A cortical circuit for gain control by behavioral state

Cell

Volumn 156, Issue 6, 2014, Pages 1139-1152

  Fu, Yu ^a   Tucciarone, Jason M ^b,c   Espinosa, J Sebastian ^a   Sheng, Nengyin ^a   Darcy, Daniel P ^a   Nicoll, Roger A ^a   Huang, Z Josh ^b   Stryker, Michael P ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

^c STONY BROOK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; NICOTINIC RECEPTOR; VASOACTIVE INTESTINAL POLYPEPTIDE; ACETYLCHOLINE;

ANIMAL EXPERIMENT; ARTICLE; BEHAVIOR; CALCIUM SIGNALING; FOREBRAIN; IN VIVO STUDY; LOCOMOTION; MOUSE; NERVE CELL; NEUROIMAGING; NEUROMODULATION; NEUROPHYSIOLOGY; NONHUMAN; OPTOGENETICS; PHOTOLYSIS; PRIORITY JOURNAL; SENSORY CORTEX; STRIATE CORTEX; VISUAL STIMULATION; ADULT; ANIMAL BEHAVIOR; ANIMAL MODEL; ANIMAL TISSUE; BEHAVIORAL STATE; CELL ACTIVITY; CONTROLLED STUDY; CORTICAL CIRCUIT; ELECTROPHYSIOLOGICAL PROCEDURES; ENZYME INHIBITION; EVOKED CORTICAL RESPONSE; EVOKED VISUAL RESPONSE; IMAGING SYSTEM; NEOCORTEX; NERVE CELL PLASTICITY; PEDUNCULOPONTINE TEGMENTAL NUCLEUS; PHYSICAL ACTIVITY; SENSORY NERVE; SIGNAL TRANSDUCTION; WAKEFULNESS;

ANIMALS; FEMALE; GABAERGIC NEURONS; GAMMA-AMINOBUTYRIC ACID; MALE; MICE; NEOCORTEX; NEURONS; RECEPTORS, NICOTINIC; RUNNING; VASOACTIVE INTESTINAL PEPTIDE; VISUAL PATHWAYS;

EID: 84896371671     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2014.01.050     Document Type: Article

References (62)

