DOI QR코드

DOI QR Code

Developmental Switch of the Serotonergic Role in the Induction of Synaptic Long-term Potentiation in the Rat Visual Cortex

  • Park, Sung-Won (Department of Physiology, College of Medicine, The Catholic University of Korea) ;
  • Jang, Hyun-Jong (Department of Physiology, College of Medicine, The Catholic University of Korea) ;
  • Cho, Kwang-Hyun (Department of Physiology, College of Medicine, The Catholic University of Korea) ;
  • Kim, Myung-Jun (Department of Physiology, College of Medicine, The Catholic University of Korea) ;
  • Yoon, Shin-Hee (Department of Physiology, College of Medicine, The Catholic University of Korea) ;
  • Rhie, Duck-Joo (Department of Physiology, College of Medicine, The Catholic University of Korea)
  • Received : 2012.01.16
  • Accepted : 2012.02.16
  • Published : 2012.02.29

Abstract

Synaptic long-term potentiation (LTP) and long-term depression (LTD) have been studied as mechanisms of ocular dominance plasticity in the rat visual cortex. Serotonin (5-hydroxytryptamine, 5-HT) inhibits the induction of LTP and LTD during the critical period of the rat visual cortex (postnatal 3~5 weeks). However, in adult rats, the increase in 5-HT level in the brain by the administration of the selective serotonin reuptake inhibitor (SSRI) fluoxetine reinstates ocular dominance plasticity and LTP in the visual cortex. Here, we investigated the effect of 5-HT on the induction of LTP in the visual cortex obtained from 3- to 10-week-old rats. Field potentials in layer 2/3, evoked by the stimulation of underlying layer 4, was potentiated by theta-burst stimulation (TBS) in 3- and 5-weekold rats, then declined to the baseline level with aging to 10 weeks. Whereas 5-HT inhibited the induction of LTP in 5-week-old rats, it reinstated the induction of N-methyl-D-aspartate receptor (NMDA)-dependent LTP in 8- and 10-week-old rats. Moreover, the selective SSRI citalopram reinstated LTP. The potentiating effect of 5-HT at 8 weeks of age was mediated by the activation of 5-$HT_2$ receptors, but not by the activation of either 5-$HT_{1A}$ or 5-$HT_3$ receptors. These results suggested that the effect of 5-HT on the induction of LTP switches from inhibitory in young rats to facilitatory in adult rats.

Keywords

References

  1. Barnes NM, Sharp T. A review of central 5-HT receptors and their function. Neuropharmacology. 1999;38:1083-1152. https://doi.org/10.1016/S0028-3908(99)00010-6
  2. Malenka RC, Bear MF. LTP and LTD: an embarrassment of riches. Neuron. 2004;44:5-21. https://doi.org/10.1016/j.neuron.2004.09.012
  3. Dori I, Dinopoulos A, Blue ME, Parnavelas JG. Regional differences in the ontogeny of the serotonergic projection to the cerebral cortex. Exp Neurol. 1996;138:1-14. https://doi.org/10.1006/exnr.1996.0041
  4. Kojic L, Dyck RH, Gu Q, Douglas RM, Matsubara J, Cynader MS. Columnar distribution of serotonin-dependent plasticity within kitten striate cortex. Proc Natl Acad Sci USA. 2000;97:1841-1844. https://doi.org/10.1073/pnas.97.4.1841
  5. Kirkwood A. Serotonergic control of developmental plasticity. Proc Natl Acad Sci USA. 2000;97:1951-1952. https://doi.org/10.1073/pnas.070044697
  6. Rittenhouse CD, Shouval HZ, Paradiso MA, Bear MF. Monocular deprivation induces homosynaptic long-term depression in visual cortex. Nature. 1999;397:347-350. https://doi.org/10.1038/16922
  7. Bear MF, Rittenhouse CD. Molecular basis for induction of ocular dominance plasticity. J Neurobiol. 1999;41:83-91. https://doi.org/10.1002/(SICI)1097-4695(199910)41:1<83::AID-NEU11>3.0.CO;2-Z
  8. Fagiolini M, Katagiri H, Miyamoto H, Mori H, Grant SG, Mishina M, Hensch TK. Separable features of visual cortical plasticity revealed by N-methyl-D-aspartate receptor 2A signaling. Proc Natl Acad Sci USA. 2003;100:2854-2859. https://doi.org/10.1073/pnas.0536089100
  9. Hensch TK. Critical period plasticity in local cortical circuits. Nat Rev Neurosci. 2005;6:877-888.
  10. Gu Q, Singer W. Involvement of serotonin in developmental plasticity of kitten visual cortex. Eur J Neurosci. 1995;7:1146-1153. https://doi.org/10.1111/j.1460-9568.1995.tb01104.x
  11. Kim HS, Jang HJ, Cho KH, Hahn SJ, Kim MJ, Yoon SH, Jo YH, Kim MS, Rhie DJ. Serotonin inhibits the induction of NMDA receptor-dependent long-term potentiation in the rat primary visual cortex. Brain Res. 2006;1103:49-55. https://doi.org/10.1016/j.brainres.2006.05.046
  12. Jang HJ, Cho KH, Park SW, Kim MJ, Yoon SH, Rhie DJ. Effects of serotonin on the induction of long-term depression in the rat visual cortex. Korean J Physiol Pharmacol. 2010;14:337-343. https://doi.org/10.4196/kjpp.2010.14.5.337
  13. Edagawa Y, Saito H, Abe K. Endogenous serotonin contributes to a developmental decrease in long-term potentiation in the rat visual cortex. J Neurosci. 2001;21:1532-1537.
  14. Edagawa Y, Saito H, Abe K. The serotonin 5-HT2 receptorphospholipase C system inhibits the induction of long-term potentiation in the rat visual cortex. Eur J Neurosci. 2000;12:1391-1396. https://doi.org/10.1046/j.1460-9568.2000.00007.x
  15. Edagawa Y, Saito H, Abe K. 5-HT1A receptor-mediated inhibition of long-term potentiation in rat visual cortex. Eur J Pharmacol. 1998;349:221-224. https://doi.org/10.1016/S0014-2999(98)00286-6
  16. Staubli U, Otaky N. Serotonin controls the magnitude of LTP induced by theta bursts via an action on NMDA-receptormediated responses. Brain Res. 1994;643:10-16. https://doi.org/10.1016/0006-8993(94)90003-5
  17. Pollandt S, Drephal C, Albrecht D. 8-OH-DPAT suppresses the induction of LTP in brain slices of the rat lateral amygdala. Neuroreport. 2003;14:895-897. https://doi.org/10.1097/00001756-200305060-00025
  18. Ohashi S, Matsumoto M, Togashi H, Ueno K, Yoshioka M. The serotonergic modulation of synaptic plasticity in the rat hippocampo- medial prefrontal cortex pathway. Neurosci Lett. 2003; 342:179-182. https://doi.org/10.1016/S0304-3940(03)00293-3
  19. Maya Vetencourt JF, Sale A, Viegi A, Baroncelli L, De Pasquale R, O'Leary OF, Castrén E, Maffei L. The antidepressant fluoxetine restores plasticity in the adult visual cortex. Science. 2008;320:385-388. https://doi.org/10.1126/science.1150516
  20. Maya Vetencourt JF, Tiraboschi E, Spolidoro M, Castrén E, Maffei L. Serotonin triggers a transient epigenetic mechanism that reinstates adult visual cortex plasticity in rats. Eur J Neurosci. 2011;33:49-57. https://doi.org/10.1111/j.1460-9568.2010.07488.x
  21. Li QH, Nakadate K, Tanaka-Nakadate S, Nakatsuka D, Cui Y, Watanabe Y. Unique expression patterns of 5-HT2A and 5-HT2C receptors in the rat brain during postnatal development: Western blot and immunohistochemical analyses. J Comp Neurol. 2004;469:128-140. https://doi.org/10.1002/cne.11004
  22. Jang HJ, Cho KH, Kim HS, Hahn SJ, Kim MS, Rhie DJ. Age-dependent decline in supragranular long-term synaptic plasticity by increased inhibition during the critical period in the rat primary visual cortex. J Neurophysiol. 2009;101:269-275.
  23. Kirkwood A, Silva A, Bear MF. Age-dependent decrease of synaptic plasticity in the neocortex of alphaCaMKII mutant mice. Proc Natl Acad Sci USA. 1997;94:3380-3383. https://doi.org/10.1073/pnas.94.7.3380
  24. Jang HJ, Cho KH, Park SW, Kim MJ, Yoon SH, Rhie DJ. The development of phasic and tonic inhibition in the rat visual cortex. Korean J Physiol Pharmacol. 2010;14:399-405. https://doi.org/10.4196/kjpp.2010.14.6.399
  25. Moreau AW, Amar M, Le Roux N, Morel N, Fossier P. Serotoninergic fine-tuning of the excitation-inhibition balance in rat visual cortical networks. Cereb Cortex. 2010;20:456-467. https://doi.org/10.1093/cercor/bhp114
  26. Hannon J, Hoyer D. Molecular biology of 5-HT receptors. Behav Brain Res. 2008;195:198-213. https://doi.org/10.1016/j.bbr.2008.03.020
  27. Morales M, Bloom FE. The 5-HT3 receptor is present in different subpopulations of GABAergic neurons in the rat telencephalon. J Neurosci. 1997;17:3157-3167.
  28. Feng J, Cai X, Zhao J, Yan Z. Serotonin receptors modulate GABAA receptor channels through activation of anchored protein kinase C in prefrontal cortical neurons. J Neurosci. 2001;21:6502-6511.
  29. Kirkwood A, Lee HK, Bear MF. Co-regulation of long-term potentiation and experience-dependent synaptic plasticity in visual cortex by age and experience. Nature. 1995;375:328-331. https://doi.org/10.1038/375328a0
  30. Huang ZJ, Kirkwood A, Pizzorusso T, Porciatti V, Morales B, Bear MF, Maffei L, Tonegawa S. BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex. Cell. 1999;98:739-755. https://doi.org/10.1016/S0092-8674(00)81509-3
  31. Hensch TK, Fagiolini M, Mataga N, Stryker MP, Baekkeskov S, Kash SF. Local GABA circuit control of experience-dependent plasticity in developing visual cortex. Science. 1998;282:1504-1508. https://doi.org/10.1126/science.282.5393.1504
  32. Kirkwood A, Bear MF. Hebbian synapses in visual cortex. J Neurosci. 1994;14:1634-1645.
  33. Kirkwood A, Rozas C, Kirkwood J, Perez F, Bear MF. Modulation of long-term synaptic depression in visual cortex by acetylcholine and norepinephrine. J Neurosci. 1999;19:1599-1609.
  34. Bear MF, Singer W. Modulation of visual cortical plasticity by acetylcholine and noradrenaline. Nature. 1986;320:172-176. https://doi.org/10.1038/320172a0
  35. Kojic L, Gu Q, Douglas RM, Cynader MS. Serotonin facilitates synaptic plasticity in kitten visual cortex: an in vitro study. Brain Res Dev Brain Res. 1997;101:299-304. https://doi.org/10.1016/S0165-3806(97)00083-7
  36. Brocher S, Artola A, Singer W. Agonists of cholinergic and noradrenergic receptors facilitate synergistically the induction of long-term potentiation in slices of rat visual cortex. Brain Res. 1992;573:27-36. https://doi.org/10.1016/0006-8993(92)90110-U
  37. Markram H, Segal M. Long-lasting facilitation of excitatory postsynaptic potentials in the rat hippocampus by acetylcholine. J Physiol. 1990;427:381-393.
  38. Wang Y, Gu Q, Cynader MS. Blockade of serotonin-2C receptors by mesulergine reduces ocular dominance plasticity in kitten visual cortex. Exp Brain Res. 1997;114:321-328. https://doi.org/10.1007/PL00005640
  39. Gordon B, Mitchell B, Mohtadi K, Roth E, Tseng Y, Turk F. Lesions of nonvisual inputs affect plasticity, norepinephrine content, and acetylcholine content of visual cortex. J Neurophysiol. 1990;64:1851-1860.
  40. Jang HJ, Cho KH, Park SW, Kim MJ, Yoon SH, Rhie DJ. Layer-specific serotonergic facilitation of IPSC in layer 2/3 pyramidal neurons of the visual cortex. J Neurophysiol. 2012;107:407-416. https://doi.org/10.1152/jn.00535.2011
  41. Mattson MP, Maudsley S, Martin B. BDNF and 5-HT: a dynamic duo in age-related neuronal plasticity and neurodegenerative disorders. Trends Neurosci. 2004;27:589-594. https://doi.org/10.1016/j.tins.2004.08.001
  42. Nakamura T, Nakamura K, Lasser-Ross N, Barbara JG, Sandler VM, Ross WN. Inositol 1,4,5-trisphosphate (IP3)-mediated $Ca^{2+}$ release evoked by metabotropic agonists and backpropagating action potentials in hippocampal CA1 pyramidal neurons. J Neurosci. 2000;20:8365-8376.
  43. Jiang B, Huang ZJ, Morales B, Kirkwood A. Maturation of GABAergic transmission and the timing of plasticity in visual cortex. Brain Res Brain Res Rev. 2005;50:126-133. https://doi.org/10.1016/j.brainresrev.2005.05.007

Cited by

  1. Effect of Serotonin on Paired Associative Stimulation-Induced Plasticity in the Human Motor Cortex vol.38, pp.11, 2012, https://doi.org/10.1038/npp.2013.127
  2. Age-Dependent Switch of the Role of Serotonergic 5-HT 1A Receptors in Gating Long-Term Potentiation in Rat Visual Cortex In Vivo vol.2016, pp.None, 2012, https://doi.org/10.1155/2016/6404082
  3. Chronic Enhancement of Serotonin Facilitates Excitatory Transcranial Direct Current Stimulation-Induced Neuroplasticity vol.41, pp.5, 2012, https://doi.org/10.1038/npp.2015.270
  4. CaMello-XR enables visualization and optogenetic control of G q/11 signals and receptor trafficking in GPCR-specific domains vol.2, pp.None, 2012, https://doi.org/10.1038/s42003-019-0292-y
  5. Serotonin type 6 receptor antagonist attenuates the impairment of long-term potentiation and memory induced by Abeta vol.364, pp.None, 2012, https://doi.org/10.1016/j.bbr.2019.02.004
  6. Layer-specific serotonergic induction of long-term depression in the prefrontal cortex of rats vol.24, pp.6, 2012, https://doi.org/10.4196/kjpp.2020.24.6.517