Arousal and Locomotion Make Distinct Contributions to Cortical Activity Patterns and Visual Encoding

Neuron

Volumn 86, Issue 3, 2015, Pages 740-754

  Vinck, Martin ^a   Batista Brito, Renata ^a   Knoblich, Ulf ^a,b   Cardin, Jessica A ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b ALLEN INSTITUTE FOR BRAIN SCIENCE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTICIPATION; AROUSAL; ARTICLE; EVOKED VISUAL RESPONSE; LOCOMOTION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PUPIL; SENSORY FEEDBACK; SIGNAL NOISE RATIO; TREADMILL; VISUAL STIMULATION; WAKEFULNESS; ACTION POTENTIAL; ANIMAL; COMPUTER SIMULATION; FOURIER ANALYSIS; PERCEPTIVE DISCRIMINATION; PHYSIOLOGY; VISUAL CORTEX; VISUAL SYSTEM;

ACTION POTENTIALS; ANIMALS; AROUSAL; COMPUTER SIMULATION; FOURIER ANALYSIS; LOCOMOTION; MALE; MICE; PUPIL; SIGNAL DETECTION, PSYCHOLOGICAL; VISUAL CORTEX; VISUAL PATHWAYS; WAKEFULNESS;

EID: 84929045501     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2015.03.028     Document Type: Article

References (60)

