Pathway-Specific Differences in Subunit Composition of Synaptic NMDA Receptors on Pyramidal Neurons in Neocortex

Journal of Neuroscience

Volumn 23, Issue 31, 2003, Pages 10074-10083

  Kumar, Sanjay S ^a   Huguenard, John R ^a  

^a STANFORD UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Neocortex; NMDA receptors; Pathway specificity; Pyramidal neurons; Subunit composition; Synaptic integration

Indexed keywords

1 (PHENANTHREN 2 YLCARBONYL)PIPERAZINE 2,3 DICARBOXYLIC ACID; 2 AMINO 5 PHOSPHONOVALERIC ACID; 6 NITRO 7 SULFAMOYLBENZO[F]QUINOXALINE 2,3 DIONE; AMPA RECEPTOR; CHELATING AGENT; IFENPRODIL; MAGNESIUM ION; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; N,N,N',N' TETRAKIS(2 PYRIDYLMETHYL)ETHYLENEDIAMINE; PICROTOXIN; RECEPTOR SUBUNIT; UNCLASSIFIED DRUG; ZINC ION;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; BRAIN ELECTROPHYSIOLOGY; BRAIN SLICE; CONTROLLED STUDY; DRUG RECEPTOR BINDING; INFORMATION PROCESSING; NEOCORTEX; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SYNAPSE; VOLTAGE CLAMP;

EID: 0242694945     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.23-31-10074.2003     Document Type: Article

References (62)