1. H. Adesnik, W. Bruns, H. Taniguchi, Z.J. Huang, and M. Scanziani A neural circuit for spatial summation in visual cortex Nature 490 2012 226 231
2. H.J. Alitto, and Y. Dan Cell-type-specific modulation of neocortical activity by basal forebrain input Front. Syst. Neurosci. 6 2012 79
3. S. Arroyo, C. Bennett, D. Aziz, S.P. Brown, and S. Hestrin Prolonged disynaptic inhibition in the cortex mediated by slow, non-α7 nicotinic excitation of a specific subset of cortical interneurons J. Neurosci. 32 2012 3859 3864
4. A. Ayaz, A.B. Saleem, M.L. Schölvinck, and M. Carandini Locomotion controls spatial integration in mouse visual cortex Curr. Biol. 23 2013 890 894
5. M. Bazhenov, I. Timofeev, M. Steriade, and T.J. Sejnowski Model of thalamocortical slow-wave sleep oscillations and transitions to activated States J. Neurosci. 22 2002 8691 8704
6. C.I. Buia, and P.H. Tiesinga Role of interneuron diversity in the cortical microcircuit for attention J. Neurophysiol. 99 2008 2158 2182
7. T.W. Chen, T.J. Wardill, Y. Sun, S.R. Pulver, S.L. Renninger, A. Baohan, E.R. Schreiter, R.A. Kerr, M.B. Orger, and V. Jayaraman et al. Ultrasensitive fluorescent proteins for imaging neuronal activity Nature 499 2013 295 300
8. Y. Chen, S. Martinez-Conde, S.L. Macknik, Y. Bereshpolova, H.A. Swadlow, and J.M. Alonso Task difficulty modulates the activity of specific neuronal populations in primary visual cortex Nat. Neurosci. 11 2008 974 982
9. S. Crochet, J.F. Poulet, Y. Kremer, and C.C. Petersen Synaptic mechanisms underlying sparse coding of active touch Neuron 69 2011 1160 1175
10. D.A. Dombeck, C.D. Harvey, L. Tian, L.L. Looger, and D.W. Tank Functional imaging of hippocampal place cells at cellular resolution during virtual navigation Nat. Neurosci. 13 2010 1433 1440
11. A. Fontanini, and D.B. Katz Behavioral states, network states, and sensory response variability J. Neurophysiol. 100 2008 1160 1168
12. S.P. Gandhi, Y. Yanagawa, and M.P. Stryker Delayed plasticity of inhibitory neurons in developing visual cortex Proc. Natl. Acad. Sci. USA 105 2008 16797 16802
13. E. Garcia-Rill The pedunculopontine nucleus Prog. Neurobiol. 36 1991 363 389
14. L.J. Gentet, Y. Kremer, H. Taniguchi, Z.J. Huang, J.F. Staiger, and C.C. Petersen Unique functional properties of somatostatin-expressing GABAergic neurons in mouse barrel cortex Nat. Neurosci. 15 2012 607 612
15. B. Haider, M. Häusser, and M. Carandini Inhibition dominates sensory responses in the awake cortex Nature 493 2013 97 100
16. C.D. Harvey, P. Coen, and D.W. Tank Choice-specific sequences in parietal cortex during a virtual-navigation decision task Nature 484 2012 62 68
17. M.E. Hasselmo, and L.M. Giocomo Cholinergic modulation of cortical function J. Mol. Neurosci. 30 2006 133 135
18. T.K. Hensch Critical period plasticity in local cortical circuits Nat. Rev. Neurosci. 6 2005 877 888
19. S. Hill, and G. Tononi Modeling sleep and wakefulness in the thalamocortical system J. Neurophysiol. 93 2005 1671 1698
20. Z.J. Huang, G. Di Cristo, and F. Ango Development of GABA innervation in the cerebral and cerebellar cortices Nat. Rev. Neurosci. 8 2007 673 686
21. D. Huber, D.A. Gutnisky, S. Peron, D.H. O'Connor, J.S. Wiegert, L. Tian, T.G. Oertner, L.L. Looger, and K. Svoboda Multiple dynamic representations in the motor cortex during sensorimotor learning Nature 484 2012 473 478
22. Y. Kawaguchi Selective cholinergic modulation of cortical GABAergic cell subtypes J. Neurophysiol. 78 1997 1743 1747
23. G.B. Keller, T. Bonhoeffer, and M. Hübener Sensorimotor mismatch signals in primary visual cortex of the behaving mouse Neuron 74 2012 809 815
24. S.J. Kuhlman, N.D. Olivas, E. Tring, T. Ikrar, X. Xu, and J.T. Trachtenberg A disinhibitory microcircuit initiates critical-period plasticity in the visual cortex Nature 501 2013 543 546
25. S. Lee, J. Hjerling-Leffler, E. Zagha, G. Fishell, and B. Rudy The largest group of superficial neocortical GABAergic interneurons expresses ionotropic serotonin receptors J. Neurosci. 30 2010 16796 16808
26. S. Lee, I. Kruglikov, Z.J. Huang, G. Fishell, and B. Rudy A disinhibitory circuit mediates motor integration in the somatosensory cortex Nat. Neurosci. 16 2013 1662 1670
27. S.H. Lee, A.C. Kwan, S. Zhang, V. Phoumthipphavong, J.G. Flannery, S.C. Masmanidis, H. Taniguchi, Z.J. Huang, F. Zhang, and E.S. Boyden et al. Activation of specific interneurons improves V1 feature selectivity and visual perception Nature 488 2012 379 383
28. J.J. Letzkus, S.B. Wolff, E.M. Meyer, P. Tovote, J. Courtin, C. Herry, and A. Lüthi A disinhibitory microcircuit for associative fear learning in the auditory cortex Nature 480 2011 331 335
29. L. Madisen, T.A. Zwingman, S.M. Sunkin, S.W. Oh, H.A. Zariwala, H. Gu, L.L. Ng, R.D. Palmiter, M.J. Hawrylycz, and A.R. Jones et al. A robust and high-throughput Cre reporting and characterization system for the whole mouse brain Nat. Neurosci. 13 2010 133 140
30. H. Markram, M. Toledo-Rodriguez, Y. Wang, A. Gupta, G. Silberberg, and C. Wu Interneurons of the neocortical inhibitory system Nat. Rev. Neurosci. 5 2004 793 807
31. J.H. Maunsell, and E.P. Cook The role of attention in visual processing Philos. Trans. R. Soc. Lond. B Biol. Sci. 357 2002 1063 1072
32. J.F. Maya Vetencourt, A. Sale, A. Viegi, L. Baroncelli, R. De Pasquale, O.F. O'Leary, E. Castrén, and L. Maffei The antidepressant fluoxetine restores plasticity in the adult visual cortex Science 320 2008 385 388
33. R. Metherate, C.L. Cox, and J.H. Ashe Cellular bases of neocortical activation: modulation of neural oscillations by the nucleus basalis and endogenous acetylcholine J. Neurosci. 12 1992 4701 4711
34. J.W. Mink, H.M. Sinnamon, and D.B. Adams Activity of basal forebrain neurons in the rat during motivated behaviors Behav. Brain Res. 8 1983 85 108
35. J.F. Mitchell, K.A. Sundberg, and J.H. Reynolds Differential attention-dependent response modulation across cell classes in macaque visual area V4 Neuron 55 2007 131 141
36. E.L. Newman, K. Gupta, J.R. Climer, C.K. Monaghan, and M.E. Hasselmo Cholinergic modulation of cognitive processing: insights drawn from computational models Front. Behav. Neurosci. 6 2012 24
37. C.M. Niell, and M.P. Stryker Modulation of visual responses by behavioral state in mouse visual cortex Neuron 65 2010 472 479
38. L. Petreanu, D.A. Gutnisky, D. Huber, N.L. Xu, D.H. O'Connor, L. Tian, L. Looger, and K. Svoboda Activity in motor-sensory projections reveals distributed coding in somatosensation Nature 489 2012 299 303
39. C.K. Pfeffer, M. Xue, M. He, Z.J. Huang, and M. Scanziani Inhibition of inhibition in visual cortex: the logic of connections between molecularly distinct interneurons Nat. Neurosci. 16 2013 1068 1076
40. H.J. Pi, B. Hangya, D. Kvitsiani, J.I. Sanders, Z.J. Huang, and A. Kepecs Cortical interneurons that specialize in disinhibitory control Nature 503 2013 521 524
41. P.O. Polack, J. Friedman, and P. Golshani Cellular mechanisms of brain state-dependent gain modulation in visual cortex Nat. Neurosci. 16 2013 1331 1339
42. M.I. Posner, and S.E. Petersen The attention system of the human brain Annu. Rev. Neurosci. 13 1990 25 42
43. J.H. Reynolds, and L. Chelazzi Attentional modulation of visual processing Annu. Rev. Neurosci. 27 2004 611 647
44. R. Rodriguez, U. Kallenbach, W. Singer, and M.H. Munk Short- and long-term effects of cholinergic modulation on gamma oscillations and response synchronization in the visual cortex J. Neurosci. 24 2004 10369 10378
45. B. Rudy, G. Fishell, S. Lee, and J. Hjerling-Leffler Three groups of interneurons account for nearly 100% of neocortical GABAergic neurons Dev. Neurobiol. 71 2011 45 61
46. H. Sato, Y. Hata, K. Hagihara, and T. Tsumoto Effects of cholinergic depletion on neuron activities in the cat visual cortex J. Neurophysiol. 58 1987 781 794
47. H. Sato, Y. Hata, H. Masui, and T. Tsumoto A functional role of cholinergic innervation to neurons in the cat visual cortex J. Neurophysiol. 58 1987 765 780
48. H. Taniguchi, M. He, P. Wu, S. Kim, R. Paik, K. Sugino, D. Kvitsiani, Y. Fu, J. Lu, and Y. Lin et al. A resource of Cre driver lines for genetic targeting of GABAergic neurons in cerebral cortex Neuron 71 2011 995 1013
49. N.M. Weinberger Associative representational plasticity in the auditory cortex: a synthesis of two disciplines Learn. Mem. 14 2007 1 16
50. I.R. Wickersham, D.C. Lyon, R.J. Barnard, T. Mori, S. Finke, K.K. Conzelmann, J.A. Young, and E.M. Callaway Monosynaptic restriction of transsynaptic tracing from single, genetically targeted neurons Neuron 53 2007 639 647
51. R.H. Wurtz, and C.W. Mohler Enhancement of visual responses in monkey striate cortex and frontal eye fields J. Neurophysiol. 39 1976 766 772
52. N.L. Xu, M.T. Harnett, S.R. Williams, D. Huber, D.H. O'Connor, K. Svoboda, and J.C. Magee Nonlinear dendritic integration of sensory and motor input during an active sensing task Nature 492 2012 247 251
53. D.H. Brainard The Psychophysics Toolbox Spat. Vis. 10 1997 433 436
54. M. Guizar-Sicairos, S.T. Thurman, and J.R. Fienup Efficient subpixel image registration algorithms Opt. Lett. 33 2008 156 158
55. K.D. Harris, D.A. Henze, J. Csicsvari, H. Hirase, and G. Buzsáki Accuracy of tetrode spike separation as determined by simultaneous intracellular and extracellular measurements J. Neurophysiol. 84 2000 401 414
56. S.J. Kuhlman, E. Tring, and J.T. Trachtenberg Fast-spiking interneurons have an initial orientation bias that is lost with vision Nat. Neurosci. 14 2011 1121 1123
57. K. Miyamichi, F. Amat, F. Moussavi, C. Wang, I. Wickersham, N.R. Wall, H. Taniguchi, B. Tasic, Z.J. Huang, and Z. He et al. Cortical representations of olfactory input by trans-synaptic tracing Nature 472 2011 191 196
58. C.M. Niell, and M.P. Stryker Highly selective receptive fields in mouse visual cortex J. Neurosci. 28 2008 7520 7536
59. D.G. Pelli The VideoToolbox software for visual psychophysics: transforming numbers into movies Spat. Vis. 10 1997 437 442
60. N. Schmitzer-Torbert, J. Jackson, D. Henze, K. Harris, and A.D. Redish Quantitative measures of cluster quality for use in extracellular recordings Neuroscience 131 2005 1 11
61. C. Stosiek, O. Garaschuk, K. Holthoff, and A. Konnerth In vivo two-photon calcium imaging of neuronal networks Proc. Natl. Acad. Sci. USA 100 2003 7319 7324
62. L. Wang, K. Sharma, H.X. Deng, T. Siddique, G. Grisotti, E. Liu, and R.P. Roos Restricted expression of mutant SOD1 in spinal motor neurons and interneurons induces motor neuron pathology Neurobiol. Dis. 29 2008 400 408