GABA-mediated repulsive coupling between circadian clock neurons in the SCN encodes seasonal time

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 29, 2015, Pages E3920-E3929

  Myung, Jihwan ^a,b   Hong, Sungho ^c   DeWoskin, Daniel ^d   De Schutter, Erik ^c   Forger, Daniel B ^d,e   Takumi, Toru ^a,b,f  

^a RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

^b HIROSHIMA UNIVERSITY   (Japan)

^c OKINAWA INSTITUTE OF SCIENCE AND TECHNOLOGY GRADUATE UNIVERSITY   (Japan)

^d UNIVERSITY OF MICHIGAN   (United States)

^e UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^f JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Chloride; Day length encoding; GABA; Repulsive coupling; SCN

Indexed keywords

4 AMINOBUTYRIC ACID; POTASSIUM CHLORIDE COTRANSPORTER 2; SODIUM POTASSIUM CHLORIDE COTRANSPORTER 1; TRANSCRIPTION FACTOR ARNTL; 4 AMINOBUTYRIC ACID A RECEPTOR; CHLORIDE;

ANIMAL CELL; ARTICLE; BIOLUMINESCENCE; CIRCADIAN RHYTHM; DAY LENGTH; LIGHT DARK CYCLE; MOUSE; NERVE CELL; NERVE CELL NETWORK; NONHUMAN; OSCILLATION; PHOTOPERIODICITY; PRIORITY JOURNAL; SEASONAL VARIATION; SUPRACHIASMATIC NUCLEUS; TIME LAPSE IMAGING; ANIMAL; BIOLOGICAL MODEL; C57BL MOUSE; COMPUTER SIMULATION; DRUG EFFECTS; INTRACELLULAR SPACE; METABOLISM; PHYSIOLOGY; SEASON; TIME; TRANSGENIC MOUSE;

ANIMALIA; MAMMALIA;

ANIMALS; CHLORIDES; CIRCADIAN CLOCKS; CIRCADIAN RHYTHM; COMPUTER SIMULATION; GAMMA-AMINOBUTYRIC ACID; INTRACELLULAR SPACE; MICE, INBRED C57BL; MICE, TRANSGENIC; MODELS, NEUROLOGICAL; NERVE NET; NEURONS; RECEPTORS, GABA-A; SEASONS; SUPRACHIASMATIC NUCLEUS; TIME FACTORS;

EID: 84937849555     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1421200112     Document Type: Article

References (55)

1. Partch CL, Green CB, Takahashi JS (2014) Molecular architecture of the mammalian circadian clock. Trends Cell Biol 24(2):90-99.
2. Daan S, et al. (2001) Assembling a clock for all seasons: Are there M and E oscillators in the genes? J Biol Rhythms 16(2):105-116.
3. Inagaki N, Honma S, Ono D, Tanahashi Y, Honma K (2007) Separate oscillating cell groups in mouse suprachiasmatic nucleus couple photoperiodically to the onset and end of daily activity. Proc Natl Acad Sci USA 104(18):7664-7669.
4. Schaap J, et al. (2003) Heterogeneity of rhythmic suprachiasmatic nucleus neurons: Implications for circadian waveform and photoperiodic encoding. Proc Natl Acad Sci USA 100(26):15994-15999.
5. Rohling J, Meijer JH, VanderLeest HT, Admiraal J (2006) Phase differences between SCN neurons and their role in photoperiodic encoding; a simulation of ensemble patterns using recorded single unit electrical activity patterns. J Physiol Paris 100(5-6): 261-270.
6. VanderLeest HT, et al. (2007) Seasonal encoding by the circadian pacemaker of the SCN. Curr Biol 17(5):468-473.
7. Brown TM, Piggins HD (2009) Spatiotemporal heterogeneity in the electrical activity of suprachiasmatic nuclei neurons and their response to photoperiod. J Biol Rhythms 24(1):44-54.
8. Mrugala M, Zlomanczuk P, Jagota A, Schwartz WJ (2000) Rhythmic multiunit neural activity in slices of hamster suprachiasmatic nucleus reflect prior photoperiod. Am J Physiol Regul Integr Comp Physiol 278(4):R987-R994.
9. Naito E, Watanabe T, Tei H, Yoshimura T, Ebihara S (2008) Reorganization of the suprachiasmatic nucleus coding for day length. J Biol Rhythms 23(2):140-149.
10. Sumová A, Trávnícková Z, Peters R, Schwartz WJ, Illnerová H (1995) The rat suprachiasmatic nucleus is a clock for all seasons. Proc Natl Acad Sci USA 92(17):7754-7758.
11. Foley NC, et al. (2011) Characterization of orderly spatiotemporal patterns of clock gene activation in mammalian suprachiasmatic nucleus. Eur J Neurosci 33(10):1851-1865.
12. Myung J, et al. (2012) Period coding of Bmal1 oscillators in the suprachiasmatic nucleus. J Neurosci 32(26):8900-8918.
13. Evans JA, Leise TL, Castanon-Cervantes O, Davidson AJ (2013) Dynamic interactions mediated by nonredundant signaling mechanisms couple circadian clock neurons. Neuron 80(4):973-983.
14. Liu C, Weaver DR, Strogatz SH, Reppert SM (1997) Cellular construction of a circadian clock: Period determination in the suprachiasmatic nuclei. Cell 91(6):855-860.
15. 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(1):35-46.
16. Kuramoto Y (1984) Chemical Oscillations, Waves, and Turbulence (Springer, Berlin).
17. Timme M (2007) Revealing network connectivity from response dynamics. Phys Rev Lett 98(22):224101.
18. Kralemann B, Cimponeriu L, Rosenblum M, Pikovsky A, Mrowka R (2008) Phase dynamics of coupled oscillators reconstructed from data. Phys Rev E Stat Nonlin Soft Matter Phys 77(6 Pt 2):066205.
19. Albus H, Vansteensel MJ, Michel S, Block GD, Meijer JH (2005) A GABAergic mechanism is necessary for coupling dissociable ventral and dorsal regional oscillators within the circadian clock. Curr Biol 15(10):886-893.
20. Choi HJ, et al. (2008) Excitatory actions of GABA in the suprachiasmatic nucleus. J Neurosci 28(21):5450-5459.
21. Meijer JH, Michel S, Vanderleest HT, Rohling JH (2010) Daily and seasonal adaptation of the circadian clock requires plasticity of the SCN neuronal network. Eur J Neurosci 32(12):2143-2151.
22. Farajnia S, van Westering TL, Meijer JH, Michel S (2014) Seasonal induction of GABAergic excitation in the central mammalian clock. Proc Natl Acad Sci USA 111(26): 9627-9632.
23. DeWoskin D, et al. (2015) Distinct roles for GABA across multiple timescales in mammalian circadian timekeeping. Proc Natl Acad Sci USA 112: E3911-E3919.
24. Ciarleglio CM, Axley JC, Strauss BR, Gamble KL, McMahon DG (2011) Perinatal photoperiod imprints the circadian clock. Nat Neurosci 14(1):25-27.
25. Kelso JAS (1995) Dynamic Patterns: The Self-Organization of Brain and Behavior (MIT Press, Cambridge, MA).
26. Pittendrigh CS, Daan S (1976) A functional analysis of circadian pacemakers in nocturnal rodents. V. Pacemaker structure: A clock for all seasons. J Comp Physiol 106:333-355.
27. Aton SJ, Huettner JE, Straume M, Herzog ED (2006) GABA and Gi/o differentially control circadian rhythms and synchrony in clock neurons. Proc Natl Acad Sci USA 103(50):19188-19193.
28. Freeman GM, Jr, Krock RM, Aton SJ, Thaben P, Herzog ED (2013) GABA networks destabilize genetic oscillations in the circadian pacemaker. Neuron 78(5):799-806.
29. Yamada J, et al. (2004) Cl- uptake promoting depolarizing GABA actions in immature rat neocortical neurones is mediated by NKCC1. J Physiol 557(Pt 3):829-841.
30. Belenky MA, et al. (2010) Cell-type specific distribution of chloride transporters in the rat suprachiasmatic nucleus. Neuroscience 165(4):1519-1537.
31. Kanaka C, et al. (2001) The differential expression patterns of messenger RNAs encoding K-Cl cotransporters (KCC1,2) and Na-K-2Cl cotransporter (NKCC1) in the rat nervous system. Neuroscience 104(4):933-946.
32. Kahle KT, et al. (2005) WNK3 modulates transport of Cl- in and out of cells: Implications for control of cell volume and neuronal excitability. Proc Natl Acad Sci USA 102(46):16783-16788.
33. Diekman CO, et al. (2013) Causes and consequences of hyperexcitation in central clock neurons. PLOS Comput Biol 9(8):e1003196.
34. Kim JK, Forger DB (2012) A mechanism for robust circadian timekeeping via stoichiometric balance. Mol Syst Biol 8:630.
35. DeWoskin D, Geng W, Stinchcombe AR, Forger DB (2014) It is not the parts, but how they interact that determines the behaviour of circadian rhythms across scales and organisms. Interface Focus 4(3):20130076.
36. Daan S, Berde C (1978) Two coupled oscillators: Simulations of the circadian pacemaker in mammalian activity rhythms. J Theor Biol 70(3):297-313.
37. Kronauer RE (1987) Temporal subdivision of the circadian cycle. Lect Math Life Sci 19:63-120.
38. Oda GA, Friesen WO (2002) A model for "splitting" of running-wheel activity in hamsters. J Biol Rhythms 17(1):76-88.
39. 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(4):476-483.
40. Wagner S, Castel M, Gainer H, Yarom Y (1997) GABA in the mammalian suprachiasmatic nucleus and its role in diurnal rhythmicity. Nature 387(6633):598-603.
41. Liou SY, Albers HE (1990) Single unit response of neurons within the hamster suprachiasmatic nucleus to GABA and low chloride perfusate during the day and night. Brain Res Bull 25(1):93-98.
42. Sumová A, Jác M, Sládek M, Sauman I, Illnerová H (2003) Clock gene daily profiles and their phase relationship in the rat suprachiasmatic nucleus are affected by photoperiod. J Biol Rhythms 18(2):134-144.
43. Azzi A, et al. (2014) Circadian behavior is light-reprogrammed by plastic DNA methylation. Nat Neurosci 17(3):377-382.
44. Iyer R, Wang TA, Gillette MU (2014) Circadian gating of neuronal functionality: A basis for iterative metaplasticity. Front Syst Neurosci 8:164.
45. Yan L, et al. (2007) Exploring spatiotemporal organization of SCN circuits. Cold Spring Harb Symp Quant Biol 72:527-541.
46. Noguchi T, et al. (2010) Dual-color luciferase mouse directly demonstrates coupled expression of two clock genes. Biochemistry 49(37):8053-8061.
47. Vandesompele J, et al. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3 (7):research0034-research0034.11.
48. Hoppensteadt FC, Izhikevich EM (1997) Weakly Connected Neural Networks (Springer, New York).
49. Hong JH, Jeong B, Min CH, Lee KJ (2012) Circadian waves of cytosolic calcium concentration and long-range network connections in rat suprachiasmatic nucleus. Eur J Neurosci 35(9):1417-1425.
50. Fan J, et al. (2015) Vasoactive intestinal polypeptide (VIP)-expressing neurons in the suprachiasmatic nucleus provide sparse GABAergic outputs to local neurons with circadian regulation occurring distal to the opening of postsynaptic GABAA ionotropic receptors. J Neurosci 35(5):1905-1920.
51. Hastie T, Tibshirani R, Friedman J (2009) The Elements of Statistical Learning (Springer, New York), 2nd Ed.
52. Grant M, Boyd S, Ye Y (2008) CVX: Matlab software for disciplined convex programming. Available at http://cvxr.com/cvx/.
53. Friedman J, Hastie T, Tibshirani R (2010) Regularization paths for generalized linear models via coordinate descent. J Stat Softw 33(1):1-22.
54. Ermentrout GB, Terman DH (2010) Mathematical Foundations of Neuroscience (Springer, New York).
55. Kononenko NI, Dudek FE (2004) Mechanism of irregular firing of suprachiasmatic nucleus neurons in rat hypothalamic slices. J Neurophysiol 91(1):267-273.