Developmental Effects of Melatonin on Synaptic Plasticity of Hippocampal CA1 Neurons in Visual Deprived Rats

Document Type: Original Article

Authors

1 Ph.D. Candidate of Neuroscience, Physiology Research Center, Kashan University of Medical Sciences, Kashan, Iran

2 Professor of Physiology, Physiology Research Center, Kashan University of Medical Sciences, Kashan, Iran

Abstract

Background & Aims: Change in visual experience impairs circadian rhythms. In this study, The effects of visual deprivation during critical period of brain development and melatonin intake on synaptic plasticity of hippocampal CA1 neurons were evaluated.
Methods: This experimental study was done on male rats kept in standard 12 hour light/dark condition (Light Reared-LR) or in complete darkness (Dark Reared-DR). Each group, was divided into 3 sub groups of 2, 4 and 6 week old rats (n=16). Excitatory post synaptic field potentials were recorded from dendrite of CA1 area neurons. Then, half of animals in each group received melatonin via ICV and field potentials recording was repeated. Finally, using tetanic stimulation, Long-term potentiation (LTP) was induced.
Results: The amplitude of basic responses of the LR animals decreased with age incaease (P<0.01). Visual deprivation and also melatonin increased the amplitude of basic responses of the DR group (P<0.01), and inhibited LTP induction in CA1 circuits. In comparison to the LR group, melatonin injection had less destructive effect on the LTP induction in the DR group (P<0.001).
Conclusion: Visual deprivation during critical period of brain development increases basic responses of rat’s CA1 neurons and inhibits LTP induction in these neurons, time dependently. Also, the visual deprivation opposes the destructive effects of melatonin on LTP induction in CA1 neurons in a time-dependent manner.

