperexcitation in central clock neurons. PLoS Comput Biol 9, e1003196.
22. Earley CJ, Kuwabara H,Wong DF, Gamaldo C, Salas RE, Brasic JR, Ravert HT, Dannals RF & Allen RP (2013). Increased synaptic dopamine in the putamen in restless legs syndrome. Sleep 36, 51-57.
23. Enezi J, Revell V, Brown T,Wynne J, Schlangen L & Lucas R (2011). A 'melanopic' spectral efficiency function predicts the sensitivity of melanopsin photoreceptors to polychromatic lights. J Biol Rhythms 26, 314-323.
24. Geisler S, Andres KH & Veh RW (2003). Morphologic and cytochemical criteria for the identification and delineation of individual subnuclei within the lateral habenular complex of the rat. J Comp Neurol 458, 78-97.
25. Geisler S & Trimble M (2008). The lateral habenula: no longer neglected. CNS Spectr 13, 484-489.
26. Goutagny R, Loureiro M, Jackson J, Chaumont J,Williams S, Isope P, Kelche C, Cassel JC & Lecourtier L (2013). Interactions between the lateral habenula and the hippocampus: implication for spatial memory processes. Neuropsychopharmacology 38, 2418-2426.
27. Granados-Fuentes D, Saxena MT, Prolo LM, Aton SJ & Herzog ED (2004). Olfactory bulb neurons express functional, entrainable circadian rhythms. Eur J Neurosci 19, 898-906.
28. Gruber C, Kahl A, Lebenheim L, Kowski A, Dittgen A & Veh RW (2007). Dopaminergic projections from the VTA substantially contribute to the mesohabenular pathway in the rat. Neurosci Lett 427, 165-170.
29. Guilding C, Hughes AT, Brown TM, Namvar S & Piggins HD (2009). A riot of rhythms: neuronal and glial circadian oscillators in the mediobasal hypothalamus. Mol Brain 2, 28.
30. Guilding C, Hughes AT & Piggins HD (2010). Circadian oscillators in the epithalamus. Neuroscience 169, 1630-1639.
31. Guilding C & Piggins HD (2007). Challenging the omnipotence of the suprachiasmatic timekeeper: are circadian oscillators present throughout the mammalian brain? Eur J Neurosci 25, 3195-3216.
32. Hattar S, Kumar M, Park A, Tong P, Tung J, Yau KW & Berson DM (2006). Central projections of melanopsin-expressing retinal ganglion cells in the mouse. J Comp Neurol 497, 326-349.
33. Herkenham M & Nauta WJ (1977). Afferent connections of the habenular nuclei in the rat. A horseradish peroxidase study, with a note on the fibre-of-passage problem. J Comp Neurol 173, 123-146.
34. Herzog ED, Takahashi JS & Block GD (1998). Clock controls circadian period in isolated suprachiasmatic nucleus neurons. Nat Neurosci 1, 708-713.
35. Hikosaka O (2010). The habenula: from stress evasion to value-based decision-making. Nat Rev Neurosci 11, 503-513.
36. Inouye ST & Kawamura H (1979). Persistence of circadian rhythmicity in a mammalian hypothalamic 'island' containing the suprachiasmatic nucleus. Proc Natl Acad Sci USA 76, 5962-5966.
37. Jalewa J, Joshi A, McGinnity TM, Prasad G, Wong-Lin K & Holscher C (2014). Neural circuit interactions between the dorsal raphe nucleus and the lateral hypothalamus: an experimental and computational study. PloS ONE 9, e88003.
38. Jesuthasan S (2012). Fear, anxiety, and control in the zebrafish. Dev Neurobiol 72, 395-403.
39. Jhou TC, Geisler S, Marinelli M, Degarmo BA & Zahm DS (2009). The mesopontine rostromedial tegmental nucleus: a structure targeted by the lateral habenula that projects to the ventral tegmental area of Tsai and substantia nigra compacta. J Comp Neurol 513, 566-596.
40. Kim U & Chang SY (2005). Dendritic morphology, local circuitry, and intrinsic electrophysiology of neurons in the rat medial and lateral habenular nuclei of the epithalamus. J Comp Neurol 483, 236-250.
41. Kowski AB, Geisler S, Krauss M & Veh RW (2008). Differential projections from subfields in the lateral preoptic area to the lateral habenular complex of the rat. J Comp Neurol 507, 1465-1478.
42. Kowski AB, Veh RW & Weiss T (2009). Dopaminergic activation excites rat lateral habenular neurons in vivo. Neuroscience 161, 1154-1165.
43. Kuhlman SJ & McMahon DG (2004). Rhythmic regulation of membrane potential and potassium current persists in SCN neurons in the absence of environmental input. Eur J Neurosci 20, 1113-1117.
44. Kuhlman SJ, Quintero JE & McMahon DG (2000). GFP fluorescence reports Period 1 circadian gene regulation in the mammalian biological clock. Neuroreport 11, 1479-1482.
45. Lammel S, Lim BK, Ran C, Huang KW, Betley MJ, Tye KM, Deisseroth K & Malenka RC (2012). Input-specific control of reward and aversion in the ventral tegmental area. Nature 491, 212-217.
46. Leslie FM, Mojica CY & Reynaga DD (2013). Nicotinic receptors in addiction pathways. Mol Pharmacol 83, 753-758.
47. Li K, Zhou T, Liao L, Yang Z,Wong C, Henn F, Malinow R, Yates JR 3rd & Hu H (2013). ßCaMKII in lateral habenula mediates core symptoms of depression. Science 341, 1016-1020.
48. Lucas RJ, Peirson SN, Berson DM, Brown TM, Cooper HM, Czeisler CA, Figueiro MG, Gamlin PD, Lockley SW, O'Hagan JB, Price LL, Provencio I, Skene DJ & Brainard GC (2014). Measuring and using light in the melanopsin age. Trends Neurosci 37, 1-9.
49. McCarthy MJ & Welsh DK (2012). Cellular circadian clocks in mood disorders. J Biol Rhythms 27, 339-352.
50. Mendoza J & Challet E (2009). Brain clocks: from the suprachiasmatic nuclei to a cerebral network. Neuroscientist 15, 477-488.
51. Moore RY, Weis R & Moga MM (2000). Efferent projections of the intergeniculate leaflet and the ventral lateral geniculate nucleus in the rat. J Comp Neurol 420, 398-418.
52. Morin LP & Studholme KM (2014). Retinofugal projections in the mouse. J Comp Neurol 522, 3733-3753.
53. Paul MJ, Indic P & SchwartzWJ (2011). A role for the habenula in the regulation of locomotor activity cycles. Eur J Neurosci 34, 478-488.
54. Paxinos G & Franklin KBJ (2001). The mouse brain in stereotaxic coordinates. Academic Press, San Diego.
55. Raman IM, Gustafson AE & Padgett D (2000). Ionic currents and spontaneous firing in neurons isolated from the cerebellar nuclei. J Neurosci 20, 9004-9016.
56. Ren P, Zhang H, Qiu F, Liu YQ, Gu H, O'Dowd DK, Zhou QY & Hu WP (2011). Prokineticin 2 regulates the electrical activity of rat suprachiasmatic nuclei neurons. PloS ONE 6, e20263.
57. A antagonist pentylenetetrazole. PloS ONE 8, e72433.
58. Sakhi K, Belle MD, Gossan N, Delagrange P & Piggins HD (2014). Daily variation in the electrophysiological activity of mouse medial habenula neurones. J Physiol 592, 587-603.
59. Sartorius A, Kiening KL, Kirsch P, von Gall CC, Haberkorn U, Unterberg AW, Henn FA & Meyer-Lindenberg A (2010). Remission of major depression under deep brain stimulation of the lateral habenula in a therapy-refractory patient. Biol Psychiat 67, e9-e11.
60. Scott FF, Belle MD, Delagrange P & Piggins HD (2010). Electrophysiological effects of melatonin on mouse Per1 and non-Per1 suprachiasmatic nuclei neurones in vitro. J Neuroendocrinol 22, 1148-1156.
61. Sego C, Goncalves L, Lima L, Furigo IC, Donato J, Jr & Metzger M (2014). Lateral habenula and the rostromedial tegmental nucleus innervate neurochemically distinct subdivisions of the dorsal raphe nucleus in the rat. J Comp Neurol 522, 1454-1484.
62. Shieh KR (2003). Distribution of the rhythm-related genes rPERIOD1, rPERIOD2, and rCLOCK, in the rat brain. Neuroscience 118, 831-843.
63. Sutherland RJ (1982). The dorsal diencephalic conduction system: a review of the anatomy and functions of the habenular complex. Neurosci Biobehav Rev 6, 1-13.
64. Tavakoli-Nezhad M & Schwartz WJ (2006). Hamsters running on time: is the lateral habenula a part of the clock? Chronobiol Int 23, 217-224.
65. van der Horst GT, Muijtjens M, Kobayashi K, Takano R, Kanno S, Takao M, deWit J, Verkerk A, Eker AP, van Leenen D, Buijs R, Bootsma D, Hoeijmakers JH & Yasui A (1999). Mammalian Cry1 and Cry2 are essential for maintenance of circadian rhythms. Nature 398, 627-630.
66. van Oosterhout F, Lucassen EA, Houben T, vanderLeest HT, Antle MC & Meijer JH (2012). Amplitude of the SCN clock enhanced by the behavioral activity rhythm. PloS ONE 7, e39693.
67. Webb IC, Baltazar RM,Wang X, Pitchers KK, Coolen LM & Lehman MN (2009). Diurnal variations in natural and drug reward, mesolimbic tyrosine hydroxylase, and clock gene expression in the male rat. J Biol Rhythms 24, 465-476.
68. Weiss T & Veh RW (2011). Morphological and electrophysiological characteristics of neurons within identified subnuclei of the lateral habenula in rat brain slices. Neuroscience 172, 74-93.
69. Yamaguchi S, Mitsui S, Miyake S, Yan L, Onishi H, Yagita K, Suzuki M, Shibata S, Kobayashi M & Okamura H (2000). The 5' upstream region of mPer1 gene contains two promoters and is responsible for circadian oscillation. Curr Biol 10, 873-876.
70. Zhang C, Truong KK & Zhou QY (2009). Efferent projections of prokineticin 2 expressing neurons in the mouse suprachiasmatic nucleus. PloS ONE 4, e7151.
71. Zhao H & Rusak B (2005). Circadian firing-rate rhythms and light responses of rat habenular nucleus neurons in vivo and in vitro. Neuroscience 132, 519-528.