Inhibitory sharpening of receptive fields contributes to whisker map plasticity in rat somatosensory cortex

Journal of Neurophysiology

Volumn 94, Issue 6, 2005, Pages 4387-4400

  Foeller, Elisabeth ^a,b   Celikel, Tansa ^a,c   Feldman, Daniel E ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b GOETHE UNIVERSITY   (Germany)

^c MAX PLANCK INSTITUTE FOR MEDICAL RESEARCH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

3 AMINO 2 (3 CARBOXYPROPYL) 6 (4 METHOXYPHENYL)PYRIDAZINIUM BROMIDE; 4 AMINOBUTYRIC ACID A RECEPTOR BLOCKING AGENT;

AGE; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DATA ANALYSIS; ELECTRORETINOGRAM; FEMALE; GABAERGIC SYSTEM; HISTOLOGY; LATENT PERIOD; MALE; MICROIONTOPHORESIS; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; RAT; RECEPTIVE FIELD; RESPONSE TIME; SOMATOSENSORY CORTEX; SPIKE; VIBRISSA;

ACTION POTENTIALS; ANIMALS; BRAIN MAPPING; DOSE-RESPONSE RELATIONSHIP, RADIATION; ELECTRIC STIMULATION; EVOKED POTENTIALS, SOMATOSENSORY; FEMALE; GABA ANTAGONISTS; IONTOPHORESIS; LINEAR MODELS; MALE; NEURAL INHIBITION; NEURONAL PLASTICITY; PYRIDAZINES; RATS; RATS, LONG-EVANS; REACTION TIME; SENSORY DEPRIVATION; SOMATOSENSORY CORTEX; TIME FACTORS; VIBRISSAE;

EID: 28044439351     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.00553.2005     Document Type: Article

References (83)

1. Allen CB, Celikel T, and Feldman DE. Long-term depression induced by sensory deprivation during cortical map plasticity in vivo. Nat Neurosci 6: 291-299, 2003.
2. Anderson JS, Carandini M, and Ferster D. Orientation tuning of input conductance, excitation, and inhibition in cat primary visual cortex. J Neurophysiol 84: 909-926, 2000.
3. Armstrong-James M, Fox K, and Das-Gupta A. Flow of excitation within rat barrel cortex on striking a single vibrissa. J Neurophysiol 68: 1345-1358, 1992.
4. Armstrong-James M and Millar J. Carbon fiber microelectrodes. J Neurosci Methods 1: 279-287, 1979.
5. Brecht M, Roth A, and Sakmann B. Dynamic receptive fields of reconstructed pyramidal cells in layers 3 and 2 of rat somatosensory barrel cortex. J Physiol 553: 243-265, 2003.
6. Brecht M and Sakmann B. Dynamic representation of whisker deflection by synaptic potentials in spiny stellate and pyramidal cells in the barrels and septa of layer 4 rat somatosensory cortex. J Physiol 543: 49-70, 2002.
7. Brumberg JC, Pinto DJ, and Simons DJ. Spatial gradients and inhibitory summation in the rat whisker barrel system. J Neurophysiol 76: 130-140, 1996.
8. Bruno RM and Simons DJ. Feedforward mechanisms of excitatory and inhibitory cortical receptive fields. J Neurosci 22: 10966-10975, 2002.
9. Calford MB. Dynamic representational plasticity in sensory cortex. Neuroscience 111: 709-738, 2002.
10. Calford MB and Tweedale R. Immediate and chronic changes in responses of somatosensory cortex in adult flying-fox after digit amputation. Nature 332: 446-448, 1988.
11. Celikel T, Szostak VA, and Feldman DE. Modulation of spike timing by sensory deprivation during induction of cortical map plasticity. Nat Neurosci 7: 534-541, 2004.
12. Chevaleyre V and Castillo PE. Heterosynaptic LTD of hippocampal GABAergic synapses: a novel role of endocannabinoids in regulating excitability. Neuron 38: 461-472, 2003.
13. Chowdhury SA and Rasmusson DD. Effect of GABAB receptor blockade on receptive fields of raccoon somatosensory cortical neurons during reorganization. Exp Brain Res 145: 150-157, 2002.
14. Darian-Smith C and Gilbert CD. Axonal sprouting accompanies functional reorganization in adult cat striate cortex. Nature 368: 737-740, 1994.
15. Darian-Smith C and Gilbert CD. Topographic reorganization in the striate cortex of the adult cat and monkey is cortically mediated. J Neurosci 15: 1631-1647, 1995.
16. Derdikman D, Hildesheim R, Ahissar E, Arieli A, and Grinvald A. Imaging spatiotemporal dynamics of surround inhibition in the barrels somatosensory cortex. J Neurosci 23: 3100-3105, 2003.
17. Douglas RJ and Martin KA. Neuronal circuits of the neocortex. Annu Rev Neurosci 27: 419-451, 2004.
18. Dykes RW. Mechanisms controlling neuronal plasticity in somatosensory cortex. Can J Physiol Pharmacol 75: 535-545, 1997.
19. Ego-Stengel V, Mello e Souza T, Jacob V, and Shulz DE. Spatiotemporal characteristics of neuronal sensory integration in the barrel cortex of the rat. J Neurophysiol 93: 1450-1467.
20. Fee MS, Mitra PP, and Kleinfeld D. Automatic sorting of multiple unit neuronal signals in the presence of anisotropic and non-Gaussian variability. J Neurosci Methods 69: 175-188, 1996.
21. Finnerty GT, Roberts LS, and Connors BW. Sensory experience modifies the short-term dynamics of neocortical synapses. Nature 400: 367-371, 1999.
22. Foeller E and Feldman DE. Synaptic basis for developmental plasticity in somatosensory cortex. Curr Opin Neurobiol 14: 89-95, 2004.
23. Foeller E, Vater M, and Kossl M. Laminar analysis of inhibition in the gerbil primary auditory cortex. J Assoc Res Otolaryngol 2: 279-296, 2001.
24. Fox K. A critical period for experience-dependent synaptic plasticity in rat barrel cortex. J Neurosci 12: 1826-1838, 1992.
25. Fox K. Anatomical pathways and molecular mechanisms for plasticity in the barrel cortex. Neuroscience 111: 799-814, 2002.
26. Friedberg MH, Lee SM, and Ebner FF. Modulation of receptive field properties of thalamic somatosensory neurons by the depth of anesthesia. J Neurophysiol 81: 2243-2252, 1999.
27. Fuchs JL and Salazar E. Effects of whisker trimming on GABA(A) receptor binding in the barrel cortex of developing and adult rats. J Comp Neurol 395: 209-216, 1998.
28. Gaiarsa JL, Caillard O, and Ben-Ari Y. Long-term plasticity at GABAergic and glycinergic synapses: mechanisms and functional significance. Trends Neurosci 25: 564-570, 2002.
29. Gierdalski M, Jablonska B, Siucinska E, Lech M, Skibinska A, and Kossut M. Rapid regulation of GAD67 mRNA and protein level in cortical neurons after sensory learning. Cereb Cortex 11: 806-815, 2001.
30. Glazewski S and Fox K. Time course of experience-dependent synaptic potentiation and depression in barrel cortex of adolescent rats. J Neurophysiol 75: 1714-1729, 1996.
31. Heeger DJ. Normalization of cell responses in cat striate cortex. Vis Neurosci 9: 181-197, 1992.
32. Hendry SH and Jones EG. Reduction in number of immunostained GABAergic neurons in deprived-eye dominance columns of monkey area 17. Nature 320: 750-753, 1986.
33. Hensch TK. Critical period regulation. Annu Rev Neurosci 27: 549-579, 2004.
34. Hensch TK and Stryker MP. Columnar architecture sculpted by GABA circuits in developing cat visual cortex. Science 303: 1678-1681, 2004.
35. Heynen AJ, Yoon BJ, Liu CH, Chung HJ, Huganir RL, and Bear MF. Molecular mechanism for loss of visual cortical responsiveness following brief monocular deprivation. Nat Neurosci 6: 854-862, 2003.
36. Jacobs KM and Donoghue JP. Reshaping the cortical motor map by unmasking latent intracortical connections. Science 251: 944-947, 1991.
37. Jones EG. GABAergic neurons and their role in cortical plasticity in primates. Cereb Cortex 3: 361-372, 1993.
38. Kandler K. Activity-dependent organization of inhibitory circuits: lessons from the auditory system. Curr Opin Neurobiol 14: 96-104, 2004.
39. Kelly MK, Carvell GE, Kodger JM, and Simons DJ. Sensory loss by selected whisker removal produces immediate disinhibition in the somatosensory cortex of behaving rats. J Neurosci 19: 9117-9125, 1999.
40. A receptor activity by phosphorylation and receptor trafficking: implications for the efficacy of synaptic inhibition. Curr Opin Neurobiol 13: 341-347, 2003.
41. Knott GW, Quairiaux C, Genoud C, and Welker E. Formation of dendritic spines with GABAergic synapses induced by whisker stimulation in adult mice. Neuron 34: 265-273, 2002.
42. Komatsu Y and Iwakiri M. Long-term modification of inhibitory synaptic transmission in developing visual cortex. Neuroreport 4: 907-910, 1993.
43. Kyriazi H, Carvell GE, Brumberg JC, and Simons DJ. Laminar differences in bicuculline methiodide's effects on cortical neurons in the rat whisker/barrel system. Somatosens Mot Res 15: 146-156, 1998.
44. Kyriazi HT, Carvell GE, Brumberg JC, and Simons DJ. Effects of baclofen and phaclofen on receptive field properties of rat whisker barrel neurons. Brain Res 712: 325-328, 1996a.
45. Kyriazi HT, Carvell GE, Brumberg JC, and Simons DJ. Quantitative effects of GABA and bicuculline methiodide on receptive field properties of neurons in real and simulated whisker barrels. J Neurophysiol 75: 547-560, 1996b.
46. Lech M, Skibinska A, and Kossut M. Delayed upregulation of GABA(A) alpha1 receptor subunit mRNA in somatosensory cortex of mice following learning-dependent plasticity of cortical representations. Brain Res Mol Brain Res 96: 82-86, 2001.
47. Lendvai B, Stern E, Chen B, and Svoboda K. Experience-dependent plasticity of dendritic spines in the developing rat barrel cortex in vivo. Nature 404: 876-881, 2000.
48. Lowel S and Singer W. Selection of intrinsic horizontal connections in the visual cortex by correlated neuronal activity. Science 255: 209-212, 1992.
49. Marsicano G, Wotjak CT, Azad SC, Bisogno T, Rammes G, Cascio MG, Hermann H, Tang J, Hofmann C, Zieglgansberger W, Di Marzo V, and Lutz B. The endogenous cannabinoid system controls extinction of aversive memories. Nature 418: 530-534, 2002.
50. Martin KA. The Wellcome Prize lecture. From single cells to simple circuits in the cerebral cortex. Q J Exp Physiol 73: 637-702, 1988.
51. Marty A and Llano I. Modulation of inhibitory synapses in the mammalian brain. Curr Opin Neurobiol 5: 335-341, 1995.
52. Massie A, Cnops L, Smolders I, Van Damme K, Vandenbussche E, Vandesande F, Eysel UT, and Arckens L. Extracellular GABA concentrations in area 17 of cat visual cortex during topographic map reorganization following binocular central retinal lesioning. Brain Res 976: 100-108, 2003.
53. Micheva KD and Beaulieu C. Quantitative aspects of synaptogenesis in the rat barrel field cortex with special reference to GABA circuitry. J Comp Neurol 373: 340-354, 1996.
54. Micheva KD and Beaulieu C. Development and plasticity of the inhibitory neocortical circuitry with an emphasis on the rodent barrel field cortex: a review. Can J Physiol Pharmacol 75: 470-478, 1997.
55. Miller KD, Pinto DJ, and Simons DJ. Processing in layer 4 of the neocortical circuit: new insights from visual and somatosensory cortex. Curr Opin Neurobiol 11: 488-497, 2001.
56. Moore CI and Nelson SB. Spatio-temporal subthreshold receptive fields in the vibrissa representation of rat primary somatosensory cortex. J Neurophysiol 80: 2882-2892, 1998.
57. Mower GD, Christen WG, Burchfiel JL, and Duffy FH. Microiontophoretic bicuculline restores binocular responses to visual cortical neurons in strabismic cats. Brain Res 309: 168-172, 1984.
58. Petersen CC, Hahn TT, Mehta M, Grinvald A, and Sakmann B. Interaction of sensory responses with spontaneous depolarization in layer 2/3 barrel cortex. Proc Natl Acad Sci USA 100: 13638-13643, 2003.
59. Porter JT, Johnson CK, and Agmon A. Diverse types of interneurons generate thalamus-evoked feedforward inhibition in the mouse barrel cortex. J Neurosci 21: 2699-2710, 2001.
60. Priebe NJ and Ferster D. Direction selectivity of excitation and inhibition in simple cells of the cat primary visual cortex. Neuron 45: 133-145, 2005.
61. Rajan R. Receptor organ damage causes loss of cortical surround inhibition without topographic map plasticity. Nat Neurosci 1: 138-143, 1998.
62. Rajan R. Plasticity of excitation and inhibition in the receptive field of primary auditory cortical neurons after limited receptor organ damage. Cereb Cortex 11: 171-182, 2001.
63. Rosier AM, Arckens L, Demeulemeester H, Orban GA, Eysel UT, Wu YJ, and Vandesande F. Effect of sensory deafferentation on immunoreactivity of GABAergic cells and on GABA receptors in the adult cat visual cortex. J Comp Neurol 359: 476-489, 1995.
64. Sillito AM, Kemp JA, and Blakemore C. The role of GABAergic inhibition in the cortical effects of monocular deprivation. Nature 291: 318-320, 1981.
65. Simons DJ and Carvell GE. Thalamocortical response transformation in the rat vibrissa/barrel system. J Neurophysiol 61: 311-330, 1989.
66. Skibinska A, Glazewski S, Fox K, and Kossut M. Age-dependent response of the mouse barrel cortex to sensory deprivation: a 2-deoxyglucose study. Exp Brain Res 132: 134-138, 2000.
67. Sompolinsky H and Shapley R. New perspectives on the mechanisms for orientation selectivity. Curr Opin Neurobiol 1: 514-522, 1997.
68. Stern EA, Maravall M, and Svoboda K. Rapid development and plasticity of layer 2/3 maps in rat barrel cortex in vivo. Neuron 31: 305-315, 2001.
69. Swadlow HA and Gusev AG. Receptive-field construction in cortical inhibitory interneurons. Nat Neurosci 5: 403-404, 2002.
70. Takahashi T, Svoboda K, and Malinow R. Experience strengthening transmission by driving AMPA receptors into synapses. Science 299: 1585-1588, 2003.
71. Trachtenberg JT and Stryker MP. Rapid anatomical plasticity of horizontal connections in the developing visual cortex. J Neurosci 21: 3476-3482, 2001.
72. Tremere L, Hicks TP, and Rasmusson DD. Role of inhibition in cortical reorganization of the adult raccoon revealed by microiontophoretic blockade of GABA(A) receptors. J Neurophysiol 86: 94-103, 2001.
73. Wallace H and Fox K. Local cortical interactions determine the form of cortical plasticity. J Neurobiol 41: 58-63, 1999.
74. Wang J, McFadden SL, Caspary D, and Salvi R. Gamma-aminobutyric acid circuits shape response properties of auditory cortex neurons. Brain Res 944: 219-231, 2002.
75. Wehr M and Zador AM. Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature 426: 442-446, 2003.
76. Welker E, Armstrong-James M, Van der Loos H, and Kraftsik R. The mode of activation of a barrel column: response properties of single units in the somatosensory cortex of the mouse upon whisker deflection. Eur J Neurosci 5: 691-712, 1993.
77. A receptor binding in layer IV of adult primate somatosensory cortex after peripheral nerve injury. Brain Res 954: 68-72, 2002.
78. Wilent WB and Contreras D. Synaptic responses to whisker deflections in rat barrel cortex as a function of cortical layer and stimulus intensity. J Neurosci 24: 3985-3998, 2004.
79. Wong-Riley M. Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry. Brain Res 171: 11-28, 1979.
80. Woodin MA, Ganguly K, and Poo MM. Coincident pre- and postsynaptic activity modifies GABAergic synapses by postsynaptic changes in Cl-transporter activity. Neuron 39: 807-820, 2003.
81. Woolsey TA and Van der Loos H. The structural organization of layer IV in the somatosensory region (SI) of mouse cerebral cortex. The description of a cortical field composed of discrete cytoarchitectonic units. Brain Res 17: 205-242, 1970.
82. A-mediated inhibition. Science 284: 962-965, 1999.
83. Zheng W and Knudsen EI. Gabaergic inhibition antagonizes adaptive adjustment of the owl's auditory space map during the initial phase of plasticity. J Neurosci 21: 4356-4365, 2001.