Distinct Firing Properties of Vasoactive Intestinal Peptide-Expressing Neurons in the Suprachiasmatic Nucleus

Journal of Biological Rhythms

Volumn 31, Issue 1, 2016, Pages 57-67

  Hermanstyne, Tracey O ^a   Simms, Carrie L ^b   Carrasquillo, Yarimar ^a,c   Herzog, Erik D ^b   Nerbonne, Jeanne M ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WASHINGTON UNIVERSITY   (United States)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

action potential waveforms; circadian rhythms; membrane excitability; rhythmic firing; SCN; VIP neuropeptide

Indexed keywords

VASOACTIVE INTESTINAL POLYPEPTIDE; VASOACTIVE INTESTINAL POLYPEPTIDE RECEPTOR 2;

ACTION POTENTIAL; ANIMAL; CIRCADIAN RHYTHM; CYTOLOGY; GENETICS; METABOLISM; MOUSE; NERVE CELL; PHOTOPERIODICITY; PHYSIOLOGY; SUPRACHIASMATIC NUCLEUS;

ACTION POTENTIALS; ANIMALS; CIRCADIAN RHYTHM; MICE; NEURONS; PHOTOPERIOD; RECEPTORS, VASOACTIVE INTESTINAL PEPTIDE, TYPE II; SUPRACHIASMATIC NUCLEUS; VASOACTIVE INTESTINAL PEPTIDE;

EID: 84954119313     PISSN: 07487304     EISSN: 15524531     Source Type: Journal    
DOI: 10.1177/0748730415619745     Document Type: Article

References (62)

1. An S, Irwin RP, Allen CN, Tsai C, Herzog ED, (2011) Vasoactive intestinal polypeptide requires parallel changes in adenylate cyclase and phospholipase C to entrain circadian rhythms to a predictable phase. J Neurophysiol 105: 2289-2296.
2. An S, Tsai C, Ronecker J, Bayly A, Herzog ED, (2012) Spatiotemporal distribution of vasoactive intestinal polypeptide receptor 2 in mouse suprachiasmatic nucleus. J Comp Neurol 520: 2730-2741.
3. Aton SJ, Block GD, Tei H, Yamazaki S, Herzog ED, (2004) Plasticity of circadian behavior and the suprachiasmatic nucleus following exposure to non-24-hour light cycles. J Biol Rhythms 19: 198-207.
4. Aton SJ, Colwell CS, Harmar AJ, Waschek J, Herzog ED, (2005) Vasoactive intestinal polypeptide mediates circadian rhythmicity and synchrony in mammalian clock neurons. Nat Neurosci 8: 476-483.
5. Ban Y, Shigeyoshi Y, Okamura H, (1997) Development of vasoactive intestinal peptide mRNA rhythm in the rat suprachiasmatic nucleus. J Neurosci 17: 3920-3931.
6. Baranauskas G, Tkatch T, Nagata K, Yeh JZ, Surmeier DJ, (2003) Kv3.4 subunits enhance the repolarizing efficiency of Kv3.1 channels in fast-spiking neurons. Nat Neurosci 6: 258-266.
7. Belle MD, Diekman CO, Forger DB, Piggins HD, (2009) Daily electrical silencing in the mammalian circadian clock. Science 326: 281-284.
8. Brown TM, Colwell CS, Waschek JA, Piggins HD, (2007) Disrupted neuronal activity rhythms in the suprachiasmatic nuclei of vasoactive intestinal polypeptide-deficient mice. J Neurophysiol 97: 2553-2558.
9. Brown TM, Hughes AT, Piggins HD, (2005) Gastrin-releasing peptide promotes suprachiasmatic nuclei cellular rhythmicity in the absence of vasoactive intestinal polypeptide-VPAC2 receptor signaling. J Neurosci 25: 11155-11164.
10. Cloues RK, Sather WA, (2003) Afterhyperpolarization regulates firing rate in neurons of the suprachiasmatic nucleus. J Neurosci 23: 1593-1604.
11. Colwell CS, (2011) Linking neural activity and molecular oscillations in the SCN. Nat Rev Neurosci 12: 553-569.
12. 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.
13. de Jeu M, Hermes M, Pennartz C, (1998) Circadian modulation of membrane properties in slices of rat suprachiasmatic nucleus. Neuroreport 9: 3725-3729.
14. Fan J, Zeng H, Olson DP, Huber KM, Gibson JR, Takahashi JS, (2015) Vasoactive intestinal polypeptide (VIP)-expressing neurons in the suprachiasmatic nucleus provide sparse GABAergic outputs to local neuorns with circadian regulation occurring distal to the opening of postsynaptic GABAA iontropic receptors. J Neurosci 35: 1905-1920.
15. Francl JM, Kaur G, Glass JD, (2010) Regulation of vasoactive intestinal polypeptide release in the suprachiasmatic nucleus circadian clock. Neuroreport 21: 1055-1059.
16. Fukuhara C, Nishiwaki T, Cagampang FR, Inouye ST, (1994) Emergence of VIP rhythmicity following somatostatin depletion in the rat suprachiasmatic nucleus. Brain Res 645: 343-346.
17. Granados-Fuentes D, Norris AJ, Carrasquillo Y, Nerbonne JM, Herzog ED, (2012) I(A) channels encoded by Kv1.4 and Kv4.2 regulate neuronal firing in the suprachiasmatic nucleus and circadian rhythms in locomotor activity. J Neurosci 32: 10045-10052.
18. Green DJ, Gillette R, (1982) Circadian rhythm of firing rate recorded from single cells in the rat suprachiasmatic brain slice. Brain Res 245: 198-200.
19. Harmar AJ, Marston HM, Shen S, Spratt C, West KM, Sheward WJ, Morrison CF, Dorin JR, Piggins HD, Reubi JC, et al. (2002) The VPAC(2) receptor is essential for circadian function in the mouse suprachiasmatic nuclei. Cell 109: 497-508.
20. 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.
21. Herzog ED, Aton SJ, Numano R, Sakaki Y, Tei H, (2004) Temporal precision in the mammalian circadian system: a reliable clock from less reliable neurons. J Biol Rhythms 19: 35-46.
22. Herzog ED, Geusz ME, Khalsa SB, Straume M, Block GD, (1997) Circadian rhythms in mouse suprachiasmatic nucleus explants on multimicroelectrode plates. Brain Res 757: 285-290.
23. Inouye ST, Kawamura H, (1979) Persistence of circadian rhythmicity in a mammalian hypothalamic €island€ containing the suprachiasmatic nucleus. Proc Natl Acad Sci U S A 76: 5962-5966.
24. Itri JN MS, Vansteensel MJ, Meijer JH, Colwell CS, (2005) Fast delayed rectifier potassium current is required for circadian neural activity. Nat Neurosci 8: 7.
25. Jiang ZG, Yang Y, Liu ZP, Allen CN, (1997) Membrane properties and synaptic inputs of suprachiasmatic nucleus neurons in rat brain slices. J Physiol 499 (Pt 1): 141-159.
26. Jobst EE, Allen CN, (2002) Calbindin neurons in the hamster suprachiasmatic nucleus do not exhibit a circadian variation in spontaneous firing rate. Eur J Neurosci 16: 2469-2474.
27. Kalsbeek A, Buijs RM, (2002) Output pathways of the mammalian suprachiasmatic nucleus: coding circadian time by transmitter selection and specific targeting. Cell Tissue Res 309: 109-118.
28. Kawakami F, Okamura H, Tamada Y, Maebayashi Y, Fukui K, Ibata Y, (1997) Loss of day-night differences in VIP mRNA levels in the suprachiasmatic nucleus of aged rats. Neurosci Lett 222: 99-102.
29. Kononenko NI, Dudek FE, (2004) Mechanism of irregular firing of suprachiasmatic nucleus neurons in rat hypothalamic slices. J Neurophysiol 91: 267-273.
30. Kudo T, Loh DH, Kuljis D, Constance C, Colwell CS, (2011) Fast delayed rectifier potassium current: critical for input and output of the circadian system. J Neurosci 31: 2746-2755.
31. Kudo T, Tahara Y, Gamble KL, McMahon DG, Block GD, Colwell CS, (2013) Vasoactive intestinal peptide produces long-lasting changes in neural activity in the suprachiasmatic nucleus. J Neurophysiol 110: 1097-1106.
32. 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.
33. Kuhlman SJ, McMahon DG, (2006) Encoding the ins and outs of circadian pacemaking. J Biol Rhythms 21: 470-481.
34. Kunst M, Tso MC, Ghosh DD, Herzog ED, Nitabach MN, (2015) Rhythmic control of activity and sleep by class B1 GPCRs. Crit Rev Biochem Mol Biol 50: 18-30.
35. Madisen L, Zwingman TA, Sunkin SM, Oh SW, Zariwala HA, Gu H, Ng LL, Palmiter RD, Hawrylycz MJ, Jones AR, et al. (2010) A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat Neurosci 13: 133-140.
36. Maywood ES, Chesham JE, O'Brien JA, Hastings MH, (2011) A diversity of paracrine signals sustains molecular circadian cycling in suprachiasmatic nucleus circuits. Proc Natl Acad Sci U S A 108: 14306-14311.
37. Maywood ES, Reddy AB, Wong GK, O'Neill JS, O'Brien JA, McMahon DG, Harmar AJ, Okamura H, Hastings MH, (2006) Synchronization and maintenance of timekeeping in suprachiasmatic circadian clock cells by neuropeptidergic signaling. Curr Biol 16: 599-605.
38. Meredith AL, Wiler SW, Miller BH, Takahashi JS, Fodor AA, Ruby NF, Aldrich RW, (2006) BK calcium-activated potassium channels regulate circadian behavioral rhythms and pacemaker output. Nat Neurosci 9: 1041-1049.
39. Nakamura W, Honma S, Shirakawa T, Honma K, (2002) Clock mutation lengthens the circadian period without damping rhythms in individual SCN neurons. Nat Neurosci 5: 399-400.
40. Okamoto S, Okamura H, Miyake M, Takahashi Y, Takagi S, Akagi Y, Fukui K, Okamoto H, Ibata Y, (1991) A diurnal variation of vasoactive intestinal peptide (VIP) mRNA under a daily light-dark cycle in the rat suprachiasmatic nucleus. Histochemistry 95: 525-528.
41. Okamura H, Kawakami F, Tamada Y, Geffard M, Nishiwaki T, Ibata Y, Inouye ST, (1995) Circadian change of VIP mRNA in the rat suprachiasmatic nucleus following p-chlorophenylalanine (PCPA) treatment in constant darkness. Brain Res Mol Brain Res 29: 358-364.
42. Pauls S, Foley NC, Foley DK, LeSauter J, Hastings MH, Maywood ES, Silver R, (2014) Differential contributions of intra-cellular and inter-cellular mechanisms to the spatial and temporal architecture of the suprachiasmatic nucleus circadian circuitry in wild-type, cryptochrome-null and vasoactive intestinal peptide receptor 2-null mutant mice. Eur J Neurosci 40: 2528-2540.
43. Pennartz CM, de Jeu MT, Bos NP, Schaap J, Geurtsen AM, (2002) Diurnal modulation of pacemaker potentials and calcium current in the mammalian circadian clock. Nature 416: 286-290.
44. Pennartz CM, de Jeu MT, Geurtsen AM, Sluiter AA, Hermes ML, (1998) Electrophysiological and morphological heterogeneity of neurons in slices of rat suprachiasmatic nucleus. J Physiol 506 (Pt 3): 775-793.
45. Perkins KL, (2006) Cell-attached voltage-clamp and current-clamp recording and stimulation techniques in brain slices. J Neurosci Methods 154: 1-18.
46. Reed HE, Cutler DJ, Brown TM, Brown J, Coen CW, Piggins HD, (2002) Effects of vasoactive intestinal polypeptide on neurones of the rat suprachiasmatic nuclei in vitro. J Neuroendocrinol 14: 639-646.
47. Reed HE, Meyer-Spasche A, Cutler DJ, Coen CW, Piggins HD, (2001) Vasoactive intestinal polypeptide (VIP) phase-shifts the rat suprachiasmatic nucleus clock in vitro. Eur J Neurosci 13: 839-843.
48. Renn SC, Park JH, Rosbash M, Hall JC, Taghert PH, (1999) A pdf neuropeptide gene mutation and ablation of PDF neurons each cause severe abnormalities of behavioral circadian rhythms in Drosophila. Cell 99: 791-802.
49. Romijn HJ, Sluiter AA, Pool CW, Wortel J, Buijs RM, (1997) Evidence from confocal fluorescence microscopy for a dense, reciprocal innervation between AVP-, somatostatin-, VIP/PHI-, GRP-, and VIP/PHI/GRP-immunoreactive neurons in the rat suprachiasmatic nucleus. Eur J Neurosci 9: 2613-2623.
50. Schaap J, Bos NP, de Jeu MT, Geurtsen AM, Meijer JH, Pennartz CM, (1999) Neurons of the rat suprachiasmatic nucleus show a circadian rhythm in membrane properties that is lost during prolonged whole-cell recording. Brain Res 815: 154-166.
51. Shinohara K, Honma S, Katsuno Y, Abe H, Honma K, (1995) Two distinct oscillators in the rat suprachiasmatic nucleus in vitro. Proc Natl Acad Sci U S A 92: 7396-7400.
52. Shinohara K, Tominaga K, Inouye ST, (1998) Luminance-dependent decrease in vasoactive intestinal polypeptide in the rat suprachiasmatic nucleus. Neurosci Lett 251: 21-24.
53. Shinohara K, Tominaga K, Isobe Y, Inouye ST, (1993) Photic regulation of peptides located in the ventrolateral subdivision of the suprachiasmatic nucleus of the rat: daily variations of vasoactive intestinal polypeptide, gastrin-releasing peptide, and neuropeptide Y. J Neurosci 13: 793-800.
54. Stoleru D, Peng Y, Nawathean P, Rosbash M, (2005) A resetting signal between Drosophila pacemakers synchronizes morning and evening activity. Nature 438: 238-242.
55. Takeuchi J, Nagasaki H, Shinohara K, Inouye ST, (1992) A circadian rhythm of somatostatin messenger RNA levels, but not of vasoactive intestinal polypeptide/peptide histidine isoleucine messenger RNA levels in rat suprachiasmatic nucleus. Mol Cell Neurosci 3: 29-35.
56. Taniguchi H, He M, Wu P, Kim S, Paik R, Sugino K, Kvitsiani D, Fu Y, Lu J, Lin Y, et al. (2011) A resource of Cre driver lines for genetic targeting of GABAergic neurons in cerebral cortex. Neuron 71: 995-1013.
57. Wang LY, Gan L, Forsythe ID, Kaczmarek LK, (1998) Contribution of the Kv3.1 potassium channel to high-frequency firing in mouse auditory neurones. J Physiol 509 (Pt 1): 183-194.
58. Watanabe K, Vanecek J, Yamaoka S, (2000) In vitro entrainment of the circadian rhythm of vasopressin-releasing cells in suprachiasmatic nucleus by vasoactive intestinal polypeptide. Brain Res 877: 361-366.
59. Webb AB, Angelo N, Huettner JE, Herzog ED, (2009) Intrinsic, nondeterministic circadian rhythm generation in identified mammalian neurons. Proc Natl Acad Sci U S A 106: 16493-16498.
60. Welsh DK, Logothetis DE, Meister M, Reppert SM, (1995) Individual neurons dissociated from rat suprachiasmatic nucleus express independently phased circadian firing rhythms. Neuron 14: 697-706.
61. Welsh DK, Takahashi JS, Kay SA, (2010) Suprachiasmatic nucleus: cell autonomy and network properties. Annu Rev Physiol 72: 551-577.
62. Yao Z, Shafer OT, (2014) The Drosophila circadian clock is a variably coupled network of multiple peptidergic units. Science 343: 1516-1520.