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GABAA Receptor-Mediated Neurotransmission in the Suprachiasmatic Nucleus

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Mechanisms of Circadian Systems in Animals and Their Clinical Relevance

Abstract

GABAergic neurotransmission is a fundamental component of the suprachiasmatic nucleus (SCN) neural network, and virtually all SCN neurons communicate using GABA as a neurotransmitter. GABAergic neurotransmission plays a critical role in light-induced phase shifts, synchronization of the dorsal and ventral SCN, and, although controversial, synchronization of the circadian phase of individual SCN neurons. The circadian clock regulates the strength of GABAA receptor-mediated neurotransmission although the signaling mechanisms mediating this regulation are not known. GABA released from axon terminals acts on synaptic GABAA receptors producing postsynaptic currents that have a rapid onset and offset and desensitize in the continued presence of GABA. In the SCN, the postsynaptic GABAA receptor-mediated currents may be excitatory or inhibitory depending on the time of day. Once released GABA is removed from the synaptic cleft by specific sodium–chloride-dependent transporters (GAT). Some GABA can diffuse out of the synaptic cleft and act on extrasynaptic GABAA receptors. These extrasynaptic GABAA receptors have high affinity for GABA and show little or no desensitization. They mediate a “tonic” GABAA current that could modulate the input–output characteristics of individual SCN neurons. While significant scientific questions remain about the roles of GABAergic neurotransmission in the circadian timing signals, recent findings have yielded important advances in our understanding of GABAergic neurotransmission in the SCN.

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References

  • Aguilar-Roblero R, Verduzco-Carbajal L, Rodríguez C et al (1993) Circadian rhythmicity in the GABAergic system in the suprachiasmatic nuclei of the rat. Neurosci Lett 157:199–202

    Article  PubMed  CAS  Google Scholar 

  • Albus H, Vansteensel MJ, Michel S et al (2005) A gabaergic mechanism is necessary for coupling dissociable ventral and dorsal regional oscillators within the circadian clock. Curr Biol 15:886–893

    Google Scholar 

  • Aradi I, Soltesz I (2002) Modulation of network behaviour by changes in variance in interneuronal properties. J Physiol (Lond) 538:227–251

    Article  CAS  Google Scholar 

  • Aradi I, Santhakumar V, Chen K et al (2002) Postsynaptic effects of GABAergic synaptic diversity: regulation of neuronal excitability by changes in IPSC variance. Neuropharmacology 43:511–522

    Article  PubMed  CAS  Google Scholar 

  • Aton SJ, Herzog ED (2005) Come together, right…now: synchronization of rhythms in a mammalian circadian clock. Neuron 48:531–534

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Aton SJ, Huettner JE, Straume M et al (2006) GABA and Gi/o differentially control circadian rhythms and synchrony in clock neurons. Proc Natl Acad Sci U S A 103:19188–19193

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Attwell D, Mobbs P (1994) Neurotransmitter transporters. Curr Opin Neurobiol 4:353–359

    Article  PubMed  CAS  Google Scholar 

  • Barnard EA, Skolnick P, Olsen RW et al (1998) International Union of Pharmacology. XV. Subtypes of gamma-aminobutyric acidA receptors: classification on the basis of subunit structure and receptor function. Pharmacol Rev 50:291–313

    PubMed  CAS  Google Scholar 

  • Battaglioli G, Liu H, Martin DL (2003) Kinetic differences between the isoforms of glutamate decarboxylase: implications for the regulation of GABA synthesis. J Neurochem 86:879–887

    Article  PubMed  CAS  Google Scholar 

  • Belenky MA, Sagiv N, Fritschy J et al (2003) Presynaptic and postsynaptic GABA(A) receptors in rat suprachiasmatic nucleus. Neuroscience 118:909–923

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Belenky MA, Sollars PJ, Mount DB et al (2010) Cell-type specific distribution of chloride transporters in the rat suprachiasmatic nucleus. Neuroscience 165:1519–1537

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Cagampang FRA, Rattray M, Powell JF et al (1996) Circadian changes of glutamate decarboxylase 65 and 67 mRNA in the rat suprachiasmatic nuclei. Neuroreport 7:1925–1928

    Article  PubMed  CAS  Google Scholar 

  • Card JP, Moore RY (1984) The suprachiasmatic nucleus of the golden hamster: immunohistochemical analysis of cell and fiber distribution. Neuroscience 13:415–431

    Article  PubMed  CAS  Google Scholar 

  • Cardinali DP, Golombek DA (1998) The rhythmic GABAergic system. Neurochem Res 23:607–614

    Article  PubMed  CAS  Google Scholar 

  • Cavelier P, Hamann M, Rossi D et al (2005) Tonic excitation and inhibition of neurons: ambient transmitter sources and computational consequences. Prog Biophys Mol Biol 87:3–16

    Article  PubMed  CAS  Google Scholar 

  • Choi HJ, Lee CJ, Schroeder A et al (2008) Excitatory actions of GABA in the suprachiasmatic nucleus. J Neurosci 28:5450–5459

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Dalby NO (2003) Inhibition of gamma-aminobutyric acid uptake: anatomy, physiology and effects against epileptic seizures. Eur J Pharmacol 479:127–137

    Article  PubMed  CAS  Google Scholar 

  • Darna M, Schmutz I, Richter K et al (2009) Time of day-dependent sorting of the vesicular glutamate transporter to the plasma membrane. J Biol Chem 284:4300–4307

    Article  PubMed  CAS  Google Scholar 

  • De Jeu M, Pennartz CMA (2002) Circadian modulation of GABA function in the rat suprachiasmatic nucleus: excitatory effects during the night phase. J Neurophys 87:834–844

    Google Scholar 

  • Decavel C, Van den Pol AN (1990) GABA: a dominant neurotransmitter in the hypothalamus. J Comp Neurol 302:1019–1037

    Article  PubMed  CAS  Google Scholar 

  • Ehlen JC, Paul KN (2009) Regulation of light’s action in the mammalian circadian clock: role of the extrasynaptic GABAA receptor. Am J Physiol Regul Integr Comp Physiol 296:R1606–R1612

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Ehlen JC, Novak CM, Karom MC et al (2006) GABAA receptor activation suppresses Period 1 mRNA and Period 2 mRNA in the suprachiasmatic nucleus during the mid-subjective day. Eur J Neurosci 23:3328–3336

    Article  PubMed  Google Scholar 

  • Ehlen JC, Novak CM, Karom MC et al (2008) Interactions of GABA A receptor activation and light on period mRNA expression in the suprachiasmatic nucleus. J Biol Rhythms 23:16–25

    Article  PubMed  CAS  Google Scholar 

  • Fenalti G, Law RH, Buckle AM et al (2007) GABA production by glutamic acid decarboxylase is regulated by a dynamic catalytic loop. Nat Struct Mol Biol 14:280–286

    Article  PubMed  CAS  Google Scholar 

  • Fiumelli H, Cancedda L, Poo MM (2005) Modulation of GABAergic transmission by activity via postsynaptic Ca2+-dependent regulation of KCC2 function. Neuron 48:773–786

    Article  PubMed  CAS  Google Scholar 

  • Freeman GM Jr, Krock RM, Aton SJ et al (2013) GABA networks destabilize genetic oscillations in the circadian pacemaker. Neuron 78:799–806

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Fritschy JM, Brunig I (2003) Formation and plasticity of GABAergic synapses: physiological mechanisms and pathophysiological implications. Pharmacol Ther 98:299–323

    Article  PubMed  CAS  Google Scholar 

  • Gao B, Moore RY (1996) Glutamic acid decarboxylase message isoforms in human suprachiasmatic nucleus. J Biol Rhythms 11:172–179

    Article  PubMed  CAS  Google Scholar 

  • Gao B, Fritschy JM, Moore RY (1995) GABAA-receptor subunit composition in the circadian timing system. Brain Res 700:142–156

    Article  PubMed  CAS  Google Scholar 

  • Gasnier B (2004) The SLC32 transporter, a key protein for the synaptic release of inhibitory amino acids. Pflugers Arch 447:756–759

    Article  PubMed  CAS  Google Scholar 

  • Gillespie CF, Huhman KL, Babagbemi TO et al (1996) Bicuculline increases and muscimol reduces the phase-delaying effects of light and VIP/PHI/GRP in the suprachiasmatic region. J Biol Rhythms 11:137–144

    Article  PubMed  CAS  Google Scholar 

  • Glykys J, Dzhala V, Egawa K et al (2014) Local impermeant anions establish the neuronal chloride concentration. Science 343:670–675

    Article  PubMed  CAS  Google Scholar 

  • Glykys J, Mody I (2007) The main source of ambient GABA responsible for tonic inhibition in the mouse hippocampus. J Physiol 582:1163–1178

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Gompf HS, Allen CN (2004) GABAergic synapses of the suprachiasmatic nucleus exhibit a diurnal rhythm of short-term synaptic plasticity. Eur J Neurosci 19:2791–2798

    Article  PubMed  Google Scholar 

  • Gompf HS, Irwin RP, Allen CN (2006) Retrograde suppression of GABAergic currents in a subset of SCN neurons. Eur J Neurosci 23:3209–3216

    Article  PubMed  Google Scholar 

  • Guldner FH (1984) Suprachiasmatic nucleus: numbers of synaptic appositions and various types of synapses. A morphometric study on male and female rats. Cell Tissue Res 235:449–452

    Article  PubMed  CAS  Google Scholar 

  • Hsu CC, Thomas C, Chen W et al (1999) Role of synaptic vesicle proton gradient and protein phosphorylation on ATP-mediated activation of membrane-associated brain glutamate decarboxylase. J Biol Chem 274:24366–24371

    Article  PubMed  CAS  Google Scholar 

  • Huhman KL, Hennessey AC, Albers HE (1996) Rhythms of glutamic acid decarboxylase mRNA in the suprachiasmatic nucleus. J Biol Rhythms 11:311–316

    Article  PubMed  CAS  Google Scholar 

  • Huhman KL, Jasnow AM, Sisitsky AK et al (1999) Glutamic acid decarboxylase mRNA in the suprachiasmatic nucleus of rats housed in constant darkness. Brain Res 851:266–269

    Article  PubMed  CAS  Google Scholar 

  • Ing T, Poulter MO (2007) Diversity of GABA(A) receptor synaptic currents on individual pyramidal cortical neurons. Eur J Neurosci 25:723–734

    Article  PubMed  Google Scholar 

  • Irwin RP, Allen CN (2009) GABAergic signaling induces divergent neuronal Ca(2+) responses in the suprachiasmatic nucleus network. Eur J Neurosci 30:1462–1475

    Article  PubMed  PubMed Central  Google Scholar 

  • Isaacson JS, Solís JM, Nicoll RA (1993) Local and diffuse synaptic actions of GABA in the hippocampus. Neuron 10:165–175

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Itri J, Michel S, Waschek JA et al (2004) Circadian rhythm in inhibitory synaptic transmission in the mouse suprachiasmatic nucleus. J Neurophysiol 92:311–319

    Article  PubMed  PubMed Central  Google Scholar 

  • Jansen HT, Gong Q, Norgren RB Jr et al (1994) Single- and double-label immunocytochemical study of the ovine suprachiasmatic nucleus (SCN): GABAergic and peptidergic relationships. Brain Res Bull 34:499–506

    Article  PubMed  CAS  Google Scholar 

  • Jiang Z-G, Allen CN, North RA (1995) Presynaptic inhibition by baclofen of retinohypothalamic excitatory synaptic transmission in rat suprachiasmatic nucleus. Neuroscience 64:813–819

    Article  PubMed  CAS  Google Scholar 

  • Jiang Z-G, Yang Y-Q, Liu Z-P et al (1997) Membrane properties and synaptic inputs of suprachiasmatic nucleus neurons in rat brain slices. J Physiol (Lond) 499:141–159

    CAS  Google Scholar 

  • Jobst EE, Robinson DW, Allen CN (2004) Potential pathways for intercellular communication within the calbindin subnucleus of the hamster suprachiasmatic nucleus. Neuroscience 123:87–99

    Article  PubMed  CAS  Google Scholar 

  • Jones MV, Jonas P, Sahara Y et al (2001) Microscopic kinetics and energetics distinguish GABA(A) receptor agonists from antagonists. Biophys J 81:2660–2670

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Kavanaugh MP, Arriza JL, North RA et al (1992) Electrogenic uptake of gamma-aminobutyric acid by a cloned transporter expressed in Xenopus oocytes. J Biol Chem 267:22007–22009