1. Aston-Jones G., Cohen J.D. An integrative theory of locus coeruleus-norepinephrine function: adaptive gain and optimal performance. Annu. Rev. Neurosci. 2005, 28:403-450.
2. Bennett C., Arroyo S., Hestrin S. Subthreshold mechanisms underlying state-dependent modulation of visual responses. Neuron 2013, 80:350-357.
3. Berger H. Über das elektrenkephalogramm des menschen. Eur. Arch. Psychiatry Clin. Neurosci. 1929, 87:527-570.
4. Bruce C.J., Goldberg M.E. Primate frontal eye fields. I. Single neurons discharging before saccades. J.Neurophysiol. 1985, 53:603-635.
5. Busse L., Ayaz A., Dhruv N.T., Katzner S., Saleem A.B., Schölvinck M.L., Zaharia A.D., Carandini M. The detection of visual contrast in the behaving mouse. J.Neurosci. 2011, 31:11351-11361.
6. 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.
7. Cardin J.A., Carlén M., Meletis K., Knoblich U., Zhang F., Deisseroth K., Tsai L.H., Moore C.I. Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature 2009, 459:663-667.
8. Carter M.E., Yizhar O., Chikahisa S., Nguyen H., Adamantidis A., Nishino S., Deisseroth K., de Lecea L. Tuning arousal with optogenetic modulation of locus coeruleus neurons. Nat. Neurosci. 2010, 13:1526-1533.
9. Civillico E.F., Contreras D. Spatiotemporal properties of sensory responses invivo are strongly dependent on network context. Front. Syst. Neurosci. 2012, 6:25.
10. Cohen M.R., Kohn A. Measuring and interpreting neuronal correlations. Nat. Neurosci. 2011, 14:811-819.
11. Cohen M.R., Maunsell J.H. Attention improves performance primarily by reducing interneuronal correlations. Nat. Neurosci. 2009, 12:1594-1600.
12. Constantinople C.M., Bruno R.M. Effects and mechanisms of wakefulness on local cortical networks. Neuron 2011, 69:1061-1068.
13. Contreras D., Timofeev I., Steriade M. Mechanisms of long-lasting hyperpolarizations underlying slow sleep oscillations in cat corticothalamic networks. J.Physiol. 1996, 494:251-264.
14. Crochet S., Petersen C.C. Correlating whisker behavior with membrane potential in barrel cortex of awake mice. Nat. Neurosci. 2006, 9:608-610.
15. Csicsvari J., Jamieson B., Wise K.D., Buzsáki G. Mechanisms of gamma oscillations in the hippocampus of the behaving rat. Neuron 2003, 37:311-322.
16. Destexhe A., Contreras D., Steriade M. Spatiotemporal analysis of local field potentials and unit discharges in cat cerebral cortex during natural wake and sleep states. J.Neurosci. 1999, 19:4595-4608.
17. Ecker A.S., Berens P., Keliris G.A., Bethge M., Logothetis N.K., Tolias A.S. Decorrelated neuronal firing in cortical microcircuits. Science 2010, 327:584-587.
18. Eldar E., Cohen J.D., Niv Y. The effects of neural gain on attention and learning. Nat. Neurosci. 2013, 16:1146-1153.
19. Fries P., Reynolds J.H., Rorie A.E., Desimone R. Modulation of oscillatory neuronal synchronization by selective visual attention. Science 2001, 291:1560-1563.
20. Fu Y., Tucciarone J.M., Espinosa J.S., Sheng N., Darcy D.P., Nicoll R.A., Huang Z.J., Stryker M.P. A cortical circuit for gain control by behavioral state. Cell 2014, 156:1139-1152.
21. Gentet L.J., Avermann M., Matyas F., Staiger J.F., Petersen C.C. Membrane potential dynamics of GABAergic neurons in the barrel cortex of behaving mice. Neuron 2010, 65:422-435.
22. Gentet L.J., Kremer Y., Taniguchi H., Huang Z.J., Staiger J.F., Petersen C.C. Unique functional properties of somatostatin-expressing GABAergic neurons in mouse barrel cortex. Nat. Neurosci. 2012, 15:607-612.
23. Gilzenrat M.S., Nieuwenhuis S., Jepma M., Cohen J.D. Pupil diameter tracks changes in control state predicted by the adaptive gain theory of locus coeruleus function. Cogn. Affect. Behav. Neurosci. 2010, 10:252-269.
24. Guo Z.V., Li N., Huber D., Ophir E., Gutnisky D., Ting J.T., Feng G., Svoboda K. Flow of cortical activity underlying a tactile decision in mice. Neuron 2014, 81:179-194.
25. Haider B., Häusser M., Carandini M. Inhibition dominates sensory responses in the awake cortex. Nature 2013, 493:97-100.
26. Harris K.D., Thiele A. Cortical state and attention. Nat. Rev. Neurosci. 2011, 12:509-523.
27. Hasenstaub A., Sachdev R.N., McCormick D.A. State changes rapidly modulate cortical neuronal responsiveness. J.Neurosci. 2007, 27:9607-9622.
28. Herrero J.L., Gieselmann M.A., Sanayei M., Thiele A. Attention-induced variance and noise correlation reduction in macaque V1 is mediated by NMDA receptors. Neuron 2013, 78:729-739.
29. Keller G.B., Bonhoeffer T., Hübener M. Sensorimotor mismatch signals in primary visual cortex of the behaving mouse. Neuron 2012, 74:809-815.
30. Lee S., Kruglikov I., Huang Z.J., Fishell G., Rudy B. A disinhibitory circuit mediates motor integration in the somatosensory cortex. Nat. Neurosci. 2013, 16:1662-1670.
31. Lee A.M., Hoy J.L., Bonci A., Wilbrecht L., Stryker M.P., Niell C.M. Identification of a brainstem circuit regulating visual cortical state in parallel with locomotion. Neuron 2014, 83:455-466.
32. Livingstone M.S., Hubel D.H. Effects of sleep and arousal on the processing of visual information in the cat. Nature 1981, 291:554-561.
33. McAdams C.J., Maunsell J.H. Effects of attention on the reliability of individual neurons in monkey visual cortex. Neuron 1999, 23:765-773.
34. McCormick D.A., Bal T. Sleep and arousal: thalamocortical mechanisms. Annu. Rev. Neurosci. 1997, 20:185-215.
35. Metherate R., Cox C.L., Ashe J.H. Cellular bases of neocortical activation: modulation of neural oscillations by the nucleus basalis and endogenous acetylcholine. J.Neurosci. 1992, 12:4701-4711.
36. Miller M.W., Vogt B.A. Direct connections of rat visual cortex with sensory, motor, and association cortices. J.Comp. Neurol. 1984, 226:184-202.
37. Mitchell J.F., Sundberg K.A., Reynolds J.H. Spatial attention decorrelates intrinsic activity fluctuations in macaque area V4. Neuron 2009, 63:879-888.
38. Munk M.H., Roelfsema P.R., König P., Engel A.K., Singer W. Role of reticular activation in the modulation of intracortical synchronization. Science 1996, 272:271-274.
39. Niell C.M., Stryker M.P. Modulation of visual responses by behavioral state in mouse visual cortex. Neuron 2010, 65:472-479.
40. Olshausen B.A., Field D.J. Emergence of simple-cell receptive field properties by learning a sparse code for natural images. Nature 1996, 381:607-609.
41. Pinto L., Goard M.J., Estandian D., Xu M., Kwan A.C., Lee S.H., Harrison T.C., Feng G., Dan Y. Fast modulation of visual perception by basal forebrain cholinergic neurons. Nat. Neurosci. 2013, 16:1857-1863.
42. Polack P.O., Friedman J., Golshani P. Cellular mechanisms of brain state-dependent gain modulation in visual cortex. Nat. Neurosci. 2013, 16:1331-1339.
43. Pouget A., Dayan P., Zemel R. Information processing with population codes. Nat. Rev. Neurosci. 2000, 1:125-132.
44. Reimer J., Froudarakis E., Cadwell C.R., Yatsenko D., Denfield G.H., Tolias A.S. Pupil fluctuations track fast switching of cortical states during quiet wakefulness. Neuron 2014, 84:355-362.
45. Saleem A.B., Ayaz A., Jeffery K.J., Harris K.D., Carandini M. Integration of visual motion and locomotion in mouse visual cortex. Nat. Neurosci. 2013, 16:1864-1869.
46. Schneider D.M., Nelson A., Mooney R. A synaptic and circuit basis for corollary discharge in the auditory cortex. Nature 2014, 513:189-194.
47. Shinomoto S., Kim H., Shimokawa T., Matsuno N., Funahashi S., Shima K., Fujita I., Tamura H., Doi T., Kawano K., et al. Relating neuronal firing patterns to functional differentiation of cerebral cortex. PLoS Comput. Biol. 2009, 5:e1000433.
48. Snyder L.H., Batista A.P., Andersen R.A. Coding of intention in the posterior parietal cortex. Nature 1997, 386:167-170.
49. Sohal V.S., Zhang F., Yizhar O., Deisseroth K. Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature 2009, 459:698-702.
50. Steriade M., McCormick D.A., Sejnowski T.J. Thalamocortical oscillations in the sleeping and aroused brain. Science 1993, 262:679-685.
51. Steriade M., Timofeev I., Grenier F. Natural waking and sleep states: a view from inside neocