Spiking in auditory cortex following thalamic stimulation is dominated by cortical network activity

Frontiers in Systems Neuroscience

Volumn 8, Issue , 2014, Pages

  Krause, Bryan M ^a   Raz, Aeyal ^b,c,d   Uhlrich, Daniel J ^b   Smith, Philip H ^b   Banks, Matthew I ^b  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^c RABIN MEDICAL CENTER   (Israel)

^d TEL AVIV UNIVERSITY   (Israel)

Author keywords

Auditory cortex; Calcium imaging; Canonical microcircuit; Multiunit activity; Patch clamp; Thalamo cortical (TC); UP states

Indexed keywords

ANIMAL TISSUE; ARTICLE; AUDITORY CORTEX; BRAIN DEPTH STIMULATION; BRAIN ELECTROPHYSIOLOGY; BRAIN HISTOLOGY; CELL COUNT; CONTROLLED STUDY; ELECTRODE; FUNCTIONAL NEUROIMAGING; LATENT PERIOD; MALE; MEMBRANE POTENTIAL; MOUSE; NERVE CELL NETWORK; NERVE POTENTIAL; NONHUMAN; PATCH CLAMP TECHNIQUE; PERCEPTION; PHOTOCHEMICAL QUENCHING; POLARIZATION AND DEPOLARIZATION; SPIKE WAVE; THALAMIC STIMULATION;

EID: 84907284189     PISSN: 16625137     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnsys.2014.00170     Document Type: Article

References (136)

1. Adams, J. C. (1981). Heavy metal intensification of DAB-based HRP reaction product. J. Histochem. Cytochem. 29, 775. doi: 10.1177/29.6.7252134
2. Aponte, Y., Bischofberger, J., and Jonas, P. (2008). Efficient Ca2+ buffering in fast-spiking basket cells of rat hippocampus. J. Physiol. 86, 2061-2075. doi: 10.1113/jphysiol.2007.147298
3. Ascoli, G. A., Alonso-Nanclares, L., Anderson, S. A., Barrionuevo, G., BenavidesPiccione, R., Burkhalter, A., et al. (2008). Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex. Nat. Rev. Neurosci. 9, 557-568. doi: 10.1038/nrn2402
4. Atencio, C. A., Sharpee, T. O., and Schreiner, C. E. (2009). Hierarchical computation in the canonical auditory cortical circuit. Proc. Natl. Acad. Sci. U.S.A. 106, 21894-21899. doi: 10.1073/pnas.0908383106
5. Banks, M. I., Uhlrich, D. J., Smith, P. H., Krause, B. M., and Manning, K. A. (2011). Descending projections from extrastriate visual cortex modulate responses of cells in primary auditory cortex. Cereb. Cortex 21, 2620-2638. doi: 10.1093/cercor/bhr048
6. Barbour, D. L., and Callaway, E. M. (2008). Excitatory local connections of superficial neurons in rat auditory cortex. J. Neurosci. 28, 11174-11185. doi: 10.1523/JNEUROSCI.2093-08.2008
7. Barth, A. L., and Poulet, J. F. (2012). Experimental evidence for sparse firing in the neocortex. Trends Neurosci. 35, 345-355. doi: 10.1016/j.tins.2012.03.008
8. Bastos, A. M., Usrey, W. M., Adams, R. A., Mangun, G. R., Fries, P., and Friston, K. J. (2012). Canonical microcircuits for predictive coding. Neuron 76, 695-711. doi: 10.1016/j.neuron.2012.10.038
9. Bathellier, B., Ushakova, L., and Rumpel, S. (2012). Discrete neocortical dynamics predict behavioral categorization of sounds. Neuron 76, 435-449. doi: 10.1016/j.neuron.2012.07.008
10. Beggs, J. M., and Plenz, D. (2003). Neuronal avalanches in neocortical circuits. J. Neurosci. 23, 11167-11177.
11. Beierlein, M., Gibson, J. R., and Connors, B. W. (2003). Two dynamically distinct inhibitory networks in layer 4 of the neocortex. J. Neurophysiol. 90, 2987-3000. doi: 10.1152/jn.00283.2003
12. Beltramo, R., D’urso, G., Dal Maschio, M., Farisello, P., Bovetti, S., Clovis, Y., et al. (2013). Layer-specific excitatory circuits differentially control recurrent network dynamics in the neocortex. Nat. Neurosci. 16, 227-234. doi: 10.1038/ nn.3306
13. Benshalom, G., and White, E. L. (1986). Quantification of thalamocortical synapses with spiny stellate neurons in layer IV of mouse somatosensory cortex. J. Comp. Neurol. 253, 303-314. doi: 10.1002/cne.902530303
14. Berry, M. S., and Pentreath, V. W. (1976). Criteria for distinguishing between monosynaptic and polysynaptic transmission. Brain Res. 105, 1-20. doi: 10.1016/0006-8993(76)90919-7
15. Binzegger, T., Douglas, R. J., and Martin, K. A. (2004). A quantitative map of the circuit of cat primary visual cortex. J. Neurosci. 24, 8441-8453. doi: 10.1523/ JNEUROSCI.1400-04.2004
16. Budd, J. M. (1998). Extrastriate feedback to primary visual cortex in primates: a quantitative analysis of connectivity. Proc. Biol. Sci. 265, 1037-1044. doi: 10.1098/rspb.1998.0396
17. Buffalo, E. A., Fries, P., Landman, R., Buschman, T. J., and Desimone, R. (2011). Laminar differences in gamma and alpha coherence in the ventral stream. Proc. Natl. Acad. Sci. U.S.A. 108, 11262-11267. doi: 10.1073/pnas.1011284108
18. Bullier, J., and Henry, G. H. (1979). Laminar distribution of first-order neurons and afferent terminals in cat striate cortex. J. Neurophysiol. 42, 1271.
19. Bureau, I., Saint Paul, F., and Svoboda, K. (2006). Interdigitated paralemniscal and lemniscal pathways in the mouse barrel cortex. PLoS Biol. 4:e382. doi: 10.1371/journal.pbio.0040382
20. Chang, E. F., Bao, S., Imaizumi, K., Schreiner, C. E., and Merzenich, M. M. (2005). Development of spectral and temporal response selectivity in the auditory cortex. Proc. Natl. Acad. Sci. U.S.A. 102, 16460-16465. doi: 10.1073/pnas.0508239102
21. Chang, E. F., and Merzenich, M. M. (2003). Environmental noise retards auditory cortical development. Science 300, 498-502. doi: 10.1126/science.1082163
22. Chauvette, S., Volgushev, M., and Timofeev, I. (2010). Origin of active states in local neocortical networks during slow sleep oscillation. Cereb. Cortex 20, 2660-2674. doi: 10.1093/cercor/bhq009
23. Christianson, G. B., Sahani, M., and Linden, J. F. (2011). Depth-dependent temporal response properties in core auditory cortex. J. Neurosci. 31, 12837-12848. doi: 10.1523/JNEUROSCI.2863-11.2011
24. Constantinople, C. M., and Bruno, R. M. (2011). Effects and mechanisms of wakefulness on local cortical networks. Neuron 69, 1061-1068. doi: 10.1016/j.neuron. 2011.02.040
25. Constantinople, C. M., and Bruno, R. M. (2013). Deep cortical layers are activated directly by thalamus. Science 340, 1591-1594. doi: 10.1126/science.1236425
26. Creutzfeldt, O. D. (1977). Generality of the functional structure of the neocortex. Naturwissenschaften 64, 507-517. doi: 10.1007/BF00483547
27. Cruikshank, S. J., Lewis, T. J., and Connors, B. W. (2007). Synaptic basis for intense thalamocortical activation of feedforward inhibitory cells in neocortex. Nat. Neurosci. 10, 462-468. doi: 10.1038/nn1861
28. Cruikshank, S. J., Rose, H. J., and Metherate, R. (2002). Auditory thalamocortical synaptic transmission in vitro. J. Neurophysiol. 87, 361-384.
29. Cruikshank, S. J., Urabe, H., Nurmikko, A. V., and Connors, B. W. (2010). Pathway-specific feedforward circuits between thalamus and neocortex revealed by selective optical stimulation of axons. Neuron 65, 230-245. doi: 10.1016/j.neuron.2009.12.025
30. Cunningham, M. O., Pervouchine, D. D., Racca, C., Kopell, N. J., Davies, C. H., Jones, R. S., et al. (2006). Neuronal metabolism governs cortical network response state. Proc. Natl. Acad. Sci. U.S.A. 103, 5597-5601. doi: 10.1073/pnas. 0600604103
31. Curto, C., Sakata, S., Marguet, S., Itskov, V., and Harris, K. D. (2009). A simple model of cortical dynamics explains variability and state dependence of sensory responses in urethane-anesthetized auditory cortex. J. Neurosci. 29, 10600-10612. doi: 10.1523/JNEUROSCI.2053-09.2009
32. Davis, M. H., and Johnsrude, I. S. (2007). Hearing speech sounds: top-down influences on the interface between audition and speech perception. Hear. Res. 229, 132-147. doi: 10.1016/j.heares.2007.01.014
33. De Kock, C. P., Bruno, R. M., Spors, H., and Sakmann, B. (2007). Layerand celltype-specific suprathreshold stimulus representation in rat primary somatosensory cortex. J. Physiol. 581, 139-154. doi: 10.1113/jphysiol.2006.124321
34. Destexhe, A., Hughes, S. W., Rudolph, M., and Crunelli, V. (2007). Are corticothalamic “up” states fragments of wakefulness? Trends Neurosci. 30, 334-342. doi: 10.1016/j.tins.2007.04.006
35. Destexhe, A., Rudolph, M., and Pare, D. (2003). The high-conductance state of neocortical neurons in vivo. Nat. Rev. Neurosci. 4, 739-751. doi: 10.1038/nrn1198
36. Deweese, M. R., and Zador, A. M. (2006). Non-gaussian membrane potential dynamics imply sparse, synchronous activity in auditory cortex. J. Neurosci. 26, 12206-12218. doi: 10.1523/JNEUROSCI.2813-06.2006
37. Douglas, R. J., and Martin, K. A. (1991). A functional microcircuit for cat visual cortex. J. Physiol. 440, 735-769.
38. Douglas, R. J., and Martin, K. A. (2004). Neuronal circuits of the neocortex. Annu. Rev. Neurosci. 27, 419-451. doi: 10.1146/annurev.neuro.27.070203.144152
39. Douglas, R. J., Martin, K. A. C., and Whitteridge, D. (1989). A canonical microcircuit for neocortex. Neural Comput. 1, 480-488. doi: 10.1162/neco.1989.1.4.480
40. Dräger, U. C., and Hubel, D. H. (1978). Studies of visual function and its decay in mice with hereditary retinal degeneration. J. Comp. Neurol. 180, 85-114. doi: 10.1002/cne.901800107
41. Fanselow, E. E., Richardson, K. A., and Connors, B. W. (2008). Selective, statedependent activation of somatostatin-expressing inhibitory interneurons in mouse neocortex. J. Neurophysiol. 100, 2640-2652. doi: 10.1152/jn.90691.2008
42. Feldmeyer, D., Lübke, J., Silver, R. A., and Sakmann, B. (2002). 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, 803-822. doi: 10.1113/jphysiol.2001.012959
43. Freeman, J., and Nicholson, C. (1975). Experimental optimization of current source-density technique for anuran cerebellum. J. Neurophysiol. 38, 369-382.
44. Frick, A., Feldmeyer, D., and Sakmann, B. (2007). Postnatal development of synaptic transmission in local networks of L5A pyramidal neurons in rat somatosensory cortex. J.Physiol 585, 103-116. doi: 10.1113/jphysiol.2007.141788
45. Fritz, J. B., Elhilali, M., and Shamma, S. A. (2007). Adaptive changes in cortical receptive fields induced by attention to complex sounds. J. Neurophysiol. 98, 2337-2346. doi: 10.1152/jn.00552.2007
46. Gabernet, L., Jadhav, S. P., Feldman, D. E., Carandini, M., and Scanziani, M. (2005). Somatosensory integration controlled by dynamic thalamocortical feedforward inhibition. Neuron 48, 315-327. doi: 10.1016/j.neuron.2005.09.022
47. Gerstein, G. L., and Kiang, N. Y. S. (1964). Responses of single units in the auditory cortex. Exp. Neurol. 10, 1-18. doi: 10.1016/0014-4886(64)90083-4
48. Gibson, J. R., Beierlein, M., and Connors, B. W. (1999). Two networks of electrically coupled inhibitory neurons in neocortex. Nature 402, 75-79. doi: 10.1038/47035
49. Gil, Z., and Amitai, Y. (1996). Properties of convergent thalamocortical and intracortical synaptic potentials in single neurons of neocortex. J. Neurosci. 16, 6567-6578.
50. Gilbert, C. D. (1983). Microcircuitry of the visual cortex. Annu. Rev. Neurosci. 6, 217-247. doi: 10.1146/annurev.ne.06.030183.001245
51. Gilbert, C. D., and Wiesel, T. N. (1983). Functional organization of the visual cortex. Prog. Brain Res. 58, 209-218. doi: 10.1016/S0079-6123(08)60022-9
52. Gireesh, E. D., and Plenz, D. (2008). Neuronal avalanches organize as nested thetaand beta/gamma-oscillations during development of cortical layer 2/3. Proc. Natl. Acad. Sci. U.S.A. 105, 7576-7581. doi: 10.1073/pnas.0800537105
53. Goard, M., and Dan, Y. (2009). Basal forebrain activation enhances cortical coding of natural scenes. Nat. Neurosci. 12, 1444-1449. doi: 10.1038/nn.2402
54. Goris, R. L., Movshon, J. A., and Simoncelli, E. P. (2014). Partitioning neuronal variability. Nat. Neurosci. 17, 858-865. doi: 10.1038/nn.3711
55. Guillery, R. W., and Sherman, S. M. (2002). Thalamic relay functions and their role in corticocortical communication: generalizations from the visual system. Neuron 33, 163-175. doi: 10.1016/S0896-6273(01)00582-7
56. Harris, K. D., and Thiele, A. (2011). Cortical state and attention. Nat. Rev. Neurosci. 12, 509-523. doi: 10.1038/nrn3084
57. He, B. J., and Raichle, M. E. (2009). The fMRI signal, slow cortical potential and consciousness. Trends Cogn. Sci. 13, 302-309. doi: 10.1016/j.tics.2009.04.004
58. Hefti, B. J., and Smith, P. H. (2003). Distribution and kinetic properties of GABAergic inputs to layer V pyramidal cells in rat auditory cortex. J. Assoc. Res. Otolaryngol. 4, 106-121. doi: 10.1007/s10162-002-3012-z
59. Hirsch, J. A., and Martinez, L. M. (2006). Laminar processing in the visual cortical column. Curr. Opin. Neurobiol. 16, 377-384. doi: 10.1016/j.conb.2006.06.014
60. Hromadka, T., Zador, A. M., and Deweese, M. R. (2013). Up states are rare in awake auditory cortex. J. Neurophysiol. 109, 1989-1995. doi: 10.1152/jn.00600.2012
61. Huang, C. L., and Winer, J. A. (2000). Auditory thalamocortical projections in the cat: laminar and areal patterns of input. J. Comp. Neurol. 427, 302-331. doi: 10.1002/1096-9861(20001113)427:2<302::AID-CNE10>3.0.CO;2-J
62. Hubel, D. H., and Wiesel, T. N. (1963). Shape and arrangement of columns in cat’s striate cortex. J. Physiol. 165, 559-568.
63. Huggenberger, S., Vater, M., and Deisz, R. A. (2009). Interlaminar differences of intrinsic properties of pyramidal neurons in the auditory cortex of mice. Cereb. Cortex 19, 1008-1018. doi: 10.1093/cercor/bhn143
64. Johnson, K. R., Erway, L. C., Cook, S. A., Willott, J. F., and Zheng, Q. Y. (1997). A major gene affecting age-related hearing loss in C57BL/6J mice. Hear. Res. 114, 83-92. doi: 10.1016/S0378-5955(97)00155-X
65. Kaas, J. H., and Collins, C. E. (2001). The organization of sensory cortex. Curr. Opin. Neurobiol. 11, 498-504. doi: 10.1016/S0959-4388(00)00240-3
66. Kampa, B. M., Letzkus, J. J., and Stuart, G. J. (2006). Cortical feed-forward networks for binding different streams of sensory information. Nat. Neurosci. 9, 1472-1473. doi: 10.1038/nn1798
67. Kawaguchi, Y. (1993). Groupings of nonpyramidal and pyramidal cells with specific physiological and morphological characteristics in rat frontal cortex. J. Neurophysiol. 69, 416-431.
