Maturation of intrinsic and synaptic properties of layer 2/3 pyramidal neurons in mouse auditory cortex

Journal of Neurophysiology

Volumn 99, Issue 6, 2008, Pages 2998-3008

  Oswald, Anne Marie M ^a   Reyes, Alex D ^a  

^a NEW YORK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; AUDITORY CORTEX; CELL MATURATION; EXCITATORY POSTSYNAPTIC POTENTIAL; MALE; MOUSE; NERVE CELL MEMBRANE STEADY POTENTIAL; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; THALAMOCORTICAL TRACT;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; AUDITORY CORTEX; AUDITORY PATHWAYS; DOSE-RESPONSE RELATIONSHIP, RADIATION; ELECTRIC STIMULATION; EXCITATORY POSTSYNAPTIC POTENTIALS; LYSINE; MICE; NEURONAL PLASTICITY; PATCH-CLAMP TECHNIQUES; PYRAMIDAL CELLS; SYNAPSES;

EID: 57049181979     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.01160.2007     Document Type: Article

References (73)

1. 2+ channels mediate transmitter release at excitatory synapses displaying different dynamic properties in rat neocortex. Cereb Cortex 16: 386-393, 2006.
2. Aramakis V, Hsieh CY, Leslie FM, Metherate R. A critical period for nicotine-induced disruption of synaptic development in rat auditory cortex. J Neurosci 20: 6106-6116, 2000.
3. Atzori M, Lei S, Evans DI, Kanold PO, Phillips-Tansey E, McIntyre O, McBain CJ. Differential synaptic processing separates stationary from transient inputs to the auditory cortex. Nat Neurosci 4: 1230-1237, 2001.
4. Bao S, Chang EF, Woods J, Merzenich MM. Temporal plasticity in the primary auditory cortex induced by operant perceptual learning. Nat Neurosci 7: 974-981, 2004.
5. Barbour DL, Wang X. Auditory cortical responses elicited in awake primates by random spectral stimuli. J Neurosci 23: 7194-7206, 2003.
6. Chang E, Merzenich MM. Environmental noise retards auditory cortical development. Science 300: 498-502, 2003.
7. Chang EF, Bao S, Imaizumi K, Schreiner C, Merzenich MM. Development of spectral and temporal response selectivity in the auditory cortex. Proc Natl Acad Sci USA 102: 16460-16465, 2005.
8. Chen H, Roper SN. Tonic activity of metabotropic glutamate receptors is involved in developmental modification of short-term plasticity in the neocortex. J Neurophysiol 92: 838-844, 2004.
9. Choi S, Lovinger DM. Decreased probability of neurotransmitter release underlies striatal long-term depression and postnatal development of corticostriatal synapses. Proc Natl Acad Sci USA 94: 2665-2670, 1997.
10. Code R, Winer JA. Commissural neurons in layer III of cat primary auditory cortex (AI): pyramidal and non-pyramidal cell input. J Comp Neurol 242: 485-510, 1985.
11. Cruikshank SJ, Rose HJ, Metherate R. Auditory thalamocortical synaptic transmission in vitro. J Neurophysiol 87: 361-384, 2002.
12. Cull-Candy S, Brickley S, Farrant M. NMDA receptor subunits: diversity, development and disease. Curr Opin Neurobiol 11: 327-335, 2001.
13. de Villers-Sidani E, Chang EF, Bao S, Merzenich MM. Critical period window for spectral tuning defined in the primary auditory cortex (A1) in the rat. J Neurosci 27: 180-190, 2007.
14. Douglas R, Koch C, Mahowald M, Martin KA, Suarez HH. Recurrent excitation in neocortical circuits. Science 269: 981-985, 1995.
15. Douglas R, Martin KA. Recurrent neuronal circuits in the neocortex. Curr Biol 17: R496-R500, 2007.
16. Du J, Zhang L, Weiser M, Rudy B, McBain CJ. Developmental expression and functional characterization of the potassium-channel subunit Kv3.1b in parvalbumin-containing interneurons of the rat hippocampus. J Neurosci 16: 506-518, 1996.
17. Ehret G. Development of absolute auditory thresholds in the house mouse (Mus musculus). J Am Audiol Soc 1: 179-184, 1976.
18. Ehret G, Romand R. Development of tone response thresholds, latencies and tuning in the mouse inferior colliculus. Brain Res Dev Brain Res 67: 317-326, 1992.
19. Ene F, Kullmann PH, Gillespie DC, Kandler K. Glutamatergic calcium responses in the developing lateral superior olive: receptor types and their specific activation by synaptic activity patterns. J Neurophysiol 90: 2581-2591, 2003.
20. Feldmeyer D, Lubke J, Sakmann B. Efficacy and connectivity of intracolumnar pairs of layer 2/3 pyramidal cells in the barrel cortex of juvenile rats. J Physiol 575: 583-602, 2006.
21. Frick A, Feldmeyer D, Sakmann B. Postnatal development of synaptic transmission in local networks of L5A pyramidal neurons in rat somatosensory cortex. J Physiol 585: 103-116, 2007.