Keywords


  1. Voss P. Sensitive and critical periods in visual sensory deprivation. Front Psychol 2013; 4: 664.
  2. Hensch TK. Critical period plasticity in local cortical circuits. Nat Rev Neurosci 2005; 6(11): 877-88.
  3. Morishita H, Hensch TK. Critical period revisited: impact on vision. Curr Opin Neurobiol 2008; 18(1): 101-7.
  4. Tropea D, Van Wart A, Sur M. Molecular mechanisms of experience-dependent plasticity in visual cortex. Philos Trans R Soc B Biol Sci 2009; 364(1515): 341-55.
  5. Beston BR, Jones DG, Murphy KM. Experience-Dependent Changes in Excitatory & Inhibitory Receptor Subunit Expression in Visual Cortex. Front Synaptic Neurosci 2010; 2: 138
  6. Salami M, Fathollahi Y, Semnanian S, Atapour N. Differential effect of dark rearing on long-term potentiation induced by layer IV and white matter stimulation in rat visual cortex. Neurosci Res 2000; 38(4): 349-56.
  7. Montey KL, Quinlan EM. Recovery from chronic monocular deprivation following reactivation of thalamocortical plasticity by dark exposure. Nat Commun 2011; 2: 317.
  8. Sloviter RS, Lomo T. Updating the lamellar hypothesis of hippocampal organization. Front Neural Circuits 2012; 6: 102.
  9. Wang SH, Morris RG. Hippocampal-neocortical interactions in memory formation, consolidation, and reconsolidation. Annu Rev Psychol 2010; 61: 49-79.
  10. Tsanov M, Manahan-Vaughan D. Synaptic plasticity from visual cortex to hippocampus: systems integration in spatial information processing. Neuroscientist 2008; 14(6): 584-97.
  11. Ge S, Yang CH, Hsu KS, Ming GL, Song H. A critical period for enhanced synaptic plasticity in newly generated neurons of the adult brain. Neuron 2007; 54(4): 559-66.
  12. Talaei SA, Salami M. Sensory experience differentially underlies developmental alterations of LTP in CA1 area and dentate gyrus. Brain Res 2013; 1537: 1-8.
  13. Novkovic T, Mittmann T, Manahan-Vaughan D. BDNF contributes to the facilitation of hippocampal synaptic plasticity and learning enabled by environmental enrichment. Hippocampus 2015; 25(1): 1-15.
  14. Hardeland Rd, Cardinali DP, Srinivasan V, Spence DW, Brown GM, Pandi-Perumal SR. Melatonin-a pleiotropic, orchestrating regulator molecule. Prog Neurobiol 2011; 93(3): 350-84.
  15. Pandi-Perumal SR, Srinivasan V, Maestroni GJ, Cardinali DP, Poeggeler B, Hardeland R. Melatonin: Nature's most versatile biological signal? FEBS J 2006; 273(13): 2813-38.
  16. Stewart LS, Leung LS. Hippocampal melatonin receptors modulate seizure threshold. Epilepsia 2005; 46(4): 473-80.
  17. Wan Q, Man HY, Liu F, Braunton J, Niznik HB, Pang SF, et al. Differential modulation of GABAA receptor function by Mel1a and Mel1b receptors. Nat Neurosci 1999; 2(5): 401-3.
  18. Ozcan M, Yilmaz B, Carpenter DO. Effects of melatonin on synaptic transmission and long-term potentiation in two areas of mouse hippocampus. Brain Res 2006; 1111(1): 90-4.
  19. Yang L, Pan Z, Zhou L, Lin S, Wu K. Continuously changed genes during postnatal periods in rat visual cortex. Neurosci Lett 2009; 462(2): 162-5.
  20. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates. Academic Press,
  21. Talaei SA, Sheibani V, Salami M. Light deprivation improves melatonin related suppression of hippocampal plasticity. Hippocampus 2010; 20(3): 447-55.
  22. Kerchner GA, Nicoll RA. Silent synapses and the emergence of a postsynaptic mechanism for LTP. Nat Rev Neurosci 2008; 9(11): 813-25.
  23. Goel A, Jiang B, Xu LW, Song L, Kirkwood A, Lee HK. Cross-modal regulation of synaptic AMPA receptors in primary sensory cortices by visual experience. Nat Neurosci 2006; 9(8): 1001-3.
  24. Yashiro K, Philpot BD. Regulation of NMDA receptor subunit expression and its implications for LTD, LTP, and metaplasticity. Neuropharmacology 2008; 55(7): 1081-94.
  25. Liu X-B, Murray KD, Jones EG. Switching of NMDA Receptor 2A and 2B Subunits at Thalamic and Cortical Synapses during Early Postnatal Development. J Neurosci 2004; 24(40): 8885-95.
  26. Koyanagi Y, Yamamoto K, Oi Y, Koshikawa N, Kobayashi M. Presynaptic Interneuron Subtype- and Age-Dependent Modulation of GABAergic Synaptic Transmission by α-Adrenoceptors in Rat Insular Cortex. J Neurophysiol 2010; 103(5): 2876-88.
  27. Tyzio R, Minlebaev M, Rheims S, Ivanov A, Jorquera I, Holmes GL, et al. Postnatal changes in somatic γ-aminobutyric acid signalling in the rat hippocampus. Eur J Neurosci 2008; 27(10): 2515-28.
  28. Quinlan EM, Philpot BD, Huganir RL, Bear MF. Rapid, experience-dependent expression of synaptic NMDA receptors in visual cortex in vivo. Nat Neurosci 1999; 2(4): 352-7.
  29. Morales B, Choi SY, Kirkwood A. Dark rearing alters the development of GABAergic transmission in visual cortex. J Neurosci 2002; 22(18): 8084-90.
  30. Berry RL, Perkins AT, Teyler TJ. Visual deprivation decreases long-term potentiation in rat visual cortical slices. Brain Res 1993; 628(1-2): 99-104.
  31. Ireland DR, Abraham WC. Mechanisms of group I mGluR-Dependent long-term depression of NMDA receptor-mediated transmission at schaffer collateral-CA1 synapses. J Neurophysiol 2009; 101: 1375-85.
  32. Molnár E. Long-term potentiation in cultured hippocampal neurons. Semin Cell Deve Biol 2011; 22(5): 506-13.
  33. Jin SX, Feig LA. Long-term potentiation in the CA1 hippocampus induced by NR2A Subunit-Containing NMDA glutamate receptors Is mediated by Ras-GRF2/Erk map kinase signaling. PLoS ONE 2010; 5(7): e11732.
  34. Erisir A, Harris JL. Decline of the critical period of visual plasticity is concurrent with the reduction of NR2B subunit of the synaptic NMDA receptor in layer 4. J Neurosci 2003; 23(12): 5208-18.
  35. Musshoff U, Riewenherm D, Berger E, Fauteck JD, Speckmann EJ. Melatonin receptors in rat hippocampus: molecular and functional investigations. Hippocampus 2002; 12(2): 165-73.
  36. Zitouni M, Pevet P, Masson-Pevet M. Brain and pituitary melatonin receptors in male rat during post-natal and pubertal development and the effect of pinealectomy and testosterone manipulation. J Neuroendocrinol 1996; 8(8): 571-7.
  37. Chaudhury D, Wang LM, Colwell CS. Circadian regulation of hippocampal long-term potentiation. J Biol Rhythms 2005; 20(3): 225-36.
  38. Marquez de Prado B, Castaneda TR, Galindo A, del Arco A, Segovia G, Reiter RJ, et al. Melatonin disrupts circadian rhythms of glutamate and GABA in the neostriatum of the aware rat: a microdialysis study. J Pineal Res 2000; 29(4): 209-16.
  39. Khaldy H, Leon J, Escames G, Bikjdaouene L, Garcia JJ, Acuna-Castroviejo D. Circadian rhythms of dopamine and dihydroxyphenyl acetic acid in the mouse striatum: effects of pinealectomy and of melatonin treatment. Neuroendocrinology 2002; 75(3): 201-8.
  40. Iuvone PM, Boatright JH, Tosini G, Ye K. N-acetylserotonin: circadian activation of the BDNF receptor and neuroprotection in the retina and brain. Adv Exp Med Biol 2014; 801: 765-71.
  41. Miller E, Morel A, Saso L, Saluk J. Melatonin Redox Activity. Its Potential Clinical Application in Neurodegenerative Disorders. Curr Top Med Chem 2015; 15(2): 163-9.
  42. Dominguez-Alonso A, Valdes-Tovar M, Solis-Chagoyan H, Benitez-King G. Melatonin stimulates dendrite formation and complexity in the hilar zone of the rat hippocampus: participation of the ca++/calmodulin complex. Int J Mol Sci 2015; 16(1): 1907-27.
  43. Ramirez-Rodriguez G, Gomez-Sanchez A, Ortiz-Lopez L. Melatonin maintains calcium-binding calretinin-positive neurons in the dentate gyrus during aging of Balb/C mice. Exp Gerontol 2014; 60: 147-52.
  44. Corrales A, Vidal R, Garcia S, Vidal V, Martinez P, Garcia E, et al. Chronic melatonin treatment rescues electrophysiological and neuromorphological deficits in a mouse model of Down syndrome. J Pineal Res 2014; 56(1): 51-61.
Escames G, Leon J, Lopez LC, Acuna-Castroviejo D. Mechanisms of N-methyl-D-aspartate receptor inhibition by melatonin in the rat striatum. J Neuroendocrinol 2004; 16(11): 929-35