68. Kawaguchi, Y., and Kubota, Y. (1993). Correlation of physiological subgroupings of nonpyramidal cells with parvalbumin and calbinding immunoreactive neurons in layer V of rat frontal cortex. J. Neurophysiol. 70, 387-396.
69. Kawaguchi, Y., and Kubota, Y. (1996). Physiological and morphological identification of somatostatinor vasoactive intestinal polypeptide-containing cells among GABAergic cell subtypes in rat frontal cortex. J. Neurosci. 16, 2701-2715.
70. Kawaguchi, Y., and Kubota, Y. (1997). GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb. Cortex 7, 476-486. doi: 10.1093/cercor/7.6.476
71. Kawaguchi, Y., and Kubota, Y. (1998). Neurochemical features and synaptic connections of large physiologically-identified GABAergic cells in the rat frontal cortex. Neuroscience 85, 677-701. doi: 10.1016/S0306-4522(97)00685-4
72. Kisley, M. A., and Gerstein, G. L. (1999). Trial-to-trial variability and statedependent modulation of auditoryevoked responses in cortex. J. Neurosci. 19, 10451-10460.
73. Lakatos, P., Shah, A. S., Knuth, K. H., Ulbert, I., Karmos, G., and Schroeder, C. E. (2005). An oscillatory hierarchy controlling neuronal excitability and stimulus processing in the auditory cortex. J. Neurophysiol. 94, 1904-1911. doi: 10.1152/jn.00263.2005
74. Lee, C. C., and Sherman, S. M. (2008). synaptic properties of thalamic and intracortical inputs to Layer 4 of the Firstand Higher-order cortical areas in the auditory and somatosensory systems. J. Neurophysiol. 100, 317-326. doi: 10.1152/jn.90391.2008
75. Lee, S. H., Rosenmund, C., Schwaller, B., and Neher, E. (2000). Differences in Ca2+ buffering properties between excitatory and inhibitory hippocampal neurons from the rat. J. Physiol. 525, 405-418. doi: 10.1111/j.1469-7793.2000.t01-300405.x
76. Li, C. Y., Poo, M. M., and Dan, Y. (2009). Burst spiking of a single cortical neuron modifies global brain state. Science 324, 643-646. doi: 10.1126/science.1169957
77. Lubke, J., and Feldmeyer, D. (2007). Excitatory signal flow and connectivity in a cortical column: focus on barrel cortex. Brain Struct. Funct. 212, 3-17. doi:10.1007/s00429-007-0144-2
78. Lübke, J., Roth, A., Feldmeyer, D., and Sakmann, B. (2003). Morphometric analysis of the columnar innervation domain of neurons connecting layer 4 and layer 2/3 of juvenile rat barrel cortex. Cereb. Cortex 13, 1051-1063. doi: 10.1093/cercor/13.10.1051
79. Luczak, A., Bartho, P., and Harris, K. D. (2013). Gating of sensory input by spontaneous cortical activity. J. Neurosci. 33, 1684-1695. doi: 10.1523/JNEUROSCI.2928-12.2013
80. Luczak, A., Bartho, P., Marguet, S. L., Buzsaki, G., and Harris, K. D. (2007). Sequential structure of neocortical spontaneous activity in vivo. Proc. Natl. Acad. Sci. U.S.A. 104, 347-352. doi: 10.1073/pnas.0605643104
81. Ma, Y., Hu, H., Berrebi, A. S., Mathers, P. H., and Agmon, A. (2006). Distinct subtypes of somatostatin-containing neocortical interneurons revealed in transgenic mice. J. Neurosci. 26, 5069-5082. doi: 10.1523/JNEUROSCI.0661-06.2006
82. MacGregor, D. G., Chesler, M., and Rice, M. E. (2001). HEPES prevents edema in rat brain slices. Neurosci. Lett. 303, 141-144. doi: 10.1016/S03043940(01)01690-1
83. MacLean, J. N., Watson, B. O., Aaron, G. B., and Yuste, R. (2005). Internal dynamics determine the cortical response to thalamic stimulation. Neuron 48, 811-823. doi: 10.1016/j.neuron.2005.09.035
84. Maier, A., Adams, G. K., Aura, C., and Leopold, D. A. (2010). Distinct superficial and deep laminar domains of activity in the visual cortex during rest and stimulation. Front. Syst. Neurosci. 4:31. doi: 10.3389/fnsys.2010.00031
85. Manns, I. D., Sakmann, B., and Brecht, M. (2004). Suband suprathreshold receptive field properties of pyramidal neurones in layers 5A and 5B of rat somatosensory barrel cortex. J. Physiol. 556, 601-622. doi: 10.1113/jphysiol.2003.053132
86. Markram, H., Toledo-Rodriguez, M., Wang, Y., Gupta, A., Silberberg, G., and Wu, C. Z. (2004). Interneurons of the neocortical inhibitory system. Nat. Rev. Neurosci. 5, 793-807. doi: 10.1038/nrn1519
87. Maunsell, J. H., and Gibson, J. R. (1992). Visual response latencies in striate cortex of the macaque monkey. J. Neurophysiol. 68, 1332-1344.
88. McCormick, D. A., Shu, Y., Hasenstaub, A., Sanchez-Vives, M., Badoual, M., and Bal, T. (2003). Persistent cortical activity: mechanisms of generation and effects on neuronal excitability. Cereb. Cortex 13, 1219-1231. doi: 10.1093/cercor/bhg104
89. Metherate, R., and Aramakis, V. B. (1999). Intrinsic electrophysiology of neurons in thalamorecipient layers of developing rat auditory cortex. Brain Res. Dev. Brain Res. 115, 131-144. doi: 10.1016/S0165-3806(99)00058-9
90. Metherate, R., Cox, C. L., and Ashe, J. H. (1992). Cellular bases of neocortical activation: modulation of neural oscillations by the nucleus basalis and endogenous acetylcholine. J. Neurosci. 12, 4701-4711.
91. Metherate, R., and Cruikshank, S. J. (1999). Thalamocortical inputs trigger a propagating envelope of gamma-band activity in auditory cortex in vitro. Exp. Brain Res. 126, 160-174. doi: 10.1007/s002210050726
92. Mitani, A., and Shimokouchi, M. (1985). Neuronal connections in the primary auditory cortex: an electrophysiological study in the cat. J. Comp. Neurol. 235, 417-429. doi: 10.1002/cne.902350402
93. Mitzdorf, U. (1985). Current source-density method and application in cat cerebral cortex: investigation of evoked potentials and EEG phenomena. Physiol. Rev. 65, 37-100.
94. Mountcastle, V. B. (1997). The columnar organization of the neocortex. Brain 120(pt 4), 701-722. doi: 10.1093/brain/120.4.701
95. Mountcastle, V. B., Davies, P. W., and Berman, A. L. (1957). Response properties of neurons of cat’s somatic sensory cortex to peripheral stimuli. J. Neurophysiol. 20, 374-407.
96. Oswald, A. M., and Reyes, A. D. (2008). Maturation of intrinsic and synaptic properties of layer 2/3 pyramidal neurons in mouse auditory cortex. J. Neurophysiol. 99, 2998-3008. doi: 10.1152/jn.01160.2007
97. Oswald, A. M., and Reyes, A. D. (2011). Development of inhibitory timescales in auditory cortex. Cereb. Cortex 21, 1351-1361. doi: 10.1093/cercor/bhq214
98. Pasley, B. N., Allen, E. A., and Freeman, R. D. (2009). State-dependent variability of neuronal responses to transcranial magnetic stimulation of the visual cortex. Neuron 62, 291-303. doi: 10.1016/j.neuron.2009.03.012
99. Paxinos, G., and Franklin, K. B. J. (2003). The Mouse Brain in Stereotaxic Coordinates. San Diego, CA: Academic Press.
