The Excitatory Neuronal Network of the C2 Barrel Column in Mouse Primary Somatosensory Cortex

Neuron

Volumn 61, Issue 2, 2009, Pages 301-316

  Lefort, Sandrine ^a   Tomm, Christian ^a   Floyd Sarria, J C ^b   Petersen, Carl C H ^a  

^a Brain Mind Institute   (Switzerland)

^b EPFL   (Switzerland)

Author keywords

SYSNEURO

Indexed keywords

ANIMAL TISSUE; ARTICLE; EXCITATORY POSTSYNAPTIC POTENTIAL; INFORMATION PROCESSING; MEMBRANE STEADY POTENTIAL; MOUSE; NERVE CELL EXCITABILITY; NERVE CELL NETWORK; NONHUMAN; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SOMATOSENSORY CORTEX; SYNAPSE;

ACTION POTENTIALS; AFFERENT PATHWAYS; ANIMALS; EXCITATORY POSTSYNAPTIC POTENTIALS; FLUORESCENT DYES; MECHANORECEPTORS; MICE; MICE, INBRED C57BL; NERVE NET; NEURAL PATHWAYS; NEURONS; ORGAN CULTURE TECHNIQUES; PATCH-CLAMP TECHNIQUES; SOMATOSENSORY CORTEX; STAINING AND LABELING; SYNAPSES; SYNAPTIC TRANSMISSION; TOUCH; TRIGEMINAL NERVE; VIBRISSAE;

EID: 58549118757     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2008.12.020     Document Type: Article

References (83)

