Postnatal development and sensory experience synergistically underlie the excitatory/inhibitory features of hippocampal neural circuits: Glutamatergic and GABAergic neurotransmission

Neuroscience

Volumn 318, Issue , 2016, Pages 230-243

  Talaei, S A ^a   Azami, A ^a   Salami, M ^a  

^a KASHAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

Author keywords

Excitatory inhibitory neurotransmission; Hippocampus; Postnatal development; Rat; Synaptic plasticity; Visual experience

Indexed keywords

AMPA RECEPTOR; GLUTAMATE DECARBOXYLASE 65; GLUTAMATE DECARBOXYLASE 67; GLUTAMATE RECEPTOR 1; GLUTAMATE RECEPTOR 2; MESSENGER RNA; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2A; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; 4 AMINOBUTYRIC ACID RECEPTOR; ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; FIELD EXCITATORY POSTSYNAPTIC POTENTIAL; GABAERGIC TRANSMISSION; HIPPOCAMPAL CA1 REGION; LONG TERM POTENTIATION; MALE; NERVE CELL PLASTICITY; NEUROTRANSMISSION; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; ANIMAL; DRUG EFFECTS; HIPPOCAMPUS; METABOLISM; NEWBORN; PHYSIOLOGY; PYRAMIDAL NERVE CELL; SYNAPTIC TRANSMISSION; WISTAR RAT;

ALPHA-AMINO-3-HYDROXY-5-METHYL-4-ISOXAZOLEPROPIONIC ACID; ANIMALS; ANIMALS, NEWBORN; EXCITATORY POSTSYNAPTIC POTENTIALS; GABAERGIC NEURONS; HIPPOCAMPUS; MALE; NEURONAL PLASTICITY; PYRAMIDAL CELLS; RATS, WISTAR; RECEPTORS, AMPA; SYNAPTIC TRANSMISSION;

EID: 84956661991     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2016.01.024     Document Type: Article

References (55)