100. Petermann, T., Thiagarajan, T. C., Lebedev, M. A., Nicolelis, M. A., Chialvo, D. R., and Plenz, D. (2009). Spontaneous cortical activity in awake monkeys composed of neuronal avalanches. Proc. Natl. Acad. Sci. U.S.A. 106, 15921-15926. doi: 10.1073/pnas.0904089106
101. Peters, A., and Payne, B. R. (1993). Numerical relationships between geniculocortical afferents and pyramidal cell modules in cat primary visual cortex. Cereb. Cortex 3, 69-78. doi: 10.1093/cercor/3.1.69
102. Petersen, C. C. H., Hahn, T. T. G., Mehta, M., Grinvald, A., and Sakmann, B. (2003). Interaction of sensory responses with spontaneous depolarization in layer 2/3 barrel cortex. Proc. Natl. Acad. Sci. U.S.A. 100, 13638-13643. doi: 10.1073/pnas.2235811100
103. Pettersen, K. H., Devor, A., Ulbert, I., Dale, A. M., and Einevoll, G. T. (2006). Current-source density estimation based on inversion of electrostatic forward solution: effects of finite extent of neuronal activity and conductivity discontinuities. J. Neurosci. Methods 154, 116-133. doi: 10.1016/j.jneumeth.2005.12.005
104. Reed, J. L., and Kaas, J. H. (2010). Statistical analysis of large-scale neuronal recording data. Neural Netw. 23, 673-684. doi: 10.1016/j.neunet.2010.04.005
105. Rigas, P., and Castro-Alamancos, M. A. (2007). Thalamocortical Up states: differential effects of intrinsic and extrinsic cortical inputs on persistent activity. J. Neurosci. 27, 4261-4272. doi: 10.1523/JNEUROSCI.0003-07.2007
106. Rigas, P., and Castro-Alamancos, M. A. (2009). Impact of persistent cortical activity (up states) on intracortical and thalamocortical synaptic inputs. J. Neurophysiol. 102, 119-131. doi: 10.1152/jn.00126.2009
107. Romand, S., Wang, Y., Toledo-Rodriguez, M., and Markram, H. (2011). Morphological development of thick-tufted layer v pyramidal cells in the rat somatosensory cortex. Front. Neuroanat. 5:5. doi: 10.3389/fnana.2011.00005
108. Rose, H. J., and Metherate, R. (2005). Auditory thalamocortical transmission is reliable and temporally precise. J. Neurophysiol. 94, 2019-2030. doi: 10.1152/jn.00860.2004
109. Sakata, S., and Harris, K. D. (2009). Laminar structure of spontaneous and sensory-evoked population activity in auditory cortex. Neuron 64, 404-418. doi: 10.1016/j.neuron.2009.09.020
110. Sakata, S., and Harris, K. D. (2012). Laminar-dependent effects of cortical state on auditory cortical spontaneous activity. Front. Neural Circuits 6:109. doi: 10.3389/fncir.2012.00109
111. Sanchez-Vives, M. V., and McCormick, D. A. (2000). Cellular and network mechanisms of rhythmic recurrent activity in neocortex. Nat. Neurosci. 3, 1027-1034. doi: 10.1038/79848
112. Schiff, M. L., and Reyes, A. D. (2012). Characterization of thalamocortical responses of regular-spiking and fast-spiking neurons of the mouse auditory cortex in vitro and in silico. J. Neurophysiol. 107, 1476-1488. doi: 10.1152/jn.00208.2011
113. Schoonover, C. E., Tapia, J.-C., Schilling, V. C., Wimmer, V., Blazeski, R., Zhang, W., et al. (2014). Comparative strength and dendritic organization of thalamocortical and corticocortical synapses onto excitatory Layer 4 neurons. J. Neurosci. 34, 6746-6758. doi: 10.1523/JNEUROSCI.0305-14.2014
114. Shen, J. X., Xu, Z. M., and Yao, Y. D. (1999). Evidence for columnar organization in the auditory cortex of the mouse. Hear. Res. 137, 174-177. doi: 10.1016/S03785955(99)00149-5
115. Shu, Y. S., Hasenstaub, A., Badoual, M., Bal, T., and McCormick, D. A. (2003). Barrages of synaptic activity control the gain and sensitivity of cortical neurons. J. Neurosci. 23, 10388-10401.
116. Singer, W. (2013). Cortical dynamics revisited. Trends Cogn. Sci. 17, 616-626. doi: 10.1016/j.tics.2013.09.006
117. Smith, P. H., and Populin, L. C. (2001). Fundamental differences between the thalamocortical recipient layers of the cat auditory and visual cortices. J. Comp. Neurol. 436, 508-519. doi: 10.1002/cne.1084
118. Smith, P. H., Uhlrich, D. J., Manning, K. A., and Banks, M. I. (2012). Thalamocortical projections to rat auditory cortex from the ventral and dorsal divisions of the medial geniculate nucleus. J. Comp. Neurol. 520, 34-51. doi: 10.1002/cne.22682
119. Steriade, M., McCormick, D. A., and Sejnowski, T. J. (1993). Thalamocortical oscillations in the sleeping and aroused brain. Science 262, 679-685. doi: 10.1126/science.8235588
120. Steriade, M., Timofeev, I., and Grenier, F. (2001). Natural waking and sleep states: a view from inside neocortical neurons. J. Neurophysiol. 85, 1969-1985.
121. Stroh, A., Adelsberger, H., Groh, A., Ruhlmann, C., Fischer, S., Schierloh, A., et al. (2013). Making waves: initiation and propagation of corticothalamic Ca2+ waves in vivo. Neuron 77, 1136-1150. doi: 10.1016/j.neuron.2013. 01.031
122. Sugimoto, S., Sakurada, M., Horikawa, J., and Taniguchi, I. (1997). The columnar and layer-specific response properties of neurons in the primary auditory cortex of Mongolian gerbils. Hear. Res. 112, 175-185. doi: 10.1016/S03785955(97)00119-6
123. Sun, Y. J., Kim, Y. J., Ibrahim, L. A., Tao, H. W., and Zhang, L. I. (2013). Synaptic mechanisms underlying functional dichotomy between intrinsic-bursting and regular-spiking neurons in auditory cortical layer 5. J. Neurosci. 33, 5326-5339. doi: 10.1523/JNEUROSCI.4810-12.2013
124. Tan, A. Y., Chen, Y., Scholl, B., Seidemann, E., and Priebe, N. J. (2014). Sensory stimulation shifts visual cortex from synchronous to asynchronous states. Nature 509, 226-229. doi: 10.1038/nature13159
125. Tan, Z., Hu, H., Huang, Z. J., and Agmon, A. (2008). Robust but delayed thalamocortical activation of dendritic-targeting inhibitory interneurons. Proc. Natl. Acad. Sci. U.S.A. 105, 2187-2192. doi: 10.1073/pnas.0710628105
126. Theyel, B. B., Llano, D. A., and Sherman, S. M. (2010). The corticothalamocortical circuit drives higher-order cortex in the mouse. Nat. Neurosci. 13, 84-88. doi: 10.1038/nn.2449
127. Thomson, A., and Bannister, A. (1998). Postsynaptic pyramidal target selection by descending layer III pyramidal axons: dual intracellular recordings and biocytin filling in slices of rat neocortex. Neuroscience 84, 669-683. doi: 10.1016/S0306-4522(97)00557-5
128. Thomson, A. M., and Bannister, A. P. (2003). Interlaminar connections in the neocortex. Cereb. Cortex 13, 5-14. doi: 10.1093/cercor/13.1.5
129. Thomson, A. M., and Lamy, C. (2007). Functional maps of neocortical local circuitry. Front. Neurosci. 1, 19-42. doi: 10.3389/neuro.01.1.1.002.2007
130. Thomson, A. M., West, D. C., Wang, Y., and Bannister, A. P. (2002). 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. doi: 10.1093/cercor/ 12.9.936
131. Verbny, Y. I., Erdelyi, F., Szabo, G., and Banks, M. I. (2006). Properties of a population of GABAergic cells in murine auditory cortex weakly excited by thalamic stimulation. J. Neurophysiol. 96, 3194-3208. doi: 10.1152/jn.004 84.2006
132. Wang, Y., Toledo-Rodriguez, M., Gupta, A., Wu, C., Silberberg, G., Luo, J., et al. (2004). Anatomical, physiological and molecular properties of Martinotti cells in the somatosensory cortex of the juvenile rat. J. Physiol. 561, 65-90. doi: 10.1113/jphysiol.2004.073353
133. Warren, R. M. (1970). Perceptual restoration of missing speech sounds. Science 167, 392-393. doi: 10.1126/science.167.3917.392
134. Watson, B. O., Maclean, J. N., and Yuste, R. (2008). UP states protect ongoing cortical activity from thalamic inputs. PLoS ONE 3:e3971. doi: 10.1371/journal.pone.0003971
135. Wester, J. C., and Contreras, D. (2012). Columnar interactions determine horizontal propagation of recurrent network activity in neocortex. J. Neurosci. 32, 5454-5471. doi: 10.1523/JNEUROSCI.5006-11.2012
136. White, B., Abbott, L. F., and Fiser, J. (2012). Suppression of cortical neural variability is stimulusand state-dependent. J. Neurophysiol. 108, 2383-2392. doi: 10.1152/jn.00723.2011