    PubMed  CAS  Google Scholar 

  • Kim YI, Dudek FE (1992) Intracellular electrophysiological study of suprachiasmatic nucleus neurons in rodents: inhibitory synaptic mechanisms. J Physiol (Lond) 458:247–260

    CAS  Google Scholar 

  • Ko CH, Yamada YR, Welsh DK et al (2010) Emergence of noise-induced oscillations in the central circadian pacemaker. PLoS Biol 8:e1000513

    Article  PubMed  PubMed Central  Google Scholar 

  • Kononenko NI, Dudek FE (2004) Mechanism of irregular firing of suprachiasmatic nucleus neurons in rat hypothalamic slices. J Neurophysiol 91:267–273

    Article  PubMed  Google Scholar 

  • Lerma J, Herranz AS, Herreras O et al (1986) In vivo determination of extracellular concentration of amino acids in the rat hippocampus. A method based on brain dialysis and computerized analysis. Brain Res 384:145–155

    Article  PubMed  CAS  Google Scholar 

  • Liu C, Reppert SM (2000) GABA synchronizes clock cells within the suprachiasmatic circadian clock. Neuron 25:123–128

    Article  PubMed  CAS  Google Scholar 

  • Liu AC, Welsh DK, Ko CH et al (2007) Intercellular coupling confers robustness against mutations in the SCN circadian clock network. Cell 129:605–616

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Low-Zeddies SS, Takahashi JS (2001) Chimera analysis of the Clock mutation in mice shows that complex cellular integration determines circadian behavior. Cell 105:25–42

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • McElroy B, Zakaria A, Glass JD et al (2009) Ethanol modulates mammalian circadian clock phase resetting through extrasynaptic gaba receptor activation. Neuroscience 164:842–848

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • McIntire SL, Reimer RJ, Schuske K et al (1997) Identification and characterization of the vesicular GABA transporter. Nature 389:870–876

    Article  PubMed  CAS  Google Scholar 

  • Michel S, Colwell CS (2001) Cellular communication and coupling within the suprachiasmatic nucleus. Chronobiol Int 18:579–600

    Article  PubMed  CAS  Google Scholar 

  • Mody I (2001) Distinguishing between GABAA receptors responsible for tonic and phasic conductances. Neurochem Res 26:907–913

    Article  PubMed  CAS  Google Scholar 

  • Mody I (2005) Aspects of the homeostaic plasticity of GABAA receptor-mediated inhibition. J Physiol 562:37–46

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Mody I, Pearce RA (2004) Diversity of inhibitory neurotransmission through GABA(A) receptors. Trends Neurosci 27:569–575

    Article  PubMed  CAS  Google Scholar 

  • Mohler H (2006) GABA(A) receptor diversity and pharmacology. Cell Tissue Res 326:505–516

    Article  PubMed  CAS  Google Scholar 

  • Moldavan MG, Allen CN (2013) GABAB receptor-mediated frequency-dependent and circadian changes in synaptic plasticity modulate retinal input to the suprachiasmatic nucleus. J Physiol (Lond) 591:2475–2490

    CAS  Google Scholar 

  • Moldavan MG, Irwin RP, Allen CN (2006) Presynaptic GABAB receptors regulate retinohypothalamic tract synaptic transmission by inhibiting voltage-gated Ca2+ channels. J Neurophysiol 95:3727–3741

    Article  PubMed  CAS  Google Scholar 

  • Moore RY, Speh JC (1993) GABA is the principal neurotransmitter of the circadian system. Neurosci Lett 150:112–116

    Article  PubMed  CAS  Google Scholar 

  • Mozrzymas JW, Zarnowska ED, Pytel M et al (2003) Modulation of GABA(A) receptors by hydrogen ions reveals synaptic GABA transient and a crucial role of the desensitization process. J Neurosci 23:7981–7992

    PubMed  CAS  Google Scholar 

  • Naum OG, Fernanda Rubio M, Golombek DA (2001) Rhythmic variation in gamma-aminobutyric acid(A)-receptor subunit composition in the circadian system and median eminence of Syrian hamsters. Neurosci Lett 310:178–182

