Adenosine modulates the excitability of layer II stellate neurons in entorhinal cortex through A1 receptors

Hippocampus

Volumn 21, Issue 3, 2011, Pages 265-280

  Li, Yang ^a   Fan, Shuangyi ^a   Yan, Jie ^a   Li, Bo ^a   Chen, Fang ^a   Xia, Jianxia ^a   Yu, Zhengping ^a   Hu, Zhian ^a  

^a THIRD MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

HCN channels; I h, mEPSCs; MIPSCs; Patch clamp

Indexed keywords

3,7 DIMETHYL 1 PROPARGYLXANTHINE; 4 (N ETHYL N PHENYLAMINO) 1,2 DIMETHYL 6 (METHYLAMINO)PYRIMIDINIUM CHLORIDE; 4 AMINOBUTYRIC ACID; 8 CYCLOPENTYL 1,3 DIPROPYLXANTHINE; ADENOSINE; ADENOSINE A1 RECEPTOR; ADENOSINE A2 RECEPTOR; GLUTAMIC ACID; PRESYNAPTIC RECEPTOR; VOLTAGE GATED CALCIUM CHANNEL;

ACTION POTENTIAL; ANIMAL TISSUE; ARTICLE; ENTORHINAL CORTEX; EXCITABILITY; EXCITATORY POSTSYNAPTIC POTENTIAL; EXTRACELLULAR CALCIUM; HYPERPOLARIZATION; INHIBITORY POSTSYNAPTIC POTENTIAL; NERVE CELL; NONHUMAN; PRESYNAPTIC MEMBRANE; PRIORITY JOURNAL; RAT; STELLATE NEURON;

ADENOSINE; ADENOSINE A1 RECEPTOR ANTAGONISTS; ADENOSINE A2 RECEPTOR ANTAGONISTS; ANIMALS; CALCIUM; CALCIUM CHANNELS; ENTORHINAL CORTEX; EXCITATORY POSTSYNAPTIC POTENTIALS; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; NEURAL INHIBITION; NEURONS; ORGAN CULTURE TECHNIQUES; PATCH-CLAMP TECHNIQUES; PRESYNAPTIC TERMINALS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, ADENOSINE A1; RECEPTORS, ADENOSINE A2; SYNAPTIC TRANSMISSION; THEOBROMINE; XANTHINES;

EID: 79951863669     PISSN: 10509631     EISSN: 10981063     Source Type: Journal    
DOI: 10.1002/hipo.20745     Document Type: Article

References (86)

1. Alonso A, Klink R. 1993. Differential electroresponsiveness of stellate and pyramidal-like cells of medial entorhinal cortex layer II. J Neurophysiol 70: 128-143.
2. Alonso A, Llinas RR. 1989. Subthreshold Na+-dependent theta-like rhythmicity in stellate cells of entorhinal cortex layer II. Nature 342: 175-177.
3. Arrang JM, Drutel G, Schwartz JC. 1995. Characterization of histamine H3 receptors regulating acetylcholine release in rat entorhinal cortex. Br J Pharmacol 114: 1518-1522.
4. Arrigoni E, Chamberlin NL, Saper CB, McCarley RW. 2006. Adenosine inhibits basal forebrain cholinergic and noncholinergic neurons in vitro. Neuroscience 140: 403-413.
5. Avsar E, Empson RM. 2004. Adenosine acting via A1 receptors, controls the transition to status epilepticus-like behaviour in an in vitro model of epilepsy. Neuropharmacology 47: 427-437.
6. Bagley EE, Vaughan CW, Christie MJ. 1999. Inhibition by adenosine receptor agonists of synaptic transmission in rat periaqueductal grey neurons. J Physiol 516 (Part 1): 219-225.
7. Bailey SJ, Dhillon A, Woodhall GL, Jones RS. 2004. Lamina-specific differences in GABA(B) autoreceptor-mediated regulation of spontaneous GABA release in rat entorhinal cortex. Neuropharmacology 46: 31-42.
8. Ballarin M, Fredholm BB, Ambrosio S, Mahy N. 1991. Extracellular levels of adenosine and its metabolites in the striatum of awake rats: inhibition of uptake and metabolism. Acta Physiol Scand 142: 97-103.
9. Barry C, Hayman R, Burgess N, Jeffery KJ. 2007. Experience-dependent rescaling of entorhinal grids. Nat Neurosci 10: 682-684.
10. Beaumont V, Zucker RS. 2000. Enhancement of synaptic transmission by cyclic AMP modulation of presynaptic Ih channels. Nat Neurosci 3: 133-141.
11. Bender RA, Kirschstein T, Kretz O, Brewster AL, Richichi C, Ruschenschmidt C, Shigemoto R, Beck H, Frotscher M, Baram TZ. 2007. Localization of HCN1 channels to presynaptic compartments: Novel plasticity that may contribute to hippocampal maturation. J Neurosci 27: 4697-4706.
12. Berretta N, Jones RS. 1996. A comparison of spontaneous EPSCs in layer II, layer IV-V neurons of the rat entorhinal cortex in vitro. J Neurophysiol 76: 1089-1100.
13. Boison D. 2008. Adenosine as a neuromodulator in neurological diseases. Curr Opin Pharmacol 8: 2-7.
14. Boonstra TW, Stins JF, Daffertshofer A, Beek PJ. 2007. Effects of sleep deprivation on neural functioning: an integrative review. Cell Mol Life Sci 64: 934-946.
15. Bramley JR, Sollars PJ, Pickard GE, Dudek FE. 2005. 5-HT1B receptor-mediated presynaptic inhibition of GABA release in the suprachiasmatic nucleus. J Neurophysiol 93: 3157-3164.
16. Brun VH, Leutgeb S, Wu HQ, Schwarcz R, Witter MP, Moser EI, Moser MB. 2008. Impaired spatial representation in CA1 after lesion of direct input from entorhinal cortex. Neuron 57: 290-302.
17. Burwell RD. 2000. The parahippocampal region: Corticocortical connectivity. Ann NY Acad Sci 911: 25-42.
18. Caruana DA, Sorge RE, Stewart J, Chapman CA. 2006. Dopamine has bidirectional effects on synaptic responses to cortical inputs in layer II of the lateral entorhinal cortex. J Neurophysiol 96: 3006-3015.
19. Chen G, van den Pol AN. 1997. Adenosine modulation of calcium currents and presynaptic inhibition of GABA release in suprachiasmatic and arcuate nucleus neurons. J Neurophysiol 77: 3035-3047.
20. Chen XW, Mu Y, Huang HP, Guo N, Zhang B, Fan SY, Xiong JX, Wang SR, Xiong W, Huang W, Liu T, Zheng LH, Zhang CX, Li LH, Yu ZP, Hu ZA, Zhou Z. 2008. Hypocretin-1 potentiates NMDA receptor-mediated somatodendritic secretion from locus ceruleus neurons. J Neurosci 28: 3202-3208.
21. Clark BD, Kurth-Nelson ZL, Newman EA. 2009. Adenosine-evoked hyperpolarization of retinal ganglion cells is mediated by g-protein-coupled inwardly rectifying K+ and small conductance Ca2+-activated K+ channel activation. J Neurosci 29: 11237-11245.
22. Cunha RA. 2001. Adenosine as a neuromodulator and as a homeostatic regulator in the nervous system: Different roles, different sources and different receptors. Neurochem Int 38: 107-125.
23. Deng PY, Lei S. 2007. Long-term depression in identified stellate neurons of juvenile rat entorhinal cortex. J Neurophysiol 97: 727-737.
24. Deng PY, Poudel SK, Rojanathammanee L, Porter JE, Lei S. 2007. Serotonin inhibits neuronal excitability by activating two-pore domain k+ channels in the entorhinal cortex. Mol Pharmacol 72: 208-218.
25. Deng PY, Xiao Z, Yang C, Rojanathammanee L, Grisanti L, Watt J, Geiger JD, Liu R, Porter JE, Lei S. 2009. GABA(B) receptor activation inhibits neuronal excitability and spatial learning in the entorhinal cortex by activating TREK-2 K+ channels. Neuron 63: 230-243.
26. Dunwiddie TV, Masino SA. 2001. The role and regulation of adenosine in the central nervous system. Annu Rev Neurosci 24: 31-55.
27. Fellous JM, Rudolph M, Destexhe A, Sejnowski TJ. 2003. Synaptic background noise controls the input/output characteristics of single cells in an in vitro model of in vivo activity. Neuroscience 122: 811-829.
28. Fontanez DE, Porter JT. 2006. Adenosine A1 receptors decrease thalamic excitation of inhibitory and excitatory neurons in the barrel cortex. Neuroscience 137: 1177-1184.
29. Garden DL, Dodson PD, O'Donnell C, White MD, Nolan MF. 2008. Tuning of synaptic integration in the medial entorhinal cortex to the organization of grid cell firing fields. Neuron 60: 875-889.
30. Genlain M, Godaux E, Ris L. 2007. Involvement of hyperpolarization-activated cation channels in synaptic modulation. Neuroreport 18: 1231-1235.
31. Halassa MM, Florian C, Fellin T, Munoz JR, Lee SY, Abel T, Haydon PG, Frank MG. 2009. Astrocytic modulation of sleep homeostasis and cognitive consequences of sleep loss. Neuron 61: 213-219.
32. Hosseinmardi N, Mirnajafi-Zadeh J, Fathollahi Y, Shahabi P. 2007. The role of adenosine A1 and A2A receptors of entorhinal cortex on piriform cortex kindled seizures in rats. Pharmacol Res 56: 110-117.
33. Insausti R, Herrero MT, Witter MP. 1997. Entorhinal cortex of the rat: cytoarchitectonic subdivisions and the origin and distribution of cortical efferents. Hippocampus 7: 146-183.
34. Jeong HJ, Jang IS, Nabekura J, Akaike N. 2003. Adenosine A1 receptor-mediated presynaptic inhibition of GABAergic transmission in immature rat hippocampal CA1 neurons. J Neurophysiol 89: 1214-1222.
35. Jones BE. 2009. Glia, adenosine, and sleep. Neuron 61: 156-157.
36. Lao LJ, Kumamoto E, Luo C, Furue H, Yoshimura M. 2001. Adenosine inhibits excitatory transmission to substantia gelatinosa neurons of the adult rat spinal cord through the activation of presynaptic A(1) adenosine receptor. Pain 94: 315-324.
37. Lavenex P, Amaral DG. 2000. Hippocampal-neocortical interaction: a hierarchy of associativity. Hippocampus 10: 420-430.
38. Lee JG, Choi IS, Park EJ, Cho JH, Lee MG, Choi BJ, Jang IS. 2007. Beta(2)-Adrenoceptor-mediated facilitation of glutamatergic transmission in rat ventromedial hypothalamic neurons. Neuroscience 144: 1255-1265.
39. Lei S, Deng PY, Porter JE, Shin HS. 2007. Adrenergic facilitation of GABAergic transmission in rat entorhinal cortex. J Neurophysiol 98: 2868-2877.
40. Leonard BW, Amaral DG, Squire LR, Zola-Morgan S. 1995. Transient memory impairment in monkeys with bilateral lesions of the entorhinal cortex. J Neurosci 15: 5637-5659.
41. Leutgeb JK, Frey JU, Behnisch T. 2003. LTP in cultured hippocampal-entorhinal cortex slices from young adult (P25-30) rats. J Neurosci Methods 130: 19-32.
42. Liu ZW, Gao XB. 2007. Adenosine inhibits activity of hypocretin/orexin neurons by the A1 receptor in the lateral hypothalamus: A possible sleep-promoting effect. J Neurophysiol 97: 837-848.
43. Lopes LV, Halldner L, Rebola N, Johansson B, Ledent C, Chen JF, Fredholm BB, Cunha RA. 2004. Binding of the prototypical adenosine A(2A) receptor agonist CGS 21680 to the cerebral cortex of adenosine A(1) and A(2A) receptor knockout mice. Br J Pharmacol 141: 1006-1014.
44. Lupica CR, Bell JA, Hoffman AF, Watson PL. 2001. Contribution of the hyperpolarization-activated current (I(h)) to membrane potential and GABA release in hippocampal interneurons. J Neurophysiol 86: 261-268.
45. Materi LM, Rasmusson DD, Semba K. 2000. Inhibition of synaptically evoked cortical acetylcholine release by adenosine: An in vivo microdialysis study in the rat. Neuroscience 97: 219-226.
46. Mohammad-Zadeh M, Amini A, Mirnajafi-Zadeh J, Fathollahi Y. 2005. The role of adenosine A(1) receptors in the interaction between amygdala and entorhinal cortex of kindled rats. Epilepsy Res 65(1-2): 1-9.
47. Nolan MF, Dudman JT, Dodson PD, Santoro B. 2007. HCN1 channels control resting and active integrative properties of stellate cells from layer II of the entorhinal cortex. J Neurosci 27: 12440-12451.
48. Oliet SH, Poulain DA. 1999. Adenosine-induced presynaptic inhibition of IPSCs and EPSCs in rat hypothalamic supraoptic nucleus neurones. J Physiol 520(Part 3): 815-825.
49. Pan WJ, Osmanovic SS, Shefner SA. 1995. Characterization of the adenosine A1 receptor-activated potassium current in rat locus ceruleus neurons. J Pharmacol Exp Ther 273: 537-544.
50. Pape HC. 1992. Adenosine promotes burst activity in guinea-pig geniculocortical neurones through two different ionic mechanisms. J Physiol 447: 729-753.
51. Pazzagli M, Corsi C, Latini S, Pedata F, Pepeu G. 1994. In vivo regulation of extracellular adenosine levels in the cerebral cortex by NMDA and muscarinic receptors. Eur J Pharmacol 254: 277-282.
52. Pazzagli M, Corsi C, Fratti S, Pedata F, Pepeu G. 1995. Regulation of extracellular adenosine levels in the striatum of aging rats. Brain Res 684: 103-106.
53. Ponzio TA, Hatton GI. 2005. Adenosine postsynaptically modulates supraoptic neuronal excitability. J Neurophysiol 93: 535-547.
54. Porkka-Heiskanen T, Strecker RE, McCarley RW. 2000. Brain site-specificity of extracellular adenosine concentration changes during sleep deprivation and spontaneous sleep: An in vivo microdialysis study. Neuroscience 99: 507-517.
55. Porkka-Heiskanen T, Strecker RE, Thakkar M, Bjorkum AA, Greene RW, McCarley RW. 1997. Adenosine: A mediator of the sleep-inducing effects of prolonged wakefulness. Science 276: 1265-1268.
56. Rainnie DG, Grunze HC, McCarley RW, Greene RW. 1994. Adenosine inhibition of mesopontine cholinergic neurons: Implications for EEG arousal. Science 263: 689-692.
57. Ribeiro JA, Sebastiao AM, de Mendonca A. 2002. Adenosine receptors in the nervous system: Pathophysiological implications. Prog Neurobiol 68: 377-392.
58. Rivkees SA, Price SL, Zhou FC. 1995. Immunohistochemical detection of A1 adenosine receptors in rat brain with emphasis on localization in the hippocampal formation, cerebral cortex, cerebellum, and basal ganglia. Brain Res 677: 193-203.
59. Robinson RB, Siegelbaum SA. 2003. Hyperpolarization-activated cation currents: From molecules to physiological function. Annu Rev Physiol 65: 453-480.
60. Sadja R, Alagem N, Reuveny E. 2003. Gating of GIRK channels: details of an intricate, membrane-delimited signaling complex. Neuron 39: 9-12.
61. Safiulina VF, Kasyanov AM, Giniatullin R, Cherubini E. 2005. Adenosine down-regulates giant depolarizing potentials in the developing rat hippocampus by exerting a negative control on glutamatergic inputs. J Neurophysiol 94: 2797-2804.
62. Salin PA, Prince DA. 1996. Spontaneous GABAA receptor-mediated inhibitory currents in adult rat somatosensory cortex. J Neurophysiol 75: 1573-1588.
63. Shalinsky MH, Magistretti J, Ma L, Alonso AA. 2002. Muscarinic activation of a cation current and associated current noise in entorhinal-cortex layer-II neurons. J Neurophysiol 88: 1197-1211.
64. Shen KZ, Johnson SW. 2003. Presynaptic inhibition of synaptic transmission by adenosine in rat subthalamic nucleus in vitro. Neuroscience 116: 99-106.
65. Solstad T, Boccara CN, Kropff E, Moser MB, Moser EI. 2008. Representation of geometric borders in the entorhinal cortex. Science 322: 1865-1868.
