Activation of α1-adrenoceptors enhances excitatory synaptic transmission via a pre- and postsynaptic protein kinase C-dependent mechanism in the medial prefrontal cortex of rats

European Journal of Neuroscience

Volumn 39, Issue 8, 2014, Pages 1281-1293

  Luo, Fei ^a   Tang, Hua ^b   Li, Bao ming ^a,b   Li, Si hai ^b  

^a FUDAN UNIVERSITY   (China)

^b NANCHANG UNIVERSITY   (China)

Author keywords

Excitatory synaptic transmission; Medial prefrontal cortex; Rat

Indexed keywords

ALPHA 1 ADRENERGIC RECEPTOR; AMPA RECEPTOR; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PHOSPHOLIPASE C; PROTEIN KINASE C; ALPHA 1 ADRENERGIC RECEPTOR STIMULATING AGENT; PHENYLEPHRINE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; FACILITATION; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN FUNCTION; PYRAMIDAL NERVE CELL; RAT; RECEPTOR UPREGULATION; SYNAPTIC TRANSMISSION; ANIMAL; CYTOLOGY; DRUG EFFECTS; METABOLISM; MINIATURE ENDPLATE POTENTIAL; PHYSIOLOGY; SPRAGUE DAWLEY RAT; SYNAPSE;

ADRENERGIC ALPHA-1 RECEPTOR AGONISTS; ANIMALS; EXCITATORY POSTSYNAPTIC POTENTIALS; MINIATURE POSTSYNAPTIC POTENTIALS; PHENYLEPHRINE; PREFRONTAL CORTEX; PROTEIN KINASE C; PYRAMIDAL CELLS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, ADRENERGIC, ALPHA-1; RECEPTORS, AMPA; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPSES;

EID: 84899103991     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.12495     Document Type: Article

References (48)