    Article  CAS  Google Scholar 

  • Novak CM, Albers HE (2004) Novel phase-shifting effects of GABAA receptor activation in the suprachiasmatic nucleus of a diurnal rodent. Am J Physiol Regul Integr Comp Physiol 286:R820–R825

    Article  PubMed  CAS  Google Scholar 

  • O’Hara BF, Andretic R, Heller HC et al (1995) GABAA, GABAC, and NMDA receptor subunit expression in the suprachiasmatic nucleus and other brain regions. Mol Brain Res 28:239–250

    Article  PubMed  Google Scholar 

  • Olsen RW, Sieghart W (2008) International Union of Pharmacology. LXX. Subtypes of gamma-aminobutyric acid(A) receptors: classification on the basis of subunit composition, pharmacology, and function. Update. Pharmacol Rev 60:243–260

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Panda S, Antoch MP, Miller BH et al (2002) Coordinated transcription of key pathways in the mouse by the circadian clock. Cell 109:307–320

    Article  PubMed  CAS  Google Scholar 

  • Ralph MR, Menaker M (1986) Effects of diazepam on circadian phase advances and delays. Brain Res 372:405–408

    Article  PubMed  CAS  Google Scholar 

  • Reppert SM, Weaver DR (2001) Molecular analysis of mammalian circadian rhythms. Annu Rev Physiol 63:647–676

    Article  PubMed  CAS  Google Scholar 

  • Riazanski V, Deriy LV, Shevchenko PD et al (2011) Presynaptic CLC-3 determines quantal size of inhibitory transmission in the hippocampus. Nat Neurosci 14:487–494

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Richerson GB, Wu Y (2003) Dynamic equilibrium of neurotransmitter transporters: not just for reuptake anymore. J Neurophysiol 90:1363–1374

    Article  PubMed  CAS  Google Scholar 

  • Rudolph U, Mohler H (2004) Analysis of GABAA receptor function and dissection of the pharmacology of benzodiazepines and general anesthetics through mouse genetics. Annu Rev Pharmacol Toxicol 44:475–498

    Article  PubMed  CAS  Google Scholar 

  • Santos MS, Park CK, Foss SM et al (2013) Sorting of the vesicular GABA transporter to functional vesicle pools by an atypical dileucine-like motif. J Neurosci 33:10634–10646

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Schofield CM, Huguenard JR (2007) GABA affinity shapes IPSCs in thalamic nuclei. J Neurosci 27:7954–7962

    Article  PubMed  CAS  Google Scholar 

  • Semyanov A, Walker MC, Kullmann DM (2003) GABA uptake regulates cortical excitability via cell type-specific tonic inhibition. Nat Neurosci 6:484–490

    PubMed  CAS  Google Scholar 

  • Semyanov A, Walker MC, Kullmann DM et al (2004) Tonically active GABA(A) receptors: modulating gain and maintaining the tone. Trends Neurosci 27:262–269

    Article  PubMed  CAS  Google Scholar 

  • Shirakawa T, Honma S, Katsuno Y et al (2000) Synchronization of circadian firing rhythms in cultured rat suprachiasmatic neurons. Eur J Neurosci 12:2833–2838

    Article  PubMed  CAS  Google Scholar 

  • Smith RD, Inouye S, Turek FW (1989) Central administration of muscimol phase-shifts the mammalian circadian clock. J Comp Physiol 164:805–814

    Article  CAS  Google Scholar 

  • Staley KJ, Mody I (1992) Shunting of excitatory input to dentate gyrus granule cells by depolarizating GABAA receptor-mediated postsynaptic conductances. J Neurophysiol 68:197–212

    PubMed  CAS  Google Scholar 

  • Stell BM, Mody I (2002) Receptors with different affinities mediate phasic and tonic GABA(A) conductances in hippocampal neurons. J Neurosci 22:RC223

    PubMed  Google Scholar 

  • Strecker GJ, Wuarin JP, Dudek FE (1997) GABAA-mediated local synaptic pathways connect neurons in the rat suprachiasmatic nucleus. J Neurophysiol 78:2217–2220

    PubMed  CAS  Google Scholar 

  • Subramanian P, Subbaraj R (1996) Diazepam modulates the period of locomotor rhythm in mice (Mus booduga) and attenuates light-induced phase advances. Pharmacol Biochem Behav 54:393–398