66. Steffenach HA, Witter M, Moser MB, Moser EI. 2005. Spatial memory in the rat requires the dorsolateral band of the entorhinal cortex. Neuron 45: 301-313.
67. Stern CE, Sherman SJ, Kirchhoff BA, Hasselmo ME. 2001. Medial temporal and prefrontal contributions to working memory tasks with novel and familiar stimuli. Hippocampus 11: 337-346.
68. Strecker RE, Morairty S, Thakkar MM, Porkka-Heiskanen T, Basheer R, Dauphin LJ, Rainnie DG, Portas CM, Greene RW, McCarley RW. 2000. Adenosinergic modulation of basal forebrain and preoptic/anterior hypothalamic neuronal activity in the control of behavioral state. Behav Brain Res 115: 183-204.
69. Thakkar MM, Delgiacco RA, Strecker RE, McCarley RW. 2003. Adenosinergic inhibition of basal forebrain wakefulness-active neurons: A simultaneous unit recording and microdialysis study in freely behaving cats. Neuroscience 122: 1107-1113.
70. Uchimura N, North RA. 1991. Baclofen and adenosine inhibit synaptic potentials mediated by gamma-aminobutyric acid and glutamate release in rat nucleus accumbens. J Pharmacol Exp Ther 258: 663-668.
71. Ulrich D, Huguenard JR. 1995. Purinergic inhibition of GABA and glutamate release in the thalamus: Implications for thalamic network activity. Neuron 15: 909-918.
72. Van der Kloot W. 1991. The regulation of quantal size. Prog Neurobiol 36: 93-130.
73. Van Dort CJ, Baghdoyan HA, Lydic R. 2009. Adenosine A(1) and A(2A) receptors in mouse prefrontal cortex modulate acetylcholine release and behavioral arousal. J Neurosci 29: 871-881.
74. Wetherington JP, Lambert NA. 2002. Differential desensitization of responses mediated by presynaptic and postsynaptic A1 adenosine receptors. J Neurosci 22: 1248-1255.
75. Witter MP, Groenewegen HJ, Lopes da Silva FH, Lohman AH. 1989. Functional organization of the extrinsic and intrinsic circuitry of the parahippocampal region. Prog Neurobiol 33: 161-253.
76. Woodhall GL, Bailey SJ, Thompson SE, Evans DI, Jones RS. 2005. Fundamental differences in spontaneous synaptic inhibition between deep and superficial layers of the rat entorhinal cortex. Hippocampus 15: 232-245.
77. Wu LG, Saggau P. 1997. Presynaptic inhibition of elicited neurotransmitter release. Trends Neurosci 20: 204-212.
78. Xia J, Chen F, Ye J, Yan J, Wang H, Duan S, Hu Z. 2009. Activity-dependent release of adenosine inhibits the glutamatergic synaptic transmission and plasticity in the hypothalamic hypocretin/orexin neurons. Neuroscience 162: 980-988.
79. Xiao Z, Deng PY, Rojanathammanee L, Yang C, Grisanti L, Permpoonputtana K, Weinshenker D, Doze VA, Porter JE, Lei S. 2009a. Noradrenergic depression of neuronal excitability in the entorhinal cortex via activation of TREK-2 K+ channels. J Biol Chem 284: 10980-10991.
80. Xiao Z, Deng PY, Yang C, Lei S. 2009b. Modulation of GABAergic transmission by muscarinic receptors in the entorhinal cortex of juvenile rats. J Neurophysiol 102: 659-669.
81. Xu C, Datta S, Wu M, Alreja M. 2004. Hippocampal theta rhythm is reduced by suppression of the H-current in septohippocampal GABAergic neurons. Eur J Neurosci 19: 2299-2309.
82. Yan Jie CF, Jia Xiao-Jun, Li Bo, Chen Xiao-Wei, Hu Zhi-An. 2008. Adenosine inhibits hyperpolarization-activated current in the pyramid neurons of prefrontal cortex. Acta Academiae Medicinae Militaris Tertiae 30: 903-905.
83. Yang K, Fujita T, Kumamoto E. 2004. Adenosine inhibits GABAergic and glycinergic transmission in adult rat substantia gelatinosa neurons. J Neurophysiol 92: 2867-2877.
84. Young BJ, Otto T, Fox GD, Eichenbaum H. 1997. Memory representation within the parahippocampal region. J Neurosci 17: 5183-5195.
85. Yum DS, Cho JH, Choi IS, Nakamura M, Lee JJ, Lee MG, Choi BJ, Choi JK, Jang IS. 2008. Adenosine A1 receptors inhibit GABAergic transmission in rat tuberomammillary nucleus neurons. J Neurochem 106: 361-371.
86. Zhong P, Yan Z. 2004. Chronic antidepressant treatment alters serotonergic regulation of GABA transmission in prefrontal cortical pyramidal neurons. Neuroscience 129: 65-73.