1. Amargos-Bosch, M., Adell, A., Bortolozzi, A. & Artigas, F. (2003) Stimulation of alpha1-adrenoceptors in the rat medial prefrontal cortex increases the local in vivo 5-hydroxytryptamine release: reversal by antipsychotic drugs. J. Neurochem., 87, 831-842.
2. Arnsten, A.F. & Li, B.-M. (2005) Neurobiology of executive functions: catecholamine influences on prefrontal cortical functions. Biol. Psychiat., 57, 1377-1384.
3. Arnsten, A.F., Mathew, R., Ubriani, R., Taylor, J.R. & Li, B.M. (1999) Alpha-1 noradrenergic receptor stimulation impairs prefrontal cortical cognitive function. Biol. Psychiat., 45, 26-31.
4. Arnsten, A.F., Wang, M.J. & Paspalas, C.D. (2012) Neuromodulation of thought: flexibilities and vulnerabilities in prefrontal cortical network synapses. Neuron, 76, 223-239.
5. Babiec, W.E., Faull, K.F. & Feldman, J.L. (2012) Cyclothiazide-induced persistent increase in respiratory-related activity in vitro. J. Physiol., 590, 4897-4915.
6. Birnbaum, S., Gobeske, K.T., Auerbach, J., Taylor, J.R. & Arnsten, A. (1999) A role for norepinephrine in stress-induced cognitive deficits: alpha-1-adrenoceptor mediation in the prefrontal cortex. Biol. Psychiat., 46, 1266-1273.
7. Birnbaum, S.G., Yuan, P., Wang, M., Vijayraghavan, S., Bloom, A., Davis, D., Gobeske, K., Sweatt, J., Manji, H. & Arnsten, A. (2004) Protein kinase C overactivity impairs prefrontal cortical regulation of working memory. Science, 306, 882-884.
8. Bodner, M., Shafi, M., Zhou, Y.D. & Fuster, J. (2005) Patterned firing of parietal cells in a haptic working memory task. Eur. J. Neurosci., 21, 2538-2546.
9. Caetano, M.S., Jin, L.E., Harenberg, L., Stachenfeld, K.L., Arnsten, A.F. & Laubach, M. (2012) Noradrenergic control of error perseveration in medial prefrontal cortex. Front. Integr. Neurosci., 6, 125-133.
10. Chen, Q., Li, D.-P. & Pan, H.-L. (2006) Presynaptic α1 adrenergic receptors differentially regulate synaptic glutamate and GABA release to hypothalamic presympathetic neurons. J. Pharmacol. Exp. Ther., 316, 733-742.
11. Evans, D.I., Jones, R.S. & Woodhall, G. (2001) Differential actions of PKA and PKC in the regulation of glutamate release by group III mGluRs in the entorhinal cortex. J. Neurophysiol., 85, 571-579.
12. Funahashi, S., Bruce, C.J. & Goldman-Rakic, P.S. (1989) Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex. J. Neurophysiol., 61, 331-349.
13. Fuster, J.M., Bodner, M. & Kroger, J.K. (2000) Cross-modal and cross-temporal association in neurons of frontal cortex. Nature, 405, 347-351.
14. Fuxe, K., Hamberger, B. & Hökfelt, T. (1968) Distribution of noradrenaline nerve terminals in cortical areas of the rat. Brain Res., 8, 125-131.
15. Goldman-Rakic, P.S. (1995a) Cellular basis of working memory. Neuron, 14, 477-485.
16. Goldman-Rakic, P.S. (1995b) Architecture of the prefrontal cortex and the central executive. Ann. NY Acad. Sci., 769, 71-84.
17. Goldstein, L.E., Rasmusson, A.M., Bunney, B.S. & Roth, R.H. (1996) Role of the amygdala in the coordination of behavioral, neuroendocrine, and prefrontal cortical monoamine responses to psychological stress in the rat. J. Neurosci., 16, 4787-4798.
18. Gordon, G.R. & Bains, J.S. (2005) Noradrenaline triggers multivesicular release at glutamatergic synapses in the hypothalamus. J. Neurosci., 25, 11385-11395.
19. Han, S.K., Chong, W., Li, L.H., Lee, I.S., Murase, K. & Ryu, P.D. (2002) Noradrenaline excites and inhibits GABAergic transmission in parvocellular neurons of rat hypothalamic paraventricular nucleus. J. Neurophysiol., 87, 2287-2296.
20. Hardingham, G.E. & Bading, H. (2003) The Yin and Yang of NMDA receptor signalling. Trends Neurosci., 26, 81-89.
21. Heidbreder, C.A. & Groenewegen, H.J. (2003) The medial prefrontal cortex in the rat: evidence for a dorso-ventral distinction based upon functional and anatomical characteristics. Neurosci. Biobehav. R., 27, 555-579.
22. Herbert, J.M., Augereau, J.M., Gleye, J. & Maffrand, J.P. (1990) Chelerythrine is a potent and specific inhibitor of protein kinase C. Biochem. Bioph. Res. Co., 172, 993-999.
23. Jett, J.D. & Morilak, D.A. (2013) Too much of a good thing: blocking noradrenergic facilitation in medial prefrontal cortex prevents the detrimental effects of chronic stress on cognition. Neuropsychopharmacol., 38, 585-595.
24. Kobayashi, M., Sasabe, T., Shiohama, Y. & Koshikawa, N. (2008) Activation of α1-adrenoceptors increases firing frequency through protein kinase C in pyramidal neurons of rat visual cortex. Neurosci. Lett., 430, 175-180.
25. Lan, J.Y., Skeberdis, V.A., Jover, T., Grooms, S.Y., Lin, Y., Araneda, R.C., Zheng, X., Bennett, M.V. & Zukin, R.S. (2001) Protein kinase C modulates NMDA receptor trafficking and gating. Nat. Neurosci., 4, 382-390.
26. Lindvall, O., Björklund, A. & Skagerberg, G. (1984) Selective histochemical demonstration of dopamine terminal systems in rat di-and telecephalon: new evidence for dopaminergic innervation of hypothalamic neurosecretory nuclei. Brain Res., 306, 19-30.
27. Liu, W., Yuen, E.Y., Allen, P.B., Feng, J., Greengard, P. & Yan, Z. (2006) Adrenergic modulation of NMDA receptors in prefrontal cortex is differentially regulated by RGS proteins and spinophilin. Proc. Natl. Acad. Sci. USA, 103, 18338-18343.
28. Manabe, T., Wyllie, D., Perkel, D.J. & Nicoll, R.A. (1993) Modulation of synaptic transmission and long-term potentiation: effects on paired pulse facilitation and EPSC variance in the CA1 region of the hippocampus. J. Neurophysiol., 70, 1451-1459.
29. Mao, Z.-M., Arnsten, A.F. & Li, B.-M. (1999) Local infusion of an αlpha-1 adrenergic agonist into the prefrontal cortex impairs spatial working memory performance in monkeys. Biol. Psychiat., 46, 1259-1265.
30. 1-adrenoceptor activation induces excitatory postsynaptic currents in layer V pyramidal cells of the medial prefrontal cortex. Eur. J. Pharmacol., 367, 197-206.
31. Mcdonald, B.J., Chung, H.J. & Huganir, R.L. (2001) Identification of protein kinase C phosphorylation sites within the AMPA receptor GluR2 subunit. Neuropharmacology, 41, 672-679.
32. Mckenna, B.S. & Eyler, L.T. (2012) Overlapping prefrontal systems involved in cognitive and emotional processing in euthymic bipolar disorder and following sleep deprivation: a review of functional neuroimaging studies. Clin. Psychol. Rev., 32, 650-663.
33. Medgett, I. & Langer, S. (1984) Heterogeneity of smooth muscle alpha adrenoceptors in rat tail artery in vitro. J. Pharmacol. Exp. Ther., 229, 823-830.
34. Miller, E.K. & Cohen, J.D. (2001) An integrative theory of prefrontal cortex function. Annu. Rev. Neurosci., 24, 167-202.
35. Minzenberg, M.J. (2012) Pharmacotherapy for attention-deficit/hyperactivity disorder: from cells to circuits. Neurotherapeutics, 9, 610-621.
36. Mouradian, R.D., Sessler, F.M. & Waterhouse, B.D. (1991) Noradrenergic potentiation of excitatory transmitter action in cerebrocortical slices: evidence for mediation by an α1 receptor-linked second messenger pathway. Brain Res., 546, 83-95.
37. Ozawa, S. (2007) Role of glutamate transporters in excitatory synapses in cerebellar Purkinje cells. Brain Nerve, 59, 669-676.
38. Paxinos, G. & Watson, C. (1986) The Rat Brain in Stereotaxic Coordinates, 2nd edn. Academic Press, New York, NY.
39. Ramos, B.P. & Arnsten, A.F. (2007) Adrenergic pharmacology and cognition: focus on the prefrontal cortex. Pharmacol. Therapeut., 113, 523-536.
40. Rotenberg, S.A., Huang, M.H., Zhu, J., Su, L. & Riedel, H. (1995) Deletion analysis of protein kinase C inactivation by calphostin C. Mol. Carcinogen., 12, 42-49.
41. Szot, P., White, S.S., Greenup, J.L., Leverenz, J.B., Peskind, E.R. & Raskind, M.A. (2007) Changes in adrenoreceptors in the prefrontal cortex of subjects with dementia: evidence of compensatory changes. Neuroscience, 146, 471-480.
42. Tamaoki, T. (1991) Use and specificity of staurosporine, UCN-01, and calphostin C as protein kinase inhibitors. Method. Enzymol., 201, 340-347.
43. Waterhouse, B., Moises, H. & Woodward, D. (1981) Alpha-receptor-mediated facilitation of somatosensory cortical neuronal responses to excitatory synaptic inputs and iontophoretically applied acetylcholine. Neuropharmacology, 20, 907-920.
44. Yan, J.Z., Xu, Z., Ren, S.Q., Hu, B., Yao, W., Wang, S.H., Liu, S.Y. & Lu, W. (2011) Protein kinase C promotes N-methyl-D-aspartate (NMDA) receptor trafficking by indirectly triggering calcium/calmodulin-dependent protein kinase II (CaMKII) autophosphorylation. J. Biol. Chem., 286, 25187-25200.
45. Yi, F., Liu, S.S., Luo, F., Zhang, X.H. & Li, B.M. (2013) Signaling mechanism underlying alpha2A -adrenergic suppression of excitatory synaptic transmission in the medial prefrontal cortex of rats. Eur. J. Neurosci., 38, 2364-2373.
46. Yuen, E.Y., Jiang, Q., Chen, P., Gu, Z., Feng, J. & Yan, Z. (2005) Serotonin 5-HT1A receptors regulate NMDA receptor channels through a microtubule-dependent mechanism. J. Neurosci., 25, 5488-5501.
47. Zhang, Z., Cordeiro Matos, S., Jego, S., Adamantidis, A. & Seguela, P. (2013) Norepinephrine drives persistent activity in prefrontal cortex via synergistic alpha1 and alpha2 adrenoceptors. PLoS One, 8, e66122.
48. Zucker, R.S. & Regehr, W.G. (2002) Short-term synaptic plasticity. Annu. Rev. Physiol., 64, 355-405.