1. Abraham W.C., Williams J.M. LTP maintenance and its protein synthesis-dependence. Neurobiol Learn Mem 2008, 89:260-268.
2. Bachtiar V., Stagg C.J. The role of inhibition in human motor cortical plasticity. Neuroscience 2014, 278:93-104.
3. Berry R.L., Perkins A.T., Teyler T.J. Visual deprivation decreases long-term potentiation in rat visual cortical slices. Brain Res 1993, 628:99-104.
4. Beston B.R., Jones D.G., Murphy K.M. Experience-dependent changes in excitatory & inhibitory receptor subunit expression in visual cortex. Front Synaptic Neurosci 2010, 2:138.
5. Cao Z., Liu L., Lickey M., Gordon B. Development of NR1, NR2A and NR2B mRNA in NR1 immunoreactive cells of rat visual cortex. Brain Res 2000, 868:296-305.
6. Collingridge G.L., Volianskis A., Bannister N., France G., Hanna L., Mercier M., Tidball P., Fang G., Irvine M.W., Costa B.M., Monaghan D.T., Bortolotto Z.A., Molnar E., Lodge D., Jane D.E. The NMDA receptor as a target for cognitive enhancement. Neuropharmacology 2012, 64:13-26.
7. Corvetti L., Aztiria E., Domenici L. Reduction of GFAP induced by long dark rearing is not restricted to visual cortex. Brain Res 2006, 1067:146-153.
8. Desai N.S., Cudmore R.H., Nelson S.B., Turrigiano G.G. Critical periods for experience-dependent synaptic scaling in visual cortex. Nat Neurosci 2002, 5:783-789.
9. Erisir A., Harris J.L. 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, 23:5208-5218.
10. Fagiolini M., Hensch T.K. Inhibitory threshold for critical-period activation in primary visual cortex. Nature 2000, 404:183-186.
11. Funahashi R., Maruyama T., Yoshimura Y., Komatsu Y. Silent synapses persist into adulthood in layer 2/3 pyramidal neurons of visual cortex in dark-reared mice. J Neurophysiol 2013, 109:2064-2076.
12. Ge S., Yang C.H., Hsu K.S., Ming G.L., Song H. A critical period for enhanced synaptic plasticity in newly generated neurons of the adult brain. Neuron 2007, 54:559-566.
13. Goel A., Jiang B., Xu L.W., Song L., Kirkwood A., Lee H.K. Cross-modal regulation of synaptic AMPA receptors in primary sensory cortices by visual experience. Nat Neurosci 2006, 9:1001-1003.
14. Graham B., Willshaw D. Probabilistic synaptic transmission in the associative net. Neural Comput 1999, 11:117-137.
15. Gruart A., Munoz M.D., Delgado-Garcia J.M. Involvement of the CA3-CA1 synapse in the acquisition of associative learning in behaving mice. J Neurosci 2006, 26:1077-1087.
16. Hoffman K.L., McNaughton B.L. Coordinated reactivation of distributed memory traces in primate neocortex. Science 2002, 297:2070-2073.
17. Huang S., Gu Y., Quinlan E.M., Kirkwood A. A refractory period for rejuvenating GABAergic synaptic transmission and ocular dominance plasticity with dark exposure. J Neurosci 2010, 30:16636-16642.
18. Ireland D.R., Abraham W.C. Mechanisms of group I mGluR-dependent long-term depression of NMDA receptor-mediated transmission at schaffer collateral-CA1 synapses. J Neurophysiol 2009, 101:1375-1385.
19. Isaac J.T.R., Ashby M.C., McBain C.J. The role of the GluR2 subunit in AMPA receptor function and synaptic plasticity. Neuron 2007, 54:859-871.
20. Jin S.X., Feig L.A. 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:e11732.
21. Keck T., Scheuss V., Jacobsen R.I., Wierenga Corette J., Eysel Ulf T., Bonhoeffer T., Hübener M. Loss of sensory input causes rapid structural changes of inhibitory neurons in adult mouse visual cortex. Neuron 2011, 71:869-882.
22. Kerchner G.A., Nicoll R.A. Silent synapses and the emergence of a postsynaptic mechanism for LTP. Nat Rev Neurosci 2008, 9:813-825.
23. Kirkwood A., Lee H.K., Bear M.F. Co-regulation of long-term potentiation and experience-dependent synaptic plasticity in visual cortex by age and experience. Nature 1995, 375:328-331.
24. 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, 103:2876-2888.
25. Liao D., Malinow R. Deficiency in induction but not expression of LTP in hippocampal slices from young rats. Learn Mem 1996, 3:138-149.
26. Liu X.-B., Murray K.D., Jones E.G. Switching of NMDA receptor 2A and 2B subunits at thalamic and cortical synapses during early postnatal development. J Neurosci 2004, 24:8885-8895.
27. Miyamoto E. Molecular mechanism of neuronal plasticity: induction and maintenance of long-term potentiation in the hippocampus. J Pharmacol Sci 2006, 100:433-442.
28. Molnár E. Long-term potentiation in cultured hippocampal neurons. Semin Cell Dev Biol 2011, 22:506-513.