1. Allen C.B., Celikel T., and Feldman D.E. Long-term depression induced by sensory deprivation during cortical map plasticity in vivo. Nat. Neurosci. 6 (2003) 291-299
2. Arenkiel B.R., Peca J., Davison I.G., Feliciano C., Deisseroth K., Augustine G.J., Ehlers M.D., and Feng G. In vivo light-induced activation of neural circuitry in transgenic mice expressing channelrhodopsin-2. Neuron 54 (2007) 205-218
3. Aronoff R., and Petersen C.C.H. Layer, column and cell-type specific genetic manipulation in mouse barrel cortex. Front. Neurosci. 2 (2008) 64-71
4. Bender K.J., Allen C.B., Bender V.A., and Feldman D.E. Synaptic basis for whisker deprivation-induced synaptic depression in rat somatosensory cortex. J. Neurosci. 26 (2006) 4155-4165
5. Binzegger T., Douglas R.J., and Martin K.A. A quantitative map of the circuit of cat primary visual cortex. J. Neurosci. 24 (2004) 8441-8453
6. Boyden E.S., Zhang F., Bamberg E., Nagel G., and Deisseroth K. Millisecond-timescale, genetically targeted optical control of neural activity. Nat. Neurosci. 8 (2005) 1263-1268
7. Braitenberg V., and Schüz A. Cortex: Statistics and Geometry of Neuronal Connectivity (1998), Springer-Verlag, Berlin
8. Brasier D.J., and Feldman D.E. Synapse-specific expression of functional presynaptic NMDA receptors in rat somatosensory cortex. J. Neurosci. 28 (2008) 2199-2211
9. Brecht M., Schneider M., Sakmann B., and Margrie T.W. Whisker movements evoked by stimulation of single pyramidal cells in rat motor cortex. Nature 427 (2004) 704-710
10. Briggman K.L., and Denk W. Towards neural circuit reconstruction with volume electron microscopy techniques. Curr. Opin. Neurobiol. 16 (2006) 562-570
11. Brunel N., Hakim V., Isope P., Nadal J.P., and Barbour B. Optimal information storage and the distribution of synaptic weights: perceptron versus Purkinje cell. Neuron 43 (2004) 745-757
12. Bureau I., Shepherd G.M., and Svoboda K. Precise development of functional and anatomical columns in the neocortex. Neuron 42 (2004) 789-801
13. Bureau I., von Saint Paul F., and Svoboda K. Interdigitated paralemniscal and lemniscal pathways in the mouse barrel cortex. PLoS Biol. 4 (2006) e382
14. Callaway E.M., and Katz L.C. Photostimulation using caged glutamate reveals functional circuitry in living brain slices. Proc. Natl. Acad. Sci. USA 90 (1993) 7661-7665
15. Cheetham C.E., Hammond M.S., Edwards C.E., and Finnerty G.T. Sensory experience alters cortical connectivity and synaptic function site specifically. J. Neurosci. 27 (2007) 3456-3465
16. Clem R.L., Celikel T., and Barth A.L. Ongoing in vivo experience triggers synaptic metaplasticity in the neocortex. Science 319 (2008) 101-104
17. Crochet S., and Petersen C.C.H. Correlating whisker behavior with membrane potential in barrel cortex of awake mice. Nat. Neurosci. 9 (2006) 608-610
18. Crochet S., Chauvette S., Boucetta S., and Timofeev I. Modulation of synaptic transmission in neocortex by network activities. Eur. J. Neurosci. 21 (2005) 1030-1044
19. Diesmann, M., and Gewaltig, M.-O. (2002). NEST: An environment for neural systems simulations. In T. Plesser and V. Macho (Eds.), Forschung und wisschenschaftliches Rechnen, Beitrage zum Heinz-Billing-Preis 2001, Volume 58 of GWDG-Bericht, (pp. 43-70). Gottingen: Ges. fur Wiss. Datenverarbeitung.
20. Douglas R.J., Koch C., Mahowald M., Martin K.A.C., and Suarez H.H. Recurrent excitation in neocortical circuits. Science 269 (1995) 981-985
21. Feldman D.E. Timing-based LTP and LTD at vertical inputs to layer II/III pyramidal cells in rat barrel cortex. Neuron 27 (2000) 45-56
22. Feldman D.E., and Brecht M. Map plasticity in somatosensory cortex. Science 310 (2005) 810-815
23. Feldmeyer D., Egger V., Lübke J., and Sakmann B. Reliable synaptic connections between pairs of excitatory layer 4 neurones within a single 'barrel' of developing rat somatosensory cortex. J. Physiol. 521 (1999) 169-190
24. Feldmeyer D., Lübke J., Silver R.A., and Sakmann B. Synaptic connections between layer 4 spiny neurone-layer 2/3 pyramidal cell pairs in juvenile rat barrel cortex: physiology and anatomy of interlaminar signalling within a cortical column. J. Physiol. 538 (2002) 803-822
25. Feldmeyer D., Roth A., and Sakmann B. Monosynaptic connections between pairs of spiny stellate cells in layer 4 and pyramidal cells in layer 5A indicate that lemniscal and paralemniscal afferent pathways converge in the infragranular somatosensory cortex. J. Neurosci. 25 (2005) 3423-3431
26. Feldmeyer D., Lübke J., and Sakmann B. Efficacy and connectivity of intracolumnar pairs of layer 2/3 pyramidal cells in the barrel cortex of juvenile rats. J. Physiol. 575 (2006) 583-602
