How do neurons work together? Lessons from auditory cortex

Hearing Research

Volumn 271, Issue 1-2, 2011, Pages 37-53

  Harris, Kenneth D ^a,b,c   Bartho, Peter ^a,d   Chadderton, Paul ^a,e   Curto, Carina ^a,f   de la Rocha, Jaime ^a   Hollender, Liad ^a   Itskov, Vladimir ^a,f,h   Luczak, Artur ^a,g   Marguet, Stephan L ^a   Renart, Alfonso ^a   Sakata, Shuzo ^a,h  

^a RUTGERS UNIVERSITY   (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

^d INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^e UNIVERSITY COLLEGE LONDON   (United Kingdom)

^f UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^g UNIVERSITY OF LETHBRIDGE   (Canada)

^h UNIVERSITY OF STRATHCLYDE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; AUDITORY CORTEX; AUDITORY STIMULATION; BRAIN NERVE CELL; CELL POPULATION; CONTROLLED STUDY; ELECTRIC POTENTIAL; INTERNEURON; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; RECORDING; SENSORY STIMULATION; SPIKE; STIMULUS RESPONSE;

ACOUSTIC STIMULATION; ANESTHESIA; ANIMALS; AUDITORY CORTEX; BEHAVIOR, ANIMAL; EVOKED POTENTIALS, AUDITORY; MEMBRANE POTENTIALS; MODELS, NEUROLOGICAL; NEURONS; RATS;

EID: 78651096590     PISSN: 03785955     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.heares.2010.06.006     Document Type: Article

References (124)

1. Arlotta P., Molyneaux B.J., Chen J., Inoue J., Kominami R., Macklis J.D. Neuronal subtype-specific genes that control corticospinal motor neuron development in vivo. Neuron 2005, 45:207-221.
2. Atencio C.A., Schreiner C.E. Laminar diversity of dynamic sound processing in cat primary auditory cortex. J. Neurophysiol. 2010, 103:192-205.
3. Bandyopadhyay S., Shamma S.A., Kanold P.O. Dichotomy of functional organization in the mouse auditory cortex. Nat. Neurosci. 2010, 13:361-368.
4. Barbour D.L., Callaway E.M. Excitatory local connections of superficial neurons in rat auditory cortex. J. Neurosci. 2008, 28:11174-11185.
5. Barlow H.B. Single units and sensation: a neuron doctrine for perceptual psychology?. Perception 1972, 1:371-394.
6. Bartho P., Curto C., Luczak A., Marguet S.L., Harris K.D. Population coding of tone stimuli in auditory cortex: dynamic rate vector analysis. Eur. J. Neurosci. 2009, 30:1767-1778.
7. Bartho P., Hirase H., Monconduit L., Zugaro M., Harris K.D., Buzsaki G. Characterization of neocortical principal cells and interneurons by network interactions and extracellular features. J. Neurophysiol. 2004, 92:600-608.
8. Berke J.D., Okatan M., Skurski J., Eichenbaum H.B. Oscillatory entrainment of striatal neurons in freely moving rats. Neuron 2004, 43:883-896.
9. Brecht M., Roth A., Sakmann B. Dynamic receptive fields of reconstructed pyramidal cells in layers 3 and 2 of rat somatosensory barrel cortex. J. Physiol. 2003, 553:243-265.
10. Brecht M. Barrel cortex and whisker-mediated behaviors. Curr. Opin. Neurobiol. 2007, 17:408-416.
11. Brincat S.L., Connor C.E. Dynamic shape synthesis in posterior inferotemporal cortex. Neuron 2006, 49:17-24.
12. Brosch M., Schreiner C.E. Correlations between neural discharges are related to receptive field properties in cat primary auditory cortex. Eur. J. Neurosci. 1999, 11:3517-3530.
13. Brosch M., Selezneva E., Scheich H. Nonauditory events of a behavioral procedure activate auditory cortex of highly trained monkeys. J. Neurosci. 2005, 25:6797-6806.
14. Bureau I., von Saint Paul F., Svoboda K. Interdigitated paralemniscal and lemniscal pathways in the mouse barrel cortex. PLoS Biol. 2006, 4:e382.
15. Buzsaki G. Two-stage model of memory trace formation: a role for 'noisy' brain states. Neuroscience 1989, 31:551-570.
16. Buzsaki G., Bickford R.G., Ponomareff G., Thal L.J., Mandel R., Gage F.H. Nucleus basalis and thalamic control of neocortical activity in the freely moving rat. J. Neurosci. 1988, 8:4007-4026.
17. Castro-Alamancos M.A. Absence of rapid sensory adaptation in neocortex during information processing states. Neuron 2004, 41:455-464.
18. Castro-Alamancos M.A. Dynamics of sensory thalamocortical synaptic networks during information processing states. Prog. Neurobiol. 2004, 74:213-247.
19. Chauvette S., Volgushev M., Timofeev I. Origin of active states in local neocortical networks during slow sleep oscillation. Cereb. Cortex 2010.
20. Clement E.A., Richard A., Thwaites M., Ailon J., Peters S., Dickson C.T. Cyclic and sleep-like spontaneous alternations of brain state under urethane anaesthesia. PLoS ONE 2008, 3:e2004.
21. Cohen M.R., Maunsell J.H. Attention improves performance primarily by reducing interneuronal correlations. Nat. Neurosci. 2009, 12:1594-1600.
22. Csicsvari J., Henze D.A., Jamieson B., Harris K.D., Sirota A., Bartho P., Wise K.D., Buzsaki G. Massively parallel recording of unit and local field potentials with silicon-based electrodes. J. Neurophysiol. 2003, 90:1314-1323.
23. Curto C., Sakata S., Marguet S., Itskov V., Harris K.D. A simple model of cortical dynamics explains variability and state dependence of sensory responses in urethane-anesthetized auditory cortex. J. Neurosci. 2009, 29:10600-10612.
24. deCharms R.C., Merzenich M.M. Primary cortical representation of sounds by the coordination of action-potential timing. Nature 1996, 381:610-613.
25. de Kock C.P., Bruno R.M., Spors H., Sakmann B. Layer-and cell-type-specific suprathreshold stimulus representation in rat primary somatosensory cortex. J. Physiol. 2007, 581:139-154.
26. DeWeese M.R., Wehr M., Zador A.M. Binary spiking in auditory cortex. J. Neurosci. 2003, 23:7940-7949.
27. Edeline J.M. The thalamo-cortical auditory receptive fields: regulation by the states of vigilance, learning and the neuromodulatory systems. Exp. Brain Res. 2003, 153:554-572.
28. Eggermont J.J. Properties of correlated neural activity clusters in cat auditory cortex resemble those of neural assemblies. J. Neurophysiol. 2006, 96:746-764.
29. Einevoll G.T., Pettersen K.H., Devor A., Ulbert I., Halgren E., Dale A.M. Laminar population analysis: estimating firing rates and evoked synaptic activity from multielectrode recordings in rat barrel cortex. J. Neurophysiol. 2007, 97:2174-2190.
30. 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. 2006, 575:583-602.
31. Felleman D.J., Van Essen D.C. Distributed hierarchical processing in the primate cerebral cortex. Cereb. Cortex 1991, 1:1-47.
32. Felsen G., Mainen Z.F. Neural substrates of sensory-guided locomotor decisions in the rat superior colliculus. Neuron 2008, 60:137-148.
33. Fitzhugh R. Mathematical models of threshold phenomena in the nerve membrane. Bull. Math. Biophysics. 1995, 17:257-278.
34. Fries P., Reynolds J.H., Rorie A.E., Desimone R. Modulation of oscillatory neuronal synchronization by selective visual attention. Science 2001, 291:1560-1563.
35. Gerstein G.L., Perkel D.H., Dayhoff J.E. Cooperative firing activity in simultaneously recorded populations of neurons: detection and measurement. J. Neurosci. 1985, 5:881-889.
36. Goard M., Dan Y. Basal forebrain activation enhances cortical coding of natural scenes. Nat. Neurosci. 2009, 12:1444-1449.
37. Gray C.M., Maldonado P.E., Wilson M., McNaughton B. Tetrodes markedly improve the reliability and yield of multiple single-unit isolation from multi-unit recordings in cat striate cortex. J. Neurosci. Methods 1995, 63:43-54.
38. Haider B., Duque A., Hasenstaub A.R., Yu Y., McCormick D.A. Enhancement of visual responsiveness by spontaneous local network activity in vivo. J. Neurophysiol. 2007, 97:4186-4202.
39. Harris K.D. Neural signatures of cell assembly organization. Nat. Rev. Neurosci. 2005, 6:399-407.
40. Harris K.D., Henze D.A., Csicsvari J., Hirase H., Buzsaki G. Accuracy of tetrode spike separation as determined by simultaneous intracellular and extracellular measurements. J. Neurophysiol. 2000, 84:401-414.
41. Hasenstaub A., Sachdev R.N., McCormick D.A. State changes rapidly modulate cortical neuronal responsiveness. J. Neurosci. 2007, 27:9607-9622.
42. Hefti B.J., Smith P.H. Anatomy, physiology, and synaptic responses of rat layer V auditory cortical cells and effects of intracellular GABA(A) blockade. J. Neurophysiol. 2000, 83:2626-2638.
43. Hefti B.J., Smith P.H. Distribution and kinetic properties of GABAergic inputs to layer V pyramidal cells in rat auditory cortex. J. Assoc. Res. Otolaryngol. 2003, 4:106-121.
44. Heil P. First-spike latency of auditory neurons revisited. Curr. Opin. Neurobiol. 2004, 14:461-467.
45. Hoffman K.L., McNaughton B.L. Coordinated reactivation of distributed memory traces in primate neocortex. Science 2002, 297:2070-2073.
46. Hoffman K.L., Battaglia F.P., Harris K., MacLean J.N., Marshall L., Mehta M.R. The upshot of up states in the neocortex: from slow oscillations to memory formation. J. Neurosci. 2007, 27:11838-11841.
47. Holmgren C., Harkany T., Svennenfors B., Zilberter Y. Pyramidal cell communication within local networks in layer 2/3 of rat neocortex. J. Physiol. 2003, 551:139-153.
48. Hromadka T., Deweese M.R., Zador A.M. Sparse representation of sounds in the unanesthetized auditory cortex. PLoS Biol. 2008, 6:e16.
49. Jermakowicz W.J., Chen X., Khaytin I., Bonds A.B., Casagrande V.A. Relationship between spontaneous and evoked spike-time correlations in primate visual cortex. J. Neurophysiol. 2009, 101:2279-2289.
50. Jeschke M., Lenz D., Budinger E., Herrmann C.S., Ohl F.W. Gamma oscillations in gerbil auditory cortex during a target-discrimination task reflect matches with short-term memory. Brain Res. 2008, 1220:70-80.
51. John E.R., Bartlett F., Shimokochi M., Kleinman D. Neural readout from memory. J. Neurophysiol. 1973, 36:893-924.
52. Kandel A., Buzsaki G. Cellular-synaptic generation of sleep spindles, spike-and-wave discharges, and evoked thalamocortical responses in the neocortex of the rat. J. Neurosci. 1997, 17:6783-6797.
53. Katzner S., Nauhaus I., Benucci A., Bonin V., Ringach D.L., Carandini M. Local origin of field potentials in visual cortex. Neuron 2009, 61:35-41.
54. Kaur S., Rose H.J., Lazar R., Liang K., Metherate R. Spectral integration in primary auditory cortex: laminar processing of afferent input, in vivo and in vitro. Neuroscience 2005, 134:1033-1045.
55. Kimura A., Donishi T., Sakoda T., Hazama M., Tamai Y. Auditory thalamic nuclei projections to the temporal cortex in the rat. Neuroscience 2003, 117:1003-1016.
56. Kisley M.A., Gerstein G.L. Trial-to-trial variability and state-dependent modulation of auditory-evoked responses in cortex. J. Neurosci. 1999, 19:10451-10460.
57. Kosslyn S.M., Ganis G., Thompson W.L. Neural foundations of imagery. Nat. Rev. Neurosci. 2001, 2:635-642.
58. Kraemer D.J., Macrae C.N., Green A.E., Kelley W.M. Musical imagery: sound of silence activates auditory cortex. Nature 2005, 434:158.
59. Kreiman G., Koch C., Fried I. Imagery neurons in the human brain. Nature 2000, 408:357-361.
60. Kruskal J.B., Wish M. Multidimensional Scaling 1978, Sage Publications, Beverly Hills, Calif.
61. Lakatos P., Chen C.M., O'Connell M.N., Mills A., Schroeder C.E. Neuronal oscillations and multisensory interaction in primary auditory cortex. Neuron 2007, 53:279-292.
62. Laurent G. Olfactory network dynamics and the coding of multidimensional signals. Nat. Rev. Neurosci. 2002, 3:884-895.
63. Linden J.F., Schreiner C.E. Columnar transformations in auditory cortex? A comparison to visual and somatosensory cortices. Cereb. Cortex 2003, 13:83-89.
64. Liu B.H., Wu G.K., Arbuckle R., Tao H.W., Zhang L.I. Defining cortical frequency tuning with recurrent excitatory circuitry. Nat. Neurosci. 2007, 10:1594-1600.
65. Logothetis N.K., Pauls J., Augath M., Trinath T., Oeltermann A. Neurophysiological investigation of the basis of the fMRI signal. Nature 2001, 412:150-157.
66. Luczak A., Bartho P., Harris K.D. Spontaneous events outline the realm of possible sensory responses in neocortical populations. Neuron 2009, 62:413-425.
67. Luczak A., Bartho P., Marguet S.L., Buzsaki G., Harris K.D. Sequential structure of neocortical spontaneous activity in vivo. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:347-352.
68. Marr D. Simple memory: a theory for archicortex. Philos. Trans. R. Soc. Lond., B, Biol. Sci. 1971, 262:23-81.
69. McNaughton B.L., O'Keefe J., Barnes C.A. The stereotrode: a new technique for simultaneous isolation of several single units in the central nervous system from multiple unit records. J. Neurosci. Methods 1983, 8:391-397.
70. Mitchell J.F., Sundberg K.A., Reynolds J.H. Spatial attention decorrelates intrinsic activity fluctuations in macaque area V4. Neuron 2009, 63:879-888.
71. Mitzdorf U. Current source-density method and application in cat cerebral cortex: investigation of evoked potentials and EEG phenomena. Physiol. Rev. 1985, 65:37-100.
72. Moshitch D., Las L., Ulanovsky N., Bar-Yosef O., Nelken I. Responses of neurons in primary auditory cortex (A1) to pure tones in the halothane-anesthetized cat. J. Neurophysiol. 2006, 95:3756-3769.
73. Murakami M., Kashiwadani H., Kirino Y., Mori K. State-dependent sensory gating in olfactory cortex. Neuron 2005, 46:285-296.
74. Ohl F.W., Scheich H., Freeman W.J. Change in pattern of ongoing cortical activity with auditory category learning. Nature 2001, 412:733-736.
75. Oram M.W., Xiao D., Dritschel B., Payne K.R. The temporal resolution of neural codes: does response latency have a unique role?. Philos. Trans. R. Soc. Lond., B, Biol. Sci. 2002, 357:987-1001.
76. Oswald A.M., Reyes A.D. Maturation of intrinsic and synaptic properties of layer 2/3 pyramidal neurons in mouse auditory cortex. J. Neurophysiol. 2008, 99:2998-3008.
77. Oswald A.M., Doiron B., Rinzel J., Reyes A.D. Spatial profile and differential recruitment of GABAB modulate oscillatory activity in auditory cortex. J. Neurosci. 2009, 29:10321-10334.
78. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates 1997, Academit Press, San Diego.
79. Pesaran B., Pezaris J.S., Sahani M., Mitra P.P., Andersen R.A. Temporal structure in neuronal activity during working memory in macaque parietal cortex. Nat. Neurosci. 2002, 5:805-811.
80. Petersen C.C., Hahn T.T., Mehta M., Grinvald A., Sakmann B. Interaction of sensory responses with spontaneous depolarization in layer 2/3 barrel cortex. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:13638-13643.
81. Pinault D. A novel single-cell staining procedure performed in vivo under electrophysiological control: morpho-functional features of juxtacellularly labeled thalamic cells and other central neurons with biocytin or neurobiotin. J. Neurosci. Methods 1996, 65:113-136.
82. Poulet J.F., Petersen C.C. Internal brain state regulates membrane potential synchrony in barrel cortex of behaving mice. Nature 2008, 454:881-885.
83. Ranade S.P., Mainen Z.F. Transient firing of dorsal raphe neurons encodes diverse and specific sensory, motor, and reward events. J. Neurophysiol. 2009, 102:3026-3037.
84. Recce M., O'Keefe J. The tetrode: a new technique for multi-unit extracellular recording. Soc. Neurosci. Abstr. 1989, 15:1250.
85. Renart A., de la Rocha J., Bartho P., Hollender L., Parga N., Reyes A., Harris K.D. The asynchronous state in cortical circuits. Science 2010, 327:587-590.
86. Romanski L.M., LeDoux J.E. Organization of rodent auditory cortex: anterograde transport of PHA-L from MGv to temporal neocortex. Cereb. Cortex 1993, 3:499-514.
87. Rothschild G., Nelken I., Mizrahi A. Functional organization and population dynamics in the mouse primary auditory cortex. Nat. Neurosci. 2010, 13:353-360.
88. Rouiller E.M., Simm G.M., Villa A.E., de Ribaupierre Y., de Ribaupierre F. Auditory corticocortical interconnections in the cat: evidence for parallel and hierarchical arrangement of the auditory cortical areas. Exp. Brain Res. 1991, 86:483-505.
89. Sakata S., Harris K.D. Laminar structure of spontaneous and sensory-evoked population activity in auditory cortex. Neuron 2009, 64:404-418.
90. Sally S.L., Kelly J.B. Organization of auditory cortex in the albino rat: sound frequency. J. Neurophysiol. 1988, 59:1627-1638.
91. Sanchez-Vives M.V., McCormick D.A. Cellular and network mechanisms of rhythmic recurrent activity in neocortex. Nat. Neurosci. 2000, 3:1027-1034.
92. Scheich H., Brechmann A., Brosch M., Budinger E., Ohl F.W. The cognitive auditory cortex: task-specificity of stimulus representations. Hear. Res. 2007, 229:213-224.
93. Schmitzer-Torbert N., Jackson J., Henze D., Harris K., Redish A.D. Quantitative measures of cluster quality for use in extracellular recordings. Neuroscience 2005, 131:1-11.
94. Schubert D., Kotter R., Staiger J.F. Mapping functional connectivity in barrel-related columns reveals layer- and cell type-specific microcircuits. Brain Struct. Funct. 2007, 212:107-119.
95. Shuler M.G., Bear M.F. Reward timing in the primary visual cortex. Science 2006, 311:1606-1609.
96. Smith P.H., Populin L.C. Fundamental differences between the thalamocortical recipient layers of the cat auditory and visual cortices. J. Comp. Neurol. 2001, 436:508-519.
97. 2+ imaging in transgenic mice. J. Neurosci. 2007, 27:2145-2149.
98. Song S., Sjostrom P.J., Reigl M., Nelson S., Chklovskii D.B. Highly nonrandom features of synaptic connectivity in local cortical circuits. PLoS Biol. 2005, 3:e68.