22. Hardingham N, Larkman AU. Rapid report: the reliability of excitatory synaptic transmission in slices of rat visual cortex in vitro is temperature dependent. J Physiol 507: 249-256, 1998.
23. Holmgren C, Harkany T, Svennenfors B, Zilberter Y. Pyramidal cell communication within local networks in layer 2/3 of rat neocortex. J Physiol 551: 139-152, 2003.
24. Hsieh C, Chen Y, Leslie FM, Metherate R. Postnatal development of NR2A and NR2B mRNA expression in rat auditory cortex and thalamus. J Assoc Res Otolaryngol 3: 479-487, 2002.
25. Joshi I, Wang LY. Developmental profiles of glutamate receptors and synaptic transmission at a single synapse in the mouse auditory brainstem. J Physiol 540: 861-873, 2002.
26. Kampa B, Letzkus JJ, Stuart GJ. Cortical feed-forward networks for binding different streams of sensory information. Nat Neurosci 9: 1472-1473, 2006.
27. Kang J, Huguenard JR, Prince DA. Development of BK channels in neocortical pyramidal neurons. J Neurophysiol 76: 188-198, 1996.
28. + channels, TASK-1 and TREK-1, in the rat cochlea. Neuroreport 15: 437-441, 2004.
29. Kasper E, Larkman AU, Lubke J, Blakemore C. Pyramidal neurons in layer 5 of the rat visual cortex. II. Development of electrophysiological properties. J Comp Neurol 339: 475-494, 1994.
30. Kaur S, Lazar R, Metherate R. Intracortical pathways determine breadth of subthreshold frequency receptive fields in primary auditory cortex. J Neurophysiol 91: 2551-2567, 2004.
31. Kotak V, Breithaupt AD, Sanes DH. Developmental hearing loss eliminates long-term potentiation in the auditory cortex. Proc Natl Acad Sci USA 104: 3550-3555, 2007.
32. Kotak V, Fujisawa S, Lee FA, Karthikeyan O, Aoki C, Sanes DH. Hearing loss raises excitability in the auditory cortex. J Neurosci 25: 3908-3918, 2005.
33. Kotak VC, Sadahiro M, Fall CP. Developmental expression of endogenous oscillations and waves in the auditory cortex involves calcium, gap junctions, and GABA. Neuroscience 146: 1629-1639, 2007.
34. Linden JF, Schreiner CE. Columnar transformations in auditory cortex? A comparison to visual and somatosensory cortices. Cereb Cortex 13: 83-89, 2003.
35. Liu B, Wu GK, Arbuckle RA, Tao HW, Zhang LI. Defining cortical frequency tuning with recurrent excitatory circuitry. Nat Neurosci 10: 1594-1600, 2007.
36. Maravall M, Stern EA, Svoboda K. Development of intrinsic properties and excitability of layer 2/3 pyramidal neurons during a critical period for sensory maps in rat barrel cortex. J Neurophysiol 92: 144-156, 2004.
37. Mason A, Nicoll A, Stratford K. Synaptic transmission between individual pyramidal neurons of the rat visual cortex in vitro. J Neurosci 11: 72-84, 1991.
38. McCormick D, Prince DA. Post-natal development of electrophysiological properties of rat cerebral cortical pyramidal neurones. J Physiol 393: 743-762, 1987.
39. Metherate R, Aramakis VB. Intrinsic electrophysiology of neurons in thalamorecipient layers of developing rat auditory cortex. Brain Res Dev Brain Res 115: 131-144, 1999.
40. Muller D, Oliver M, Lynch G. Developmental changes in synaptic properties in hippocampus of neonatal rats. Brain Res Dev Brain Res 49: 105-114, 1989.
41. Nakamura Y, Takahashi T. Developmental changes in potassium currents at the rat calyx of Held presynaptic terminal. J Physiol 581: 1101-1112, 2007.
42. Ojima H, Honda CN, Jones EG. Patterns of axon collateralization of identified supragranular pyramidal neurons in the cat auditory cortex. Cereb Cortex 1: 80-94, 1991.
43. Ojima H, Murakami K. Intracellular characterization of suppressive responses in supragranular pyramidal neurons of cat primary auditory cortex in vivo. Cereb Cortex 12: 1079-1091, 2002.
44. Oswald A, Schiff ML, Reyes AD. Synaptic mechanisms underlying auditory processing. Curr Opin Neurobiol 16: 371-376, 2006.
45. Ou X, Buckwalter G, McNeill TH, Walsh JP. Age-related change in short-term synaptic plasticity intrinsic to excitatory striatal synapses. Synapse 27: 57-68, 1997.
46. Pouzat C, Hestrin S. Developmental regulation of basket/stellate cell→Purkinje cell synapses in the cerebellum. J Neurosci 17: 9104-9112, 1997.
47. Ramoa A, Sur M. Short-term synaptic plasticity in the visual cortex during development. Cereb Cortex 6: 640-646, 1996.
48. Reyes A, Sakmann B. Developmental switch in the short-term modification of unitary EPSPs evoked in layer 2/3 and layer 5 pyramidal neurons of rat neocortex. J Neurosci 19: 3827-3835, 1999.
49. Romand R, Ehret G. Development of tonotopy in the inferior colliculus. I. Electrophysiological mapping in house mice. Brain Res Dev Brain Res 54: 221-234, 1990.
50. 2+ buffers in facilitating and depressing nerve terminals of pyramidal cells in layer 2/3 of the rat neocortex indicates a target cell-specific difference in presynaptic calcium dynamics. J Physiol 531: 807-826, 2001.
51. Saeb S, Gharibzadeh S, Towhidkhah F, Farajidavar A. Modeling the primary auditory cortex using dynamic synapses: can synaptic plasticity explain the temporal tuning? J Theor Biol 248: 1-9, 2007.
52. Sanes D, Constantine-Paton M. The development of stimulus following in the cochlear nerve and inferior colliculus of the mouse. Brain Res 354: 255-267, 1985a.
53. Sanes D, Constantine-Paton M. The sharpening of frequency tuning curves requires patterned activity during development in the mouse, Mus musculus. J Neurosci 5: 1152-1166, 1985b.
54. Seidl A, Grothe B. Development of sound localization mechanisms in the Mongolian gerbil is shaped by early acoustic experience. J Neurophysiol 94: 1028-1036, 2005.
55. Song L, McGee J, Walsh EJ. Frequency- and level-dependent changes in auditory brainstem responses (ABRs) in developing mice. J Acoust Soc Am 119: 2242-2257, 2006.
56. Sprenkle P, McGee J, Bertoni JM, Walsh EJ. Development of auditory brainstem responses (ABRs) in Tshr mutant mice derived from euthyroid and hypothyroid dams. J Assoc Res Otolaryngol 2: 330-347, 2001.
57. Tansey E, Chow A, Rudy B, McBain CJ. Developmental expression of potassium-channel subunit Kv3.2 within subpopulations of mouse hippocampal inhibitory interneurons. Hippocampus 12: 137-148, 2002.
58. Tennigkeit F, Schwarz DW, Puil E. Postnatal development of signal generation in auditory thalamic neuron. Brain Res Dev Brain Res 109: 255-263, 1998.
59. Thomson A, West DC, Wang Y, Bannister AP. Synaptic connections and small circuits involving excitatory and inhibitory neurons in Layers 2-5 of adult rat and cat neocortex: triple intracellular recordings and biocytin labelling in vitro. Cereb Cortex 12: 936-953, 2002.
60. Volgushev M, Kudryashov I, Chistiakova M, Mukovski M, Niesmann J, Eysel UT. Probability of transmitter release at neocortical synapses at different temperatures. J Neurophysiol 92: 212-220, 2004.
61. Wang X, Lu T, Snider RK, Liang L. Sustained firing in auditory cortex evoked by preferred stimuli. Nature 435: 341-346, 2005.
62. Winer J. The pyramidal neurons in layer III of cat primary auditory cortex (AI). J Comp Neurol 229: 476-496, 1984.
63. Winer J. Structure of layer II in cat primary auditory cortex (AI). J Comp Neurol 238: 10-37, 1985.
64. Wu S, Oertel D. Maturation of synapses and electrical properties of cells in the cochlear nuclei. Hear Res 30: 99-110, 1987.
65. Xu H, Kotak VC, Sanes DH. Conductive hearing loss disrupts synaptic and spike adaptation in developing auditory cortex. J Neurosci 27: 9417-9426, 2007.
66. Yanagisawa T, Tsumoto T, Kimura F. Transiently higher release probability during critical period at thalamocortical synapses in the mouse barrel cortex: relevance to differential short-term plasticity of AMPA and NMDA EPSCs and possible involvement of silent synapses. Eur J Neurosci 20: 3006-3018, 2004.
67. Yoshimura Y, Callaway EM. Fine scale specificity of cortical networks depends on inhibitory cell type and connectivity. Nat Neurosci 8: 1552-1559, 2005a.
68. Yoshimura Y, Dantzker JL, Callaway EM. Excitatory cortical neurons form fine-scale functional networks. Nature 433: 868-873, 2005b.
69. Yu X, Sanes DH, Aristizabal O, Wadghiri YZ, Turnbull DH. Large-scale reorganization of the tonotopic map in mouse auditory midbrain revealed by MRI. Proc Natl Acad Sci USA 104: 12193-12198, 2007.
70. Zhang L, Bao S, Merzenich MM. Persistent and specific influences of early acoustic environments on primary auditory cortex. Nat Neurosci 4: 1123-1130, 2001.
71. Zhang Z. Maturation of layer V pyramidal neurons in the rat prefrontal cortex: intrinsic properties and synaptic function. J Neurophysiol 91: 1171-1182, 2004.
72. Zucker R. Short-term synaptic plasticity. Annu Rev Neurosci 12: 13-31, 1989.
73. Zucker RS, Regehr WG. Short term synaptic plasticity. Ann Rev Physiol 64: 355-405, 2002.