Thalamic synaptic transmission of sensory information modulated by synergistic interaction of adenosine and serotonin

Journal of Neurochemistry

Volumn 128, Issue 6, 2014, Pages 852-863

  Yang, Ya Chin ^a   Hu, Chun Chang ^a   Huang, Chen Syuan ^a   Chou, Pei Yu ^a  

^a CHANG GUNG UNIVERSITY COLLEGE OF MEDICINE   (Taiwan)

Author keywords

context dependent neuromodulation; neuromodulators; short term synaptic plasticity; sleep wakefulness regulation; synaptic transmission; thalamocortical network

Indexed keywords

ADENOSINE; SEROTONIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN FUNCTION; CONTROLLED STUDY; FEMALE; HYPNAGOGIC STATE; INTERNEURON; MALE; MOUSE; NERVE CELL PLASTICITY; NEUROMODULATION; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; SENSORY SYSTEM; SHORT TERM SYNAPTIC DEPRESSION; SIGNAL NOISE RATIO; SIGNAL TRANSDUCTION; SLEEP WAKING CYCLE; SLOW WAVE SLEEP; SYNAPTIC TRANSMISSION; THALAMIC SYNAPTIC TRANSMISSION; THALAMOCORTICAL TRACT;

CONTEXT-DEPENDENT NEUROMODULATION; NEUROMODULATORS; SHORT-TERM SYNAPTIC PLASTICITY; SLEEP-WAKEFULNESS REGULATION; SYNAPTIC TRANSMISSION; THALAMOCORTICAL NETWORK;

ADENOSINE; AFFERENT PATHWAYS; ANIMALS; DRUG SYNERGISM; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; GENICULATE BODIES; MALE; MICE; MICE, INBRED C57BL; NEURONAL PLASTICITY; NEUROTRANSMITTER AGENTS; ORGAN CULTURE TECHNIQUES; RECEPTOR, ADENOSINE A1; SEROTONIN; SEROTONIN RECEPTOR AGONISTS; SLEEP; SYNAPTIC TRANSMISSION; THALAMUS;

EID: 84895928250     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.12499     Document Type: Article

References (74)