1. Andrasfalvy BK, Magee JC (2001) Distance-dependent increase in AMPA receptor number in the dendrites of adult hippocampal CA1 pyramidal neurons. J Neurosci 21:9151-9159.
2. Barria A, Malinow R (2002) Subunit-specific NMDA receptor trafficking to synapses. Neuron 35:345-353.
3. Barth AL, Malenka RC (2001) NMDAR EPSC kinetics do not regulate the critical period for LTP at thalamocortical synapses. Nat Neurosci 4:235-236.
4. Billups D, Liu YB, Birnstiel S, Slater NT (2002) NMDA receptor-mediated currents in rat cerebellar granule and unipolar brush cells. J Neurophysiol 87:1948-1959.
5. Braitenberg V, Schüz A (1991) Anatomy of the cortex: statistics and geometry. Berlin: Springer-Verlag.
6. Burkhalter A, Charles V (1990) Organization of local axon collaterals of efferent projection neurons in rat visual cortex. J Comp Neurol 302:920-934.
7. 2+ block of NMDA-receptor channels as a mechanism of modulation. Nature 356:521-523.
8. Clark BA, Cull-Candy SG (2002) Activity-dependent recruitment of extrasynaptic NMDA receptor activation at an AMPA receptor-only synapse. J Neurosci 22:4428-4436.
9. Clayton DA, Mesches MH, Alvarez E, Bickford PC, Browning MD (2002) A hippocampal NR2B deficit can mimic age-related changes in long-term potentiation and spatial learning in the Fischer 344 rat. J Neurosci 22:3628-3637.
10. Connors BW, Amitai Y (1995) Functions of local circuits in neocortex: synchrony and laminae. In: The cortical neuron (Gutnick MJ, Mody I, eds), pp 123-155. New York: Oxford UP.
11. Conti F, Manzoni T (1994) The neurotransmitters and postsynaptic actions of callosally projecting neurons. Behav Brain Res 64:37-53.
12. Cull-Candy SG, Brickley SG, Misra C, Feldmeyer D, Momiyama A, Farrant M (1998) NMDA receptor diversity in the cerebellum: identification of sub-units contributing to functional receptors. Neuropharmacology 37:1369-1380.
13. Cull-Candy S, Brickley S, Farrant M (2001) NMDA receptor subunits: diversity, development and disease. Curr Opin Neurobiol 11:327-335.
14. Das S, Sasaki YF, Rothe T, Premkumar LS, Takasu M, Crandall JE, Dikkes P, Conner DA, Rayudu PV, Cheung W, Chen HS, Lipton SA, Nakanishi N (1998) Increased NMDA current and spine density, in mice lacking the NMDA receptor subunit NR3A. Nature 393:377-381.
15. Dobrunz LE, Stevens CF (1997) Heterogeneity of release probability, facilitation and depletion. Neuron 18:995-1008.
16. Fleidervish IA, Binshtok AM, Gutnick MJ (1998) Functionally distinct NMDA receptors mediate horizontal connectivity within layer 4 of mouse barrel cortex. Neuron 21:1055-1065.
17. Flint AC, Maisch US, Weishaupt JH, Kriegstein AR, Monyer H (1997) NR2A subunit expression shortens NMDA receptor synaptic currents in developing neocortex. J Neurosci 17:2469-2476.
18. Geiger JR, Lubke J, Roth A, Frotscher M, Jonas P (1997) Submillisecond AMPA receptor-mediated signaling at a principal neuron-interneuron synapse. Neuron 18:1009-1023.
19. Gil Z, Connors BW, Amitai Y (1999) Efficacy of thalamocortical and intracortical synaptic connections: quanta, innervation, and reliability. Neuron 23:385-397.
20. Guo H, Huang LY (2001) Alteration in the voltage dependence of NMDA receptor channels in rat dorsal horn neurones following peripheral inflammation. J Physiol (Lond) 537:115-123.
21. Hass K (2001) Directing AMPA receptor traffic. Trends Neurosci 24:137.
22. Hausser M, Major G, Stuart GJ (2001) Differential shunting of EPSPs by action potentials. Science 291:138-141.
23. Hestrin S (1992) Developmental regulation of NMDA receptor-mediated synaptic currents at a central synapse. Nature 357:686-689.
24. Hestrin S, Sah P, Nicoll RA (1990) Mechanisms generating the time course of dual component excitatory synaptic currents recorded in hippocampal slices. Neuron 5:247-253.
25. Hrabetova S, Serrano P, Blace N, Tse HW, Skifter DA, Jane DE, Monaghan DT, Sacktor TC (2000) Distinct NMDA receptor subpopulations contribute to long-term potentiation and long-term depression induction. J Neurosci 20:RC81(1-6).
26. Ito I, Futai K, Katagiri H, Watanabe M, Sakimura K, Mishina M, Sugiyama H (1997) Synapse-selective impairment of NMDA receptor functions in mice lacking NMDA receptor epsilon 1 or epsilon 2 subunit. J Physiol (Lond) 500:401-408.
27. Johnson RR, Jiang X, Burkhalter A (1996) Regional and laminar differences in synaptic localization of NMDA receptor subunit NR1 splice variants in rat visual cortex and hippocampus. J Comp Neurol 368:335-355.
28. Joshi I, Wang LY (2002) Developmental profiles of glutamate receptors and synaptic transmission at a single synapse in the mouse auditory brainstem. J Physiol (Lond) 540:861-873.
29. König P, Engel AK, Singer W (1996) Integrator of coincidence Integrator or coincidence detector? The role of cortical neuron revisited. Trends Neurosci 19:130-137.
30. Kumar SS, Huguenard JR (2001) Properties of excitatory synaptic connections mediated by the corpus callosum in the developing rat neocortex. J Neurophysiol 86:2973-2985.
31. Kumar SS, Bacci A, Kharazia V, Huguenard JR (2002) A developmental switch of AMPA receptor subunits in neocortical pyramidal neurons. J Neurosci 22:3005-3015.