    Article  PubMed  CAS  Google Scholar 

  • Tossman U, Jonsson G, Ungerstedt U (1986) Regional distribution and extracellular levels of amino acids in rat central nervous system. Acta Physiol Scand 127:533–545

    Article  PubMed  CAS  Google Scholar 

  • Van den Pol AN (1980) The hypothalamic suprachiasmatic nucleus of rat: intrinsic anatomy. J Comp Neurol 191:661–702

    Article  PubMed  Google Scholar 

  • vanderLeest HT, Rohling JH, Michel S et al (2009) Phase shifting capacity of the circadian pacemaker determined by the SCN neuronal network organization. PLoS One 4:e4976

    Article  PubMed  PubMed Central  Google Scholar 

  • Wagner S, Castel M, Gainer H et al (1997) GABA in the mammalian suprachiasmatic nucleus and its role in diurnal rhythmicity. Nature 387:598–603

    Article  PubMed  CAS  Google Scholar 

  • Wagner S, Sagiv N, Yarom Y (2001) GABA-induced current and circadian regulation of chloride in neurones of the rat suprachiasmatic nucleus. J Physiol (Lond) 537:853–869

    Article  CAS  Google Scholar 

  • Welsh DK, Logothetis DE, Meister M et al (1995) Individual neurons dissociated from rat suprachiasmatic nucleus express independently phased circadian firing rhythms. Neuron 14:697–706

    Article  PubMed  CAS  Google Scholar 

  • Welsh DK, Takahashi JS, Kay SA (2010) Suprachiasmatic nucleus: cell autonomy and network properties. Annu Rev Physiol 72:551–577

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Woodin MA, Ganguly K, Poo MM (2003) Coincident pre- and postsynaptic activity modifies GABAergic synapses by postsynaptic changes in Cl- transporter activity. Neuron 39:807–820

    Article  PubMed  CAS  Google Scholar 

  • Yamazaki S, Numano R, Abe M et al (2000) Resetting central and peripheral circadian oscillators in transgenic rats. Science 288:682–685

    Article  PubMed  CAS  Google Scholar 

  • Yamazaki S, Yoshikawa T, Biscoe EW et al (2009) Ontogeny of circadian organization in the rat. J Biol Rhythms 24:55–63

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Yoo SH, Yamazaki S, Lowrey PL et al (2004) PERIOD2::LUCIFERASE real-time reporting of circadian dynamics reveals persistent circadian oscillations in mouse peripheral tissues. Proc Natl Acad Sci U S A 101:5339–5346

    Article  PubMed  CAS  PubMed Central  Google Scholar 

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Acknowledgments

The work was supported by grants from NINDS (NS036607) and NIGMS (GM096972) to CNA.

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Authors and Affiliations

  1. Oregon Institute of Occupational Health Sciences, Oregon Health & Science University, Portland, OR, 97239, USA

    Charles N. Allen, Nathan J. Klett, Robert P. Irwin & Mykhaylo G. Moldavan

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  1. Charles N. Allen
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  2. Nathan J. Klett
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  3. Robert P. Irwin
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  4. Mykhaylo G. Moldavan
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Correspondence to Charles N. Allen .

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Editors and Affiliations

  1. Instituto de Fisiología Celular, Universidad Nacional Autonoma de México, México, Distrito Federal, Mexico

    Raúl Aguilar-Roblero

  2. Instituto de Neurobiología, Universidad Nacional Autónoma de México, Juriquilla, Querétaro, Mexico

    Mauricio Díaz-Muñoz

  3. Facultad de Ciencias, Universidad Nacional Autónoma de México, México, Distrito Federal, Mexico

    Mária Luisa Fanjul-Moles

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Allen, C.N., Klett, N.J., Irwin, R.P., Moldavan, M.G. (2015). GABAA Receptor-Mediated Neurotransmission in the Suprachiasmatic Nucleus. In: Aguilar-Roblero, R., Díaz-Muñoz, M., Fanjul-Moles, M. (eds) Mechanisms of Circadian Systems in Animals and Their Clinical Relevance. Springer, Cham. https://doi.org/10.1007/978-3-319-08945-4_8

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