1. Agnati L. F., Ferré S., Lluis C., Franco R., and, Fuxe K., (2003) Molecular mechanisms and therapeutical implications of intramembrane receptor/receptor interactions among heptahelical receptors with examples from the striatopallidal GABA neurons. Pharmacol. Rev. 55, 509-550.
2. 1 receptor. Eur. J. Pharmacol. 340, 301-310.
3. Basheer R., Strecker R. E., Thakkar M. M., and, McCarley R. W., (2004) Adenosine and sleep-wake regulation. Progr. Neurobiol. 73, 379-396.
4. Blundon J. A., Bayazitov I. T., and, Zakharenko S. S., (2011) Presynaptic gating of postsynaptically expressed plasticity at mature thalamocortical synapses. J. Neurosci. 31, 16012-16025.
5. Boschert U., Amara D. A., Segu L., and, Hen R., (1994) The mouse 5-hydroxytryptamine1B receptor is localized predominantly on axon terminals. Neuroscience 58, 167-182.
6. Brenowitz S., David J., and, Trussell L., (1998) Enhancement of synaptic efficacy by presynaptic GABA(B) receptors. Neuron 20, 135-141.
7. Brust T. B., Cayabyab F. S., Zhou N., and, MacVicar B. A., (2006) p38 mitogen-activated protein kinase contributes to adenosine A1 receptor-mediated synaptic depression in area CA1 of the rat hippocampus. J. Neurosci. 26, 12427-12438.
8. Chen C., and, Regehr W. G., (2000) Developmental remodeling of the retinogeniculate synapse. Neuron 28, 955-966.
9. Chen C., and, Regehr W. G., (2003) Presynaptic modulation of the retinogeniculate synapse. J. Neurosci. 23, 3130-3135.
10. Ciruela F., Ferré S., Casadõ V., Cortés A., Cunha R. A., Lluis C., and, Franco R., (2006) Heterodimeric adenosine receptors: a device to regulate neurotransmitter release. Cell. Mol. Life Sci. 63, 2427-2431.
11. Coulon P., Budde T., and, Pape H. C., (2012) The sleep relay-the role of the thalamus in central and decentral sleep regulation. Pflugers Arch. 463, 53-71.
12. Cunha R. A., (2001) Adenosine as a neuromodulator and a homeostatic regulator in the nervous system: different roles, different sources and different receptors. Neurochem. Int. 38, 107-125.
13. De Lima A. D., and, Singer W., (1987) The serotoninergic fibers in the dorsal lateral geniculate nucleus of the cat: distribution and synaptic connections demonstrated with immunocytochemistry. J. Comp. Neurol. 258, 339-351.
14. Destexhe A., and, Sejnowski T. J., (2003) Interactions between membrane conductances underlying thalamocortical slow-wave oscillations. Physiol. Rev. 83, 1401-1453.
15. Dinopoulos A., Dori I., and, Parnavelas J. G., (1995) Serotonergic innervation of the lateral geniculate nucleus of the rat during postnatal development: a light and electron microscopic immunocytochemical analysis. J. Comp. Neurol. 363, 532-544.
16. Dixon A. K., Gubitz A. K., Sirinathsinghji D. J., Richardson P. J., and, Freeman T. C., (1996) Tissue distribution of adenosine receptor mRNAs in the rat. Br. J. Pharmacol. 118, 1461-1468.
17. Dobolyi Á., Reichart A., Szikra T., Nyitrai G., Kékesi K. A., and, Juhász G., (2000) Sustained depolarization induces changes in the extracellular concentrations of purine and pyramidine nucleosides in the rat thalamus. Neurochem. Int. 32, 247-256.
18. Dunwiddie T. V., and, Masino S. A., (2001) The role and regulation of adenosine in the central nervous system. Annu. Rev. Neurosci. 24, 31-55.
19. Fastbom J., Pazos A., and, Palacios J. M., (1987a) The distribution of adenosine A1 receptors and 5'-nucleotidase in the brain of some commonly used experimental animals. Neuroscience 22, 813-826.
20. Fastbom J., Pazos A., Probst A., and, Palacios J. M., (1987b) Adenosine A1 receptors in the human brain: A quantitative autoradiographic study. Neuroscience 22, 827-839.
21. Franco R., Ferré S., Agnati L., et al,. (2000) Evidence for adenosine/dopamine receptor interactions: indications for heteromerization. Neuropsychopharmacology 23 (4 Suppl), S50-S59.
22. Fredholm B. B., (1995) Adenosine receptors in the central nervous system. News Physiol. Sci. 10, 122-128.
23. Fuller P. M., Gooley J. J., and, Saper C. B., (2006) Neurobiology of the sleep-wake cycle: sleep architecture, circadian regulation, and regulatory feedback. J. Biol. Rhythms 21, 482-493.
24. Fuxe K., Ferre S., Zoli M., and, Agnati L. F., (1998) Integrated events in central dopamine transmission as analyzed at multiple levels. Evidence for intramembrane adenosine A2A/dopamine D2 and adenosine A1/dopamine D1 receptor interactions in the basal ganglion. Brain Res. Rev. 26, 258-273.