32. Lei S, McBain CJ (2002) Distinct NMDA receptors provide differential modes of transmission at mossy fiber-interneuron synapses. Neuron 33:921-933.
33. Lu HC, Gonzalez E, Crair MC (2001) Barrel cortex critical period plasticity is independent of changes in NMDA receptor subunit composition. Neuron 32:619-634.
34. Luscher C, Xia H, Beattie EC, Carroll RC, von Zastrow M, Malenka RC, Nicoll RA (1999) Role of AMPA receptor cycling in synaptic transmission and plasticity. Neuron 24:649-658.
35. Maccaferri G, Dingledine R (2002) Control of feedforward dendriti inhibition by NMDA receptor dependent spike timing in hippocampal interneurons. J Neurosci 22:5462-5472.
36. Mayer ML, Westbrook GL (1987) Permeation and block of N-methyl-D-aspartic acid receptor channels by divalent cations in mouse cultured central neurones. J Physiol (Lond) 394:501-527.
37. 2+ of NMDA responses in spinal cord neurones. Nature 309:261-263.
38. Mayer ML, Vyklicky Jr L, Westbrook GL (1989) Modulation of excitatory amino acid receptors by group IIB metal cations in cultured mouse hippocampal neurones. J Physiol (Lond) 415:329-350.
39. Misra C, Brickley SG, Farrant M, Cull-Candy SG (2000) Identification of subunits contributing to synaptic and extrasynaptic NMDA receptors in Golgi cells of the rat cerebellum. J Physiol (Lond) 524:147-162.
40. Momiyama A (2000) Distinct synaptic and extrasynaptic NMDA receptors identified in dorsal horn neurones of the adult rat spinal cord. J Physiol (Lond) 523:621-628.
41. Monyer H, Burnashev N, Laurie DI, Sakmann B, Seeburg PH (1994) Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 12:529-540.
42. Nowak L, Bregestovski P, Ascher P, Herbet A, Prochiantz A (1984) Magnesium gates glutamate-activated channels in mouse central neurones. Nature 307:462-465.
43. Otmakhova NA, Otmakhov N, Lisman JE (2002) Pathway-specific properties of AMPA and NMDA-mediated transmission in CA1 hippocampal pyramidal cells. J Neurosci 22:1199-1207.
44. Pandya DN, Seltzer B (1986) The topography of commissural fibers. In: Two hemispheres-one brain: functions of the corpus callosum (Lepore F, Ptito M, Jasper HH, eds), pp 47-73. New York; Liss.
45. Paoletti P, Ascher P, Neyton J (1997) High-affinity zinc inhibition of NMDA NR1-NR2A receptors. J Neurosci 17:5711-5725.
46. Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates, Ed 2. San Diego: Academic.
47. Perez-Otano I, Schulteis CT, Contractor A, Lipton SA, Trimmer JS, Sucher NJ, Heinemann SF (2001) Assembly with the NR1 subunit is required for surface expression of NR3A-containing NMDA receptors. J Neurosci 21:1228-1237.
48. Philpot BD, Weisberg MP, Ramos MS, Sawtell NB, Tang YP, Tsien JZ, Bear MF (2001) Effect of transgenic overexpression of NR2B on NMDA receptor function and synaptic plasticity in visual cortex. Neuropharmacology 41:762-770.
49. Pitzer KS, Mayorga G (1973) Thermodynamics of electrolytes. II. Activity and osmotic coefficients for strong electrolytes with one or both ions univalent. J Phys Chem 77:2300-2308.
50. Shadlen MN, Newsome WT (1994) Noise, neural codes and cortical organization. Curr Opin Neurobiol 4:569-579.
51. Sheng M (2001) Molecular organization of the postsynaptic specialization. Proc Natl Acad Sci USA 98:7058-7061.
52. Stern EA, Maravall M, Svoboda K (2001) Rapid development and plasticity of layer 2/3 maps in rat barrel cortex in vivo. Neuron 31:305-315.
53. Szinyei C, Stork O, Pape HC (2003) Contribution of NR2B subunits to synaptic transmission in amygdaloid interneurons. J Neurosci 23:2549-2556.
54. Tang YP, Shimizu E, Dube GR, Rampon C, Kerchner GA, Zhuo M, Liu G, Tsien JZ (1999) Genetic enhancement of learning and memory in mice. Nature 401:63-69.
55. Toth K, McBain CJ (1998) Afferent-specific innervation of two distinct AMPA receptor subtypes on single hippocampal interneurons. Nat Neurosci 1:572-578.
56. Toth K, McBain CJ (2000) Target-specific expression of pre- and postsynaptic mechanisms. J Physiol (Lond) 525:41-51.
57. Tovar KR, Westbrook GL (1999) The incorporation of NMDA receptors with a distinct subunit composition at nascent hippocampal synapses in vitro. J Neurosci 19:4180-4188.
58. Tovar KR, Sprouffske K, Westbrook GL (2000) Fast NMDA receptor-mediated synaptic currents in neurons from mice lacking the ε2 (NR2B) subunit. J Neurophysiol 83:616-620.
59. Vicini S, Wang JF, Li JH, Zhu WJ, Wang YH, Luo JH, Wolfe BB, Grayson DR (1998) Functional and pharmacological differences between recombinant N-methyl-D-aspartate receptors. J Neurophysiol 79:555-566.
60. Walker HC, Lawrence JJ, McBain CJ (2002) Activation of kinetically distinct synaptic conductances on inhibitory interneurons by electrotonically overlapping afferents. Neuron 35:161-171.
61. Williams K (1993) Ifenprodil discriminates subtypes of the N-methyl-D-aspartate receptor: selectivity and mechanisms at recombinant heteromeric receptors. Mol Pharmacol 44:851-859.
62. Zhu Y, Auerbach A (2001) K(+) occupancy of the N-methyl-D-aspartate receptor channel probed by Mg(2+) block. J Gen Physiol 117: 287-298.