Sensory learning-induced enhancement of inhibitory synaptic transmission in the barrel cortex of the mouse

European Journal of Neuroscience

Volumn 26, Issue 1, 2007, Pages 134-141

  Tokarski, Krzysztof ^a   Urban Ciecko, Joanna ^b   Kossut, Malgorzata ^b,d   Hess, Grzegorz ^a,c  

^a INSTITUTE OF PHARMACOLOGY   (Poland)

^b NENCKI INSTITUTE OF EXPERIMENTAL BIOLOGY   (Poland)

^c JAGIELLONIAN UNIVERSITY   (Poland)

^d SWPS UNIVERSITY OF SOCIAL SCIENCES AND HUMANITIES   (Poland)

Author keywords

Brain slices; Classical conditioning; Cortical maps; Inhibitory transmission; Somatosensory cortex

Indexed keywords

AMPLITUDE MODULATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; FEMALE; GABAERGIC TRANSMISSION; INHIBITORY POSTSYNAPTIC POTENTIAL; MOUSE; NONHUMAN; POSTSYNAPTIC INHIBITION; PRIORITY JOURNAL; RECORDING; SOMATOSENSORY CORTEX; SPIKE WAVE; STATE DEPENDENT LEARNING; SYNAPTIC INHIBITION; SYNAPTIC TRANSMISSION; VIBRISSA;

ANIMALS; CONDITIONING, CLASSICAL; ELECTROPHYSIOLOGY; EVOKED POTENTIALS, SOMATOSENSORY; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; INTERNEURONS; KINETICS; MEMBRANE POTENTIALS; MICE; NEURONS; SOMATOSENSORY CORTEX; SYNAPTIC TRANSMISSION;

EID: 34447128208     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2007.05629.x     Document Type: Article

References (51)

1. Beierlein, M., Gibson, J.R. Connors, B.W. (2003) Two dynamically distinct inhibitory networks in layer 4 of the neocortex. J. Neurophysiol., 90, 2987 3000.
2. Carvell, G.E. Simons, D.J. (1990) Biometric analyses of vibrissal tactile discrimination in the rat. J. Neurosci., 10, 2638 2648.
3. Castro-Alamancos, M.A. (2002) Role of thalamocortical sensory suppression during arousal: focusing sensory inputs in neocortex. J. Neurosci., 22, 9651 9655.
4. Chmielowska, J., Carvell, G.E. Simons, D.J. (1989) Spatial organization of thalamocortical and corticothalamic projection systems in rat SmI barrel cortex. J. Comp. Neurol., 285, 325 338.
5. Cybulska-Klosowicz, A. Kossut, M. (2006) Early phase of learning enhances communication between brain hemispheres. Eur. J. Neurosci., 24, 1470 1476.
6. Emptage, N.J., Reid, C.A. Fine, A. (2001) Calcium stores in hippocampal synaptic boutons mediate short-term plasticity, store-operated Ca2+ entry, and spontaneous transmitter release. Neuron, 29, 197 208.
7. Feldman, D.E., Nicoll, R.A. Malenka, R.C. (1999) Synaptic plasticity at thalamocortical synapses in developing rat somatosensory cortex: LTP, LTD and silent synapses. J. Neurobiol., 41, 92 101.
8. Foeller, E. Feldman, D.E. (2004) Synaptic basis for developmental plasticity in somatosensory cortex. Curr. Opin. Neurobiol., 14, 89 95.
9. Fox, K. (2002) Anatomical pathways and molecular mechanisms for plasticity in the barrel cortex. Neuroscience, 111, 799 814.
10. Galante, M. Marty, A. (2003) Presynaptic ryanodine-sensitive calcium stores contribute to evoked neurotransmitter release at the basket cell-Purkinje cell synapse. J. Neurosci., 23, 11229 11234.
11. Gibson, J.R., Beierlein, M. Connors, B.W. (1999) Two networks of electrically coupled inhibitory neurons in neocortex. Nature, 402, 75 79.
12. Gierdalski, M., Jablonska, B., Siucinska, E., Lech, M., Skibinska, A. Kossut, M. (2001) Rapid regulation of GAD67 mRNA and protein level in cortical neurons after sensory learning. Cereb. Cortex, 11, 806 815.
13. Glazewski, S., McKenna, M., Jacquin, M. Fox, K. (1998) Experience-dependent depression of vibrissae responses in adolescent rat barrel cortex. Eur. J. Neurosci., 10, 2107 2116.
14. Gu, Q. (2002) Neuromodulatory transmitter systems in the cortex and their role in cortical plasticity. Neuroscience, 111, 815 835.
15. Hardingham, N. Fox, K. (2006) The role of nitric oxide and GluR1 in presynaptic and postsynaptic components of neocortical potentiation. J. Neurosci., 26, 7395 7404.
16. Herron, P., Zhang, L., Li, Z. Schweitzer, J.B. (1997) Effects of cholinergic depletion on glutamic acid decarboxylase immunoreactivity in the somatosensory cortex of rats. Anat. Embryol. (Berl.), 196, 27 38.
17. Hess, G., Jacobs, K.M. Donoghue, J.P. (1994) N-methyl-d-aspartate receptor-mediated component of field potentials evoked in horizontal pathways of rat motor cortex. Neuroscience, 61, 225 235.
18. Holmgren, C.D. Zilberter, Y. (2001) Concident spiking activity induces long-term changes in inhibition of neocortical pyramidal cells. J. Neurosci., 21, 8270 8277.
19. Jablonska, B., Kossut, M. Skangiel-Kramska, J. (1996) Transient increase of AMPA and NMDA receptor binding in the barrel cortex of mice after tactile stimulation. Neurobiol. Learn. Mem., 66, 36 43.
20. Jablonska, B. Skangiel-Kramska, J. (1995) Sensory conditioning and sensory stimulation do not affect GABAA receptor binding in the barrel field of mice. Acta Neurobiol. Exp. (Wars.), 55, 289 293.
21. Jiao, Y., Zhang, C., Yanagawa, Y. Sun, Q.-Q. (2006) Major effects of sensory experience on the neocortical inhibitory circuits. J. Neurosci., 26, 8691 8701.
22. Kawaguchi, Y. Kubota, Y. (1997) GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb. Cortex, 7, 476 486.
23. Knott, G.W., Quairiaux, C., Genoud, C. Welker, E. (2002) Formation of dendritic spines with GABAergic synapses induced by whisker stimulation in adult mice. Neuron, 34, 265 273.
24. Komatsu, Y. (1994) Age-dependent long-term potentiation of inhibitory synaptic transmission in rat visual cortex. J. Neurosci., 14, 6488 6499.
25. Lauri, S.E., Palmer, M., Segerstrale, M., Vesikansa, A., Taira, T. Collingridge, G.L. (2007) Presynaptic mechanisms involved in the expression of STP and LTP at CA1 synapses in the hippocampus. Neuropharmacology, 52, 1 11.
26. Lech, M., Skibinska, A. Kossut, M. (2001) Delayed upregulation of GABAA alpha1 receptor subunit mRNA in somatosensory cortex of mice following learning-dependent plasticity of cortical representations. Mol. Brain Res., 96, 82 86.
27. Lech, M., Skibinska, A., Siucinska, E. Kossut, M. (2005) Learning-induced plasticity of cortical representations does not affect GAD65 mRNA expression and immunolabeling of cortical neuropil. Brain Res., 1044, 266 271.
28. Lee, W.C., Huang, H., Feng, G., Sanes, J.R., Brown, E.N., So, P.T. Nedivi, E. (2006) Dynamic remodeling of dendritic arbors in GABAergic interneurons of adult visual cortex. PLoS Biol. 4, e29.
29. Lübke, J., Egger, V., Sakmann, B. Feldmeyer, D. (2000) Columnar organization of dendrites and axons of single and synaptically coupled excitatory spiny neurons in layer 4 of the rat barrel cortex. J. Neurosci., 20, 5300 5311.
30. Maffei, A., Nataraj, K., Nelson, S.B. Turrigiano, G.G. (2006) Potentiation of cortical inhibition by visual deprivation. Nature, 443, 81 84.
31. Micheva, K.D. Beaulieu, C. (1995) An anatomical substrate for experience-dependent plasticity of the rat barrel cortex. Proc. Natl Acad. Sci. USA, 92, 11834 11838.
32. Miller, K.D., Pinto, D.J. Simons, D.J. (2001) Processing in layer 4 of the neocortical circuit: New insights from visual and somatosensory cortex. Curr. Opin. Neurobiol., 11, 488 497.
33. Porter, J., Johnson, C.K. Agmon, A. (2001) Diverse types of interneurons generate thalamus-evoked feedforward inhibition in the mouse barrel cortex. J. Neurosci., 21, 2699 2710.
34. Quairiaux, C., Armstrong-James, M. Welker, E. (2007) Modified sensory processing in the barrel cortex of the adult mouse following chronic whisker stimulation. J. Neurophysiol., 97, 2130 2147.
35. Salin, P.A. Prince, D.A. (1996) Spontaneous GABAA receptor-mediated inhibitory currents in adult rat somatosensory cortex. J. Neurophysiol., 75, 1573 1588.
36. Schubert, D., Kötter, R., Zilles, K., Luhmann, H.J. Staiger, J.F. (2003) Cell type-specific circuits of cortical layer IV spiny neurons. J. Neurosci., 23, 2961 2970.
37. Simkus, C.R. Stricker, C. (2002) Properties of mEPSCs recorded in layer II neurones of rat barrel cortex. J. Physiol., 545, 509 520.
38. Siucinska, E. (2006) GAD67-positive puncta: Contributors to learning-dependent plasticity in the barrel cortex of adult mice. Brain Res., 1106, 52 62.
39. Siucinska, E. Kossut, M. (1996) Short-lasting classical conditioning induces reversible changes of representational maps in mouse SI cortex - a 2DG study. Cereb. Cortex, 6, 506 513.
40. Siucinska, E. Kossut, M. (2006) Short-term sensory learning does not alter parvalbumin neurons in the barrel cortex of adult mice: a double-labeling study. Neuroscience, 138, 715 724.
41. Siucinska, E., Kossut, M. Stewart, M.G. (1999) GABA immunoreactivity in mouse barrel field after aversive and appetitive classical conditioning training involving facial vibrissae. Brain Res., 843, 62 70.
42. Skibinska, A., Lech, M. Kossut, M. (2005) Differential regulation of cortical NMDA receptor subunits by sensory learning. Brain Res., 1065, 26 36.
43. Sola, E., Prestori, F., Rossi, P., Taglietti, V. D'Angelo, E. (2004) Increased neurotransmitter release during long-term potentiation at mossy fibre-granule cell synapses in rat cerebellum. J. Physiol., 557, 843 861.
44. Sun, Q.-Q., Huguenard, J.R. Prince, D.A. (2006) Barrel cortex microcircuits: thalamocortical inhibition in spiny stellate cells is mediated by a small number of fast-spiking interneurons. J. Neurosci., 26, 1219 1230.
45. Tokarski, K., Zahorodna, A., Bobula, B. Hess, G. (2003) 5-HT7 receptors increase the excitability of rat hippocampal CA1 pyramidal neurons. Brain Res., 993, 230 234.
46. Urban-Ciecko, J., Kossut, M. Hess, G. (2005) Effects of sensory learning on intracortical synaptic transmission in the barrel cortex of mice. Acta Neurobiol. Exp. (Wars.), 65, 195 200.
47. Welker, E., Soriano, E., Dorfl, J. Van der Loos, H. (1989a) Plasticity in the barrel cortex of the adult mouse: transient increase of GAD-immunoreactivity following sensory stimulation. Exp. Brain Res., 78, 659 664.
48. Welker, E., Soriano, E. Van der Loos, H. (1989b) Plasticity in the barrel cortex of the adult mouse: effects of peripheral deprivation on GAD-immunoreactivity. Exp. Brain Res., 74, 441 452.
49. Woolsey, T.A. Van der Loos, H. (1970) The structural organization of layer IV in the somatosensory region (SI) of mouse cerebral cortex. Brain Res., 17, 205 242.
50. Wrobel, A., Kublik, E. Musial, P. (1998) Gating of the sensory activity within barrel cortex of the awake rat. Exp. Brain Res., 123, 117 123.
51. Yamada, K., Inagaki, T., Funahashi, R., Yoshimura, Y. Komatsu, Y. (2006) High-frequency stimulation together with adrenoceptor activation facilitates the maintenance of long-term potentiation at visual cortical inhibitory synapses. Cereb. Cortex, 16, 1239 1248.