27. Ferezou I., Bolea S., and Petersen C.C.H. Visualizing the cortical representation of whisker touch: voltage-sensitive dye imaging in freely moving mice. Neuron 50 (2006) 617-629
28. Ferezou I., Haiss F., Gentet L.J., Aronoff R., Weber B., and Petersen C.C.H. Spatiotemporal dynamics of cortical sensorimotor integration in behaving mice. Neuron 56 (2007) 907-923
29. Finnerty G.T., Roberts L.S., and Connors B.W. Sensory experience modifies the short-term dynamics of neocortical synapses. Nature 400 (1999) 367-371
30. Fox K. Anatomical pathways and molecular mechanisms for plasticity in the barrel cortex. Neuroscience 111 (2002) 799-814
31. Frick A., Feldmeyer D., Helmstaedter M., and Sakmann B. Monosynaptic connections between pairs of L5A pyramidal neurons in columns of juvenile rat somatosensory cortex. Cereb. Cortex 18 (2008) 397-406
32. Gerstner W., and Kistler W. Spiking Neuron Models: Single Neurons, Populations, Plasticity (2002), Cambridge University Press, United Kingdom
33. Gilbert C.D., and Sigman M. Brain states: top-down influences in sensory processing. Neuron 54 (2007) 677-696
34. Gong S., Zheng C., Doughty M.L., Losos K., Didkovsky N., Schambra U.B., Nowak N.J., Joyner A., Leblanc G., Hatten M.E., and Heintz N. A gene expression atlas of the central nervous system based on bacterial artificial chromosomes. Nature 425 (2003) 917-925
35. Greenberg D.S., Houweling A.R., and Kerr J.N. Population imaging of ongoing neuronal activity in the visual cortex of awake rats. Nat. Neurosci. 11 (2008) 749-751
36. Grinvald A., Lieke E., Frostig R.D., Gilbert C.D., and Wiesel T.N. Functional architecture of cortex revealed by optical imaging of intrinsic signals. Nature 324 (1986) 361-364
37. Harris J.A., Petersen R.S., and Diamond M.E. Distribution of tactile learning and its neural basis. Proc. Natl. Acad. Sci. USA 96 (1999) 7587-7591
38. Hebb D.O. The Organization of Behaviour (1949), Wiley, New York
39. Heynen A.J., Yoon B.J., Liu C.H., Chung H.J., Huganir R.L., and Bear M.F. Molecular mechanism for loss of visual cortical responsiveness following brief monocular deprivation. Nat. Neurosci. 6 (2003) 854-862
40. Houweling A.R., and Brecht M. Behavioural report of single neuron stimulation in somatosensory cortex. Nature 451 (2008) 65-68
41. Huber D., Petreanu L., Ghitani N., Ranade S., Hromádka T., Mainen Z., and Svoboda K. Sparse optical microstimulation in barrel cortex drives learned behaviour in freely moving mice. Nature 451 (2008) 61-64
42. Hutson K.A., and Masterton R.B. The sensory contribution of a single vibrissa's cortical barrel. J. Neurophysiol. 56 (1986) 1196-1223
43. Kampa B.M., Letzkus J.J., and Stuart G.J. Cortical feed-forward networks for binding different streams of sensory information. Nat. Neurosci. 9 (2006) 1472-1473
44. Kozloski J., Hamzei-Sichani F., and Yuste R. Stereotyped position of local synaptic targets in neocortex. Science 293 (2001) 868-872
45. Le Bé J.V., Silberberg G., Wang Y., and Markram H. Morphological, electrophysiological, and synaptic properties of corticocallosal pyramidal cells in the neonatal rat neocortex. Cereb. Cortex 17 (2007) 2204-2213
46. Lee A.K., Manns I.D., Sakmann B., and Brecht M. Whole-cell recordings in freely moving rats. Neuron 51 (2006) 399-407
47. Luo L., Callaway E.M., and Svoboda K. Genetic dissection of neural circuits. Neuron 57 (2008) 634-660
48. Maffei A., Nelson S.B., and Turrigiano G.G. Selective reconfiguration of layer 4 visual cortical circuitry by visual deprivation. Nat. Neurosci. 7 (2004) 1353-1359
49. Markram H. The blue brain project. Nat. Rev. Neurosci. 7 (2006) 153-160
50. Markram H., Lübke J., Frotscher M., and Sakmann B. Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science 275 (1997) 213-215
51. Nagel G., Szellas T., Huhn W., Kateriya S., Adeishvili N., Berthold P., Ollig D., Hegemann P., and Bamberg E. Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. Proc. Natl. Acad. Sci. USA 100 (2003) 13940-13945
52. Nelson S.B., Sugino K., and Hempel C.M. The problem of neuronal cell types: a physiological genomics approach. Trends Neurosci. 29 (2006) 339-345
53. Nevian T., Larkum M.E., Polsky A., and Schiller J. Properties of basal dendrites of layer 5 pyramidal neurons: a direct patch-clamp recording study. Nat. Neurosci. 10 (2007) 206-214
54. Nikolenko V., Poskanzer K.E., and Yuste R. Two-photon photostimulation and imaging of neural circuits. Nat. Methods 4 (2007) 943-950
55. Petersen C.C.H. The functional organization of the barrel cortex. Neuron 56 (2007) 339-355
56. Petersen C.C.H., and Sakmann B. The excitatory neuronal network of rat layer 4 barrel cortex. J. Neurosci. 20 (2000) 7579-7586
57. Petersen C.C.H., and Sakmann B. Functionally independent columns of rat somatosensory barrel cortex revealed with voltage-sensitive dye imaging. J. Neurosci. 21 (2001) 8435-8446
58. Petreanu L., Huber D., Sobczyk A., and Svoboda K. Channelrhodopsin-2-assisted circuit mapping of long-range callosal projections. Nat. Neurosci. 10 (2007) 663-668
59. Poulet J.F.A., and Petersen C.C.H. Internal brain state regulates membrane potential synchrony in barrel cortex of behaving mice. Nature 454 (2008) 881-885
60. Sarid L., Bruno R., Sakmann B., Segev I., and Feldmeyer D. Modeling a layer 4-to-layer 2/3 module of a single column in rat neocortex: interweaving in vitro and in vivo experimental observations. Proc. Natl. Acad. Sci. USA 104 (2007) 16353-16358
61. Sawatari A., and Callaway E.M. Diversity and cell type specificity of local excitatory connections to neurons in layer 3B of monkey primary visual cortex. Neuron 25 (2000) 459-471
62. Schubert D., Staiger J.F., Cho N., Kötter R., Zilles K., and Luhmann H.J. Layer-specific intracolumnar and transcolumnar functional connectivity of layer V pyramidal cells in rat barrel cortex. J. Neurosci. 21 (2001) 3580-3592
63. Schubert D., Kötter R., Zilles K., Luhmann H.J., and Staiger J.F. Cell type-specific circuits of cortical layer IV spiny neurons. J. Neurosci. 23 (2003) 2961-2970
64. Schubert D., Kötter R., Luhmann H.J., and Staiger J.F. Morphology, electrophysiology and functional input connectivity of pyramidal neurons characterizes a genuine layer Va in the primary somatosensory cortex. Cereb. Cortex 16 (2006) 223-236
65. Shepherd G.M., and Svoboda K. Laminar and columnar organization of ascending excitatory projections to layer 2/3 pyramidal neurons in rat barrel cortex. J. Neurosci. 25 (2005) 5670-5679
66. Shepherd G.M., Pologruto T.A., and Svoboda K. Circuit analysis of experience-dependent plasticity in the developing rat barrel cortex. Neuron 38 (2003) 277-289
67. Shepherd G.M., Stepanyants A., Bureau I., Chklovskii D., and Svoboda K. Geometric and functional organization of cortical circuits. Nat. Neurosci. 8 (2005) 782-790
68. Silberberg G., Grillner S., LeBeau F.E., Maex R., and Markram H. Synaptic pathways in neural microcircuits. Trends Neurosci. 28 (2005) 541-551
69. Silver R.A., Lubke J., Sakmann B., and Feldmeyer D. High-probability uniquantal transmission at excitatory synapses in barrel cortex. Science 302 (2003) 1981-1984
70. Sjöström P.J., Turrigiano G.G., and Nelson S.B. Rate, timing, and cooperativity jointly determine cortical synaptic plasticity. Neuron 32 (2001) 1149-1164
71. Sjöström P.J., Turrigiano G.G., and Nelson S.B. Neocortical LTD via coincident activation of presynaptic NMDA and cannabinoid receptors. Neuron 39 (2003) 641-654
72. Song S., Sjöström P.J., Reigl M., Nelson S.B., and Chklovskii D.B. Highly nonrandom features of synaptic connectivity in local cortical circuits. PLoS Biol. 3 (2005) e68
73. Sugino K., Hempel C.M., Miller M.N., Hattox A.M., Shapiro P., Wu C., Huang Z.J., and Nelson S.B. Molecular taxonomy of major neuronal classes in the adult mouse forebrain. Nat. Neurosci. 9 (2006) 99-107
74. Takahashi T., Svoboda K., and Malinow R. Experience strengthening transmission by driving AMPA receptors into synapses. Science 299 (2003) 1585-1588
75. Tamamaki N., Yanagawa Y., Tomioka R., Miyazaki J., Obata K., and Kaneko T. Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67-GFP knock-in mouse. J. Comp. Neurol. 467 (2003) 60-79
76. Thomson A.M., and Lamy C. Functional maps of neocortical local circuitry. Front. Neurosci. 1 (2007) 19-42
77. Wang H., Peca J., Matsuzaki M., Matsuzaki K., Noguchi J., Qiu L., Wang D., Zhang F., Boyden E., Deisseroth K., et al. High-speed mapping of synaptic connectivity using photostimulation in Channelrhodopsin-2 transgenic mice. Proc. Natl. Acad. Sci. USA 104 (2007) 8143-8148
78. Watts D.J., and Strogatz S.H. Collective dynamics of 'small-world' networks. Nature 393 (1998) 440-442
79. Weiler N., Wood L., Yu J., Solla S.A., and Shepherd G.M. Top-down laminar organization of the excitatory network in motor cortex. Nat. Neurosci. 11 (2008) 360-366
80. Wickersham I.R., Lyon D.C., Barnard R.J., Mori T., Finke S., Conzelmann K.K., Young J.A., and Callaway E.M. Monosynaptic restriction of transsynaptic tracing from single, genetically targeted neurons. Neuron 53 (2007) 639-647
81. Williams S.R., and Stuart G.J. Dependence of EPSP efficacy on synapse location in neocortical pyramidal neurons. Science 295 (2002) 1907-1910
82. Woolsey T.A., 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 (1970) 205-242
83. Yoshimura Y., Dantzker J.L., and Callaway E.M. Excitatory cortical neurons form fine-scale functional networks. Nature 433 (2005) 868-873