29. Montey K.L., Quinlan E.M. Recovery from chronic monocular deprivation following reactivation of thalamocortical plasticity by dark exposure. Nat Commun 2011, 2:317.
30. Morishita H., Hensch T.K. Critical period revisited: impact on vision. Curr Opin Neurobiol 2008, 18:101-107.
31. Moser E.I. Learning-related changes in hippocampal field potentials. Behav Brain Res 1995, 71:11-18.
32. Mower G.D., Chen L. Laminar distribution of NMDA receptor subunit (NR1, NR2A, NR2B) expression during the critical period in cat visual cortex. Brain Res Mol Brain Res 2003, 119:19-27.
33. Paoletti P., Bellone C., Zhou Q. NMDA receptor subunit diversity: impact on receptor properties, synaptic plasticity and disease. Nat Rev Neurosci 2013, 14:383-400.
34. Philpot B.D., Cho K.K.A., Bear M.F. Obligatory role of NR2A for metaplasticity in visual cortex. Neuron 2007, 53:495-502.
35. Pickard L., Noel J., Henley J.M., Collingridge G.L., Molnar E. Developmental changes in synaptic AMPA and NMDA receptor distribution and AMPA receptor subunit composition in living hippocampal neurons. J Neurosci 2000, 20:7922-7931.
36. Quinlan E.M., Olstein D.H., Bear M.F. Bidirectional, experiencedependent regulation of N-methyl-D-aspartate receptor subunit composition in the rat visual cortex during postnatal development. Proc Natl Acad Sci U S A 1999, 96:12876-12880.
37. Quinlan E.M., Philpot B.D., Huganir R.L., Bear M.F. Rapid, experience-dependent expression of synaptic NMDA receptors in visual cortex in vivo. Nat Neurosci 1999, 2:352-357.
38. Rozas C., Frank H., Heynen A.J., Morales B., Bear M.F., Kirkwood A. Developmental inhibitory gate controls the relay of activity to the superficial layers of the visual cortex. J Neurosci 2001, 21:6791-6801.
39. Salami M., Fathollahi Y., Esteky H., Motamedi F., Atapour N. Effects of ketamine on synaptic transmission and long-term potentiation in layer II/III of rat visual cortex in vitro. Eur J Pharmacol 2000, 390:287-293.
40. 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, 38:349-356.
41. Salami M., Aghanouri Z., Noureddini M., Rashidi A.A. Early dark rearing influences spatial performances in the radial arm maze. J Med Sci 2008, 8:699-706.
42. Salami M., Talaei S.A., Davari S., Hamidi G. Interaction of visual experience and melatonin in the spatial task learning. Biol Rhythm Res 2012, 43:385-396.
43. Salami M. Light deprivation-related changes of strategy selection in the radial arm maze. Physiol Res 2007, 56:123-128.
44. Sloviter R.S., Lomo T. Updating the lamellar hypothesis of hippocampal organization. Front Neural Circuits 2012, 6:102.
45. Smart T.G., Paoletti P. Synaptic neurotransmitter-gated receptors. Cold Spring Harb Perspect Biol 2012, 4. pii: a009662.
46. Talaei S.A., Salami M. Sensory experience differentially underlies developmental alterations of LTP in CA1 area and dentate gyrus. Brain Res 2013, 1537:1-8.
47. Talaei S.A., Sheibani V., Salami M. Light deprivation improves melatonin related suppression of hippocampal plasticity. Hippocampus 2010, 20:447-455.
48. Tongiorgi E., Ferrero F., Cattaneo A., Domenici L. Dark-rearing decreases NR2A N-methyl-d-aspartate receptor subunit in all visual cortical layers. Neuroscience 2003, 119:1013-1022.
49. Tsanov M., Manahan-Vaughan D. Synaptic plasticity from visual cortex to hippocampus: systems integration in spatial information processing. Neuroscientist 2008, 14:584-597.
50. Tyzio R., Minlebaev M., Rheims S., Ivanov A., Jorquera I., Holmes G.L., Zilberter Y., Ben-Ari Y., Khazipov R. Postnatal changes in somatic γ-aminobutyric acid signalling in the rat hippocampus. Eur J Neurosci 2008, 27:2515-2528.
51. Voss P. Sensitive and critical periods in visual sensory deprivation. Front Psychol 2013, 4:664.
52. Waters N.S., Klintsova A.Y., Foster T.C. Insensitivity of the hippocampus to environmental stimulation during postnatal development. J Neurosci 1997, 17:7967-7973.
53. Yang L., Pan Z., Zhou L., Lin S., Wu K. Continuously changed genes during postnatal periods in rat visual cortex. Neurosci Lett 2009, 462:162-165.
54. Yashiro K., Philpot B.D. Regulation of NMDA receptor subunit expression and its implications for LTD, LTP, and metaplasticity. Neuropharmacology 2008, 55:1081-1094.
55. Yazaki-Sugiyama Y., Kang S., Cateau H., Fukai T., Hensch T.K. Bidirectional plasticity in fast-spiking GABA circuits by visual experience. Nature 2009, 462:218-221.