25. Govindaiah G., and, Cox C. L., (2005) Excitatory actions of dopamine via D1-like receptors in the rat lateral geniculate nucleus. J. Neurophysiol. 94, 3708-3718.
26. Govindaiah G., and, Cox C. L., (2006) Depression of retinogeniculate synaptic transmission by presynaptic D2-like dopamine receptors in rat lateral geniculate nucleus. Eur. J. Neurosci. 23, 423-434.
27. Haas H. L., and, Lin J. S., (2011) Waking with the hypothalamus. Pflugers Arch. 463, 31-42.
28. Halassa M. M., (2011) Thalamocortical dynamics of sleep: roles of purinergic neuromodulation. Semin. Cell Dev. Biol. 22, 245-251.
29. Huang Z. L., Urade Y., and, Hayaishi O., (2007) Prostaglandins and adenosine in the regulation of sleep and wakefulness. Curr. Opin. Pharmacol. 7, 33-38.
30. Jacobs B. L., and, Fornal C. A., (1999) Activity of serotonergic neurons in behaving animals. Neuropsychopharmacology 21 (2 Suppl), 9S-15S.
31. Jouvet M., (1969) Biogenic amines and the states of sleep. Science 163, 32-41.
32. Jouvet M., (1999) Sleep and serotonin: an unfinished story. Neuropsychopharmacology 21, 24S-27S.
33. Kreitzer A. C., and, Regehr W. G., (2000) Modulation of transmission during trains at a cerebellar synapse. J. Neurosci. 20, 1348-1357.
34. Krueger J. M., Rector D. M., Roy S., Van Dongen H. P. A., Belenky G., and, Panksepp J., (2008) Sleep as a fundamental property of neuronal assemblies. Nat. Rev. Neurosci. 9, 910-919.
35. Latini S., and, Pedata F., (2001) Adenosine in the central nervous system: release mechanisms and extracellular concentrations. J. Neurochem. 79, 463-484.
36. Lin J. S., Anaclet C., Sergeeva O. A., and, Haas H. L., (2011) The waking brain: an update. Cell. Mol. Life Sci. 68, 2499-2512.
37. Magnin M., Rey M., Bastuji H., Guillemant P., Mauguiere F., and, Garcia-Larrea L., (2010) Thalamic deactivation at sleep onset precedes that of the cerebral cortex in humans. Proc. Natl Acad. Sci. USA 107, 3829-3833.
38. 2+ channel subtypes in acutely isolated rat basolateral amygdala neurons. Br. J. Pharmacol. 132, 879-888.
39. McCormick D. A., (1992) Neurotransmitter actions in the thalamus and cerebral cortex and their roles in neuromodulation of thalamocortical activity. Prog. Neurobiol. 39, 337-388.
40. McCormick D. A., and, Bal T., (1994) Sensory gating mechanisms of the thalamus. Curr. Opin. Neurobiol. 4, 550-556.
41. McCormick D. A., and, Bal T., (1997) Sleep and arousal: thalamocortical mechanisms. Annu. Rev. Neurosci. 20, 185-215.
42. Monti J. M., and, Jantos H., (2008) The roles of dopamine and serotonin, and of their receptors, in regulating sleep and waking. Prog. Brain Res. 172, 625-646.
43. Okada M., Nutt D. J., Murakami T., Zhu G., Kamata A., Kawata Y., and, Kaneko S., (2001) Adenosine receptor subtypes modulate two major functional pathways for hippocampal serotonin release. J. Neurosci. 21, 628-640.
44. O'Neill C., Nolan B. J., Macari A., O'Boyle K. M., and, O'Connor J. J., (2007) Adenosine A1 receptor-mediated inhibition of dopamine release from rat striatal slices is modulated by D1 dopamine receptors. Eur. J. Neurosci. 26, 3421-3428.
45. Papadopoulos G. C., and, Parnavelas J. G., (1990) Distribution and synaptic organization of serotoninergic and noradrenergic axons in the lateral geniculate nucleus of the rat. J. Comp. Neurol. 294, 345-355.
46. Pape H. C., (1992) Adenosine promotes burst activity in guinea-pig geniculocortical neurons through two different ionic mechanisms. J. Physiol. 447, 729-753.
47. Pascual O., Casper K. B., Kubera C., Zhang J., Revilla-Sanchez R., Sul J. Y., Takano H., Moss S. J., McCarthy K., and, Haydon P. G., (2005) Astrocytic purinergic signaling coordinates synaptic networks. Science 310, 113-116.
48. Porkka-Heiskanen T., Strecker R. E., Thakkar M. M., Bjørkum A. A., Greene R. W., and, McCarley R. W., (1997) Adenosine: a mediator of the sleep-inducing effects of prolonged wakefulness. Science 276, 1625-1628.
49. Porkka-Heiskanen T., Alanko L., Kalinchuk A., and, Stenberg D., (2002) Adenosine and sleep. Sleep Med. Rev. 6, 321-332.
50. Poulet J. F. A., Fernandez L. M. J., Crochet S., and, Petersen C. C. H., (2012) Thalamic control of cortical states. Nat. Neurosci. 15, 370-372.
51. Pugliese A. M., Traini C., Cipriani S., Gianfriddo M., Mello T., Giovannini M. G., Galli A., and, Pedata F., (2009) The adenosine A2A receptor antagonist ZM241385 enhances neuronal survival after oxygen-glucose deprivation in rat CA1 hippocampal slices. Br. J. Pharmacol. 157, 818-830.
52. Rush A. M., Kilbride J., Rowan M. J., and, Anwyl R., (2002) Presynaptic group III mGluR modulation of short-term plasticity in the lateral perforant path of the dentate gyrus in vitro. Brain Res. 11, 38-43.
53. Saper C. B., Scammel T. E., and, Lu J., (2005) Hypothalamic regulation of sleep and circadian rhythms. Nature 437, 1257-1263.
54. Scanziani M., Capogna M., Gahwiler B. H., and, Thompson S. M., (1992) Presynaptic inhibition of miniature excitatory synaptic currents by baclofen and adenosine in the hippocampus. Neuron 9, 919-927.
55. Seeburg D. P., Liu X., and, Chen C., (2004) Frequency-dependent modulation of retinogeniculate transmission by serotonin. J. Neurosci. 24, 10950-10962.
56. Serrano A., Haddjeri N., Lacaille J. C., and, Robitaille R., (2006) GABAergic network activation of glial cells underlies hippocampal heterosynaptic depression. J. Neurosci. 26, 5370-5382.
57. Shen K.-Z., and, Johnson S. W., (1997) Presynaptic GABAB and adenosine A1 receptors regulate synaptic transmission to rat substantia nigra reticulata neurons. J. Physiol. 505, 153-163.
58. Sijbesma H., Schipper J., Cornelissen J. C., and, de Kloet E. R., (1991) Species differences in the distribution of central 5-HT1 binding sites: a comparative autoradiographic study between rat and guinea pig. Brain Res. 555, 295-304.
59. Sodickson D. L., and, Bean B. P., (1998) Neurotransmitter activation of inwardly rectifying potassium current in dissociated hippocampal CA3 neurons: interactions among multiple receptors. J. Neurosci. 18, 8153-8162.
60. Steriade M., Jones E. G., and, McCormick D. A., (1997) in Thalamus: organization and function. Elsevier, Oxford.
61. Strecker R., Morairty S., Thakkar M. M., Porkka-Heiskanen T., Basheer R., et al,. (2000) Adenosinergic modulation of basal forebrain and preoptic/anterior hypothalamic neuronal activity in the control of behavioral state. Behav. Brain Res. 115, 183-204.
62. Thomson A. M., (2000) Facilitation, augmentation and potentiation at central synapses. Trends Neurosci. 23, 305-312.
63. Tononi G., and, Cirelli C., (2003) Sleep and synaptic homeostasis: a hypothesis. Brain Res. Bull. 62, 143-150.
64. Tononi G., and, Cirelli C., (2006) Sleep function and synaptic homeostasis. Sleep Med. Rev. 10, 49-62.
65. Trussell L. O., and, Jackson M. B., (1985) Adenosine-activated potassium conductance in cultured striatal neurons. Proc. Natl Acad. Sci. USA 82, 4857-4861.
66. Ulrich D., and, Huguenard J. R., (1995) Purinergic inhibition of GABA and glutamatergic release in thalamus: implications for thalamic network activity. Neuron 15, 909-918.
67. Varnäs K., Hurd Y. L., and, Hall H., (2005) Regional expression of 5-HT1B receptor mRNA in the human brain. Synapse 56, 21-28.
68. Wang S., Kurada L., Cilz N. I., Chen X., Xiao Z., Dong H., and, Lei S., (2013) Adenosinergic depression of glutamatergic transmission in the entorhinal cortex of juvenile rats via reduction of glutamate release probability and the number of releasable vesicles. PLoS One 8, e62185.
69. Wu L. G., and, Saggau P., (1994) Adenosine inhibits evoked synaptic transmission primarily by reducing presynaptic calcium influx in area CA1 of hippocampus. Neuron 12, 1139-1148.
70. Wu L. G., and, Saggau P., (1997) Presynaptic inhibition of elicited neurotransmitter release. Trends Neurosci. 20, 204-212.
71. Wu L. G., Westenbroek R. E., Borst J. G. G., Catterall W. A., and, Sakmann B., (1999) Calcium channel types with distinct presynaptic localization couple differentially to transmitter release in single calyx-type synapses. J. Neurosci. 19, 726-736.
72. 2+ channels by adenosine autoreceptors. Nature 365, 256-258.
73. Zhang C., and, Schmidt J. T., (1999) Adenosine A1 and class II metabotropic glutamate receptors mediate shared presynaptic inhibition of retinotectal transmission J. Neurophysiol, 82, 2947-2955.
74. Zucker R. S., and, Regehr W. G., (2002) Short-term synaptic plasticity. Annu. Rev. Physiol. 64, 355-405.