99. Steriade M., McCormick D.A., Sejnowski T.J. Thalamocortical oscillations in the sleeping and aroused brain. Science 1993, 262:679-685.
100. Steriade M., Nunez A., Amzica F. A novel slow (<1 Hz) oscillation of neocortical neurons in vivo: depolarizing and hyperpolarizing components. J. Neurosci. 1993, 13:3252-3265.
101. Steriade M., Timofeev I., Grenier F. Natural waking and sleep states: a view from inside neocortical neurons. J. Neurophysiol. 2001, 85:1969-1985.
102. Stopfer M., Jayaraman V., Laurent G. Intensity versus identity coding in an olfactory system. Neuron 2003, 39:991-1004.
103. Storm J.F. K(+) channels and their distribution in large cortical pyramidal neurones. J. Physiol. 2000, 525(Pt 3):565-566.
104. Sugase Y., Yamane S., Ueno S., Kawano K. Global and fine information coded by single neurons in the temporal visual cortex. Nature 1999, 400:869-873.
105. Sugino K., Hempel C.M., Miller M.N., Hattox A.M., Shapiro P., Wu C., Huang Z.J., Nelson S.B. Molecular taxonomy of major neuronal classes in the adult mouse forebrain. Nat. Neurosci. 2006, 9:99-107.
106. Swadlow H.A. Efferent neurons and suspected interneurons in binocular visual cortex of the awake rabbit: receptive fields and binocular properties. J. Neurophysiol. 1988, 59:1162-1187.
107. Swadlow H.A. Efferent neurons and suspected interneurons in S-1 vibrissa cortex of the awake rabbit: receptive fields and axonal properties. J. Neurophysiol. 1989, 62:288-308.
108. Swadlow H.A. Efferent neurons and suspected interneurons in motor cortex of the awake rabbit: axonal properties, sensory receptive fields, and subthreshold synaptic inputs. J. Neurophysiol. 1994, 71:437-453.
109. Szymanski F.D., Garcia-Lazaro J.A., Schnupp J.W. Current source density profiles of stimulus-specific adaptation in rat auditory cortex. J. Neurophysiol. 2009, 102:1483-1490.
110. Thomson A.M., Lamy C. Functional maps of neocortical local circuitry. Front. Neurosci. 2007, 1:19-42.
111. Turner J.G., Hughes L.F., Caspary D.M. Divergent response properties of layer-V neurons in rat primary auditory cortex. Hear. Res. 2005, 202:129-140.
112. Ulanovsky N., Las L., Nelken I. Processing of low-probability sounds by cortical neurons. Nat. Neurosci. 2003, 6:391-398.
113. Ulanovsky N., Las L., Farkas D., Nelken I. Multiple time scales of adaptation in auditory cortex neurons. J. Neurosci. 2004, 24:10440-10453.
114. van Brederode J.F., Spain W.J. Differences in inhibitory synaptic input between layer II-III and layer V neurons of the cat neocortex. J. Neurophysiol. 1995, 74:1149-1166.
115. Vanderwolf C.H. Are neocortical gamma waves related to consciousness?. Brain Res. 2000, 855:217-224.
116. Vanderwolf C.H. An Odyssey through the Brain, Behavior, and the Mind 2003, Kluwer Academic Pub, Boston.
117. Volkov I.O., Galazjuk A.V. Formation of spike response to sound tones in cat auditory cortex neurons: interaction of excitatory and inhibitory effects. Neuroscience 1991, 43:307-321.
118. Wallace M.N., Palmer A.R. Laminar differences in the response properties of cells in the primary auditory cortex. Exp. Brain Res. 2008, 184:179-191.
119. Wang X., Lu T., Snider R.K., Liang L. Sustained firing in auditory cortex evoked by preferred stimuli. Nature 2005, 435:341-346.
120. Wiest M.C., Nicolelis M.A. Behavioral detection of tactile stimuli during 7-12 Hz cortical oscillations in awake rats. Nat. Neurosci. 2003, 6:913-914.
121. Winer J.A., Lee C.C. The distributed auditory cortex. Hear. Res. 2007, 229:3-13.
122. Worgotter F., Suder K., Zhao Y., Kerscher N., Eysel U.T., Funke K. State-dependent receptive-field restructuring in the visual cortex. Nature 1998, 396:165-168.
123. Wu G.K., Arbuckle R., Liu B.H., Tao H.W., Zhang L.I. Lateral sharpening of cortical frequency tuning by approximately balanced inhibition. Neuron 2008, 58:132-143.
124. Zhou Y., Liu B.H., Wu G.K., Kim Y.J., Xiao Z., Tao H.W., Zhang L.I. Preceding inhibition silences layer 6 neurons in auditory cortex. Neuron 2010, 65:706-717.