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

Journal of Neuroscience

Volumn 35, Issue 5, 2015, Pages 1905-1920

  Fan, Junmei ^a   Zeng, Hongkui ^c   Olson, David P ^d   Huber, Kimberly M ^a   Gibson, Jay R ^a   Takahashi, Joseph S ^a,b  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c ALLEN INSTITUTE FOR BRAIN SCIENCE   (United States)

^d UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Circadian; GABA; Network; SCN; Synapse; VIP

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; VASOACTIVE INTESTINAL POLYPEPTIDE; 4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID RECEPTOR;

ACTION POTENTIAL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL SYNCHRONIZATION; CIRCADIAN RHYTHM; ELECTROPHYSIOLOGY; EVOKED RESPONSE; FEMALE; GABAERGIC SYSTEM; MALE; MEMBRANE DEPOLARIZATION; MOUSE; NERVE CELL; NERVE CELL EXCITABILITY; NERVE CELL MEMBRANE POTENTIAL; NERVE STIMULATION; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; SUPRACHIASMATIC NUCLEUS; SYNAPTIC TRANSMISSION; ANIMAL; CYTOLOGY; GENETICS; METABOLISM; PHYSIOLOGY; SENSORY NERVE CELL; SYNAPSE; SYNAPTIC POTENTIAL;

ACTION POTENTIALS; ANIMALS; CIRCADIAN RHYTHM; FEMALE; GABAERGIC NEURONS; GAMMA-AMINOBUTYRIC ACID; MALE; MICE; NEURONS, AFFERENT; RECEPTORS, GABA-A; SUPRACHIASMATIC NUCLEUS; SYNAPSES; SYNAPTIC POTENTIALS; VASOACTIVE INTESTINAL PEPTIDE;

EID: 84922369760     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2661-14.2015     Document Type: Article

References (51)

1. Abrahamson EE, Moore RY (2001) Suprachiasmatic nucleus in the mouse: retinal innervation, intrinsic organization and efferent projections. Brain Res 916:172–191. CrossRef Medline
2. 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 15:886–893. CrossRef Medline
3. 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. CrossRef Medline
4. Belenky MA, Yarom Y, Pickard GE (2008) Heterogeneous expression of gamma-aminobutyric acid and gamma-aminobutyric acid-associated receptors and transporters in the rat suprachiasmatic nucleus. J Comp Neurol 506:708–732. CrossRef Medline
5. Belle MD, Diekman CO, Forger DB, Piggins HD (2009) Daily electrical silencing in the mammalian circadian clock. Science 326:281–284. CrossRef Medline
6. Brancaccio M, Maywood ES, Chesham JE, Loudon AS, Hastings MH (2013) A Gq-Ca2+ axis controls circuit-level encoding of circadian time in the suprachiasmatic nucleus. Neuron 78:714–728. CrossRef Medline
7. Castel M, Morris JF (2000) Morphological heterogeneity of the GABAergic network in the suprachiasmatic nucleus, the brain’s circadian pacemaker. J Anat 196:1–13. CrossRef Medline
8. Choi HJ, Lee CJ, Schroeder A, Kim YS, Jung SH, Kim JS, Kim do Y, Son EJ, Han HC, Hong SK, Colwell CS, Kim YI (2008) Excitatory actions of GABA in the suprachiasmatic nucleus. J Neurosci 28:5450–5459. CrossRef Medline
9. 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. CrossRef Medline
10. De Jeu M, Pennartz C (2002) Circadian modulation of GABA function in the rat suprachiasmatic nucleus: excitatory effects during the night phase. J Neurophysiol 87:834–844. Medline
11. Evans JA, Leise TL, Castanon-Cervantes O, Davidson AJ (2013) Dynamic interactions mediated by nonredundant signaling mechanisms couple circadian clock neurons. Neuron 80:973–983. CrossRef Medline
12. Freeman GM Jr, Krock RM, Aton SJ, Thaben P, Herzog ED (2013) GABA networks destabilize genetic oscillations in the circadian pacemaker. Neuron 78:799–806. CrossRef Medline
13. Gillette MU, Medanic M, McArthur AJ, Liu C, Ding JM, Faiman LE, Weber ET, Tcheng TK, Gallman EA (1995) Intrinsic neuronal rhythms in the suprachiasmatic nuclei and their adjustment. Ciba Found Symp 183:134–144; discussion 144–153. Medline
14. Hamada T, LeSauter J, Venuti JM, Silver R (2001) Expression of period genes: rhythmic and nonrhythmic compartments of the suprachiasmatic nucleus pacemaker. J Neurosci 21:7742–7750. Medline
15. Han S, Yu FH, Schwartz MD, Linton JD, Bosma MM, Hurley JB, Catterall WA, de la Iglesia HO (2012) Na(V)1.1 channels are critical for intercellular communication in the suprachiasmatic nucleus and for normal circadian rhythms. Proc Natl Acad Sci U S A 109:E368–377. CrossRef Medline
16. Harmar AJ, Marston HM, Shen S, Spratt C, West KM, Sheward WJ, Morrison CF, Dorin JR, Piggins HD, Reubi JC, Kelly JS, Maywood ES, Hastings MH (2002) The VPAC(2) receptor is essential for circadian function in the mouse suprachiasmatic nuclei. Cell 109:497–508. CrossRef Medline
17. Hogenesch JB, Herzog ED (2011) Intracellular and intercellular processes determine robustness of the circadian clock. FEBS Lett 585:1427–1434. CrossRef Medline
18. 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 35:1417–1425. CrossRef Medline
19. Huntsman MM, Porcello DM, Homanics GE, DeLorey TM, Huguenard JR (1999) Reciprocal inhibitory connections and network synchrony in the mammalian thalamus. Science 283:541–543. CrossRef Medline
20. Itri J, Colwell CS (2003) Regulation of inhibitory synaptic transmission by vasoactive intestinal peptide (VIP) in the mouse suprachiasmatic nucleus. J Neurophysiol 90:1589–1597. CrossRef Medline
21. Itri JN, Michel S, Vansteensel MJ, Meijer JH, Colwell CS (2005) Fast delayed rectifier potassium current is required for circadian neural activity. Nat Neurosci 8:650–656. CrossRef Medline
22. Itri J, Michel S, Waschek JA, Colwell CS (2004) Circadian rhythm in inhibitory synaptic transmission in the mouse suprachiasmatic nucleus. J Neurophysiol 92:311–319. CrossRef Medline
23. Jiang ZG, Yang Y, Liu ZP, Allen CN (1997) Membrane properties and synaptic inputs of suprachiasmatic nucleus neurons in rat brain slices. J Physiol 499:141–159. Medline
24. 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. CrossRef Medline
25. Kim YI, Dudek FE (1992) Intracellular electrophysiological study of suprachiasmatic nucleus neurons in rodents: inhibitory synaptic mechanisms. J Physiol 458:247–260. Medline
26. 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. CrossRef Medline
27. Landisman CE, Long MA, Beierlein M, Deans MR, Paul DL, Connors BW (2002) Electrical synapses in the thalamic reticular nucleus. J Neurosci 22:1002–1009. Medline
28. Liu C, Reppert SM (2000) GABA synchronizes clock cells within the suprachiasmatic circadian clock. Neuron 25:123–128. CrossRef Medline
29. Liu C, Weaver DR, Jin X, Shearman LP, Pieschl RL, Gribkoff VK, Reppert SM (1997) Molecular dissection of two distinct actions of melatonin on the suprachiasmatic circadian clock. Neuron 19:91–102. CrossRef Medline
30. Madisen L, Mao T, Koch H, Zhuo JM, Berenyi A, Fujisawa S, Hsu YW, Garcia AJ, Gu X, Zanella S, Kidney J, Gu H, Mao Y, Hooks BM, Boyden ES, Buzsáki G, Ramirez JM, Jones AR, Svoboda K, Han X, et al. (2012) A toolbox of Cre-dependent optogenetic transgenic mice for light-induced activation and silencing. Nat Neurosci 15:793–802. CrossRef Medline
31. Madisen L, Zwingman TA, Sunkin SM, Oh SW, Zariwala HA, Gu H, Ng LL, Palmiter RD, Hawrylycz MJ, Jones AR, Lein ES, Zeng H (2010) A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat Neurosci 13:133–140. CrossRef Medline
32. 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. CrossRef Medline
33. Mohawk JA, Takahashi JS (2011) Cell autonomy and synchrony of supra- chiasmatic nucleus circadian oscillators. Trends Neurosci 34:349–358. CrossRef Medline
34. Moore RY, Speh JC (1993) GABA is the principal neurotransmitter of the circadian system. Neurosci Lett 150:112–116. CrossRef Medline
35. Morin LP (2013) Neuroanatomy of the extended circadian rhythm system. Exp Neurol 243:4–20. CrossRef Medline
36. 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:R987–R994. Medline
37. Patel AB, Hays SA, Bureau I, Huber KM, Gibson JR (2013) A target cellspecific role for presynaptic Fmr1 in regulating glutamate release onto neocortical fast-spiking inhibitory neurons. J Neurosci 33:2593–2604. CrossRef Medline
38. Pei H, Sutton AK, Burnett KH, Fuller PM, Olson DP (2014) AVP neurons in the paraventricular nucleus of the hypothalamus regulate feeding. Molecular metabolism 3:209–215. CrossRef Medline
39. 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. CrossRef Medline
40. Perkins KL (2006) Cell-attached voltage-clamp and current-clamp recording and stimulation techniques in brain slices. J Neurosci Methods 154: 1–18. CrossRef Medline
41. Petreanu L, Huber D, Sobczyk A, Svoboda K (2007) Channelrhodopsin-2- assisted circuit mapping of long-range callosal projections. Nat Neurosci 10:663–668. CrossRef Medline
42. Petreanu L, Mao T, Sternson SM, Svoboda K (2009) The subcellular organization of neocortical excitatory connections. Nature 457:1142–1145. CrossRef Medline
43. Raastad M, Storm JF, Andersen P (1992) Putative single quantum and single fibre excitatory postsynaptic currents show similar amplitude range and variability in rat hippocampal slices. Eur J Neurosci 4:113–117. CrossRef Medline
44. Schaap J, Albus H, VanderLeest HT, Eilers PH, Détári L, Meijer JH (2003) Heterogeneity of rhythmic suprachiasmatic nucleus neurons: implications for circadian waveform and photoperiodic encoding. Proc Natl Acad Sci U S A 100:15994–15999. CrossRef Medline
45. Shepherd GM, Pologruto TA, Svoboda K (2003) Circuit analysis of experience-dependent plasticity in the developing rat barrel cortex. Neuron 38:277–289. CrossRef Medline
46. Strecker GJ, Wuarin JP, Dudek FE (1997) GABAA-mediated local synaptic pathways connect neurons in the rat suprachiasmatic nucleus. J Neurophysiol 78:2217–2220. Medline
47. Taniguchi H, He M, Wu P, Kim S, Paik R, Sugino K, Kvitsani D, Fu Y, Lu J, Lin Y, Miyoshi G, Shima Y, Fishell G, Nelson SB, Huang ZJ (2011) A resource of Cre driver lines for genetic targeting of GABAergic neurons in cerebral cortex. Neuron 71:995–1013. CrossRef Medline
48. Wagner S, Castel M, Gainer H, Yarom Y (1997) GABA in the mammalian suprachiasmatic nucleus and its role in diurnal rhythmicity. Nature 387: 598–603. CrossRef Medline
49. Wang TA, Yu YV, Govindaiah G, Ye X, Artinian L, Coleman TP, Sweedler JV, Cox CL, Gillette MU (2012) Circadian rhythm of redox state regulates excitability in suprachiasmatic nucleus neurons. Science 337:839–842. CrossRef Medline
50. 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. CrossRef Medline
51. Welsh DK, Takahashi JS, Kay SA (2010) Suprachiasmatic nucleus: cell autonomy and network properties. Annu Rev Physiol 72:551–577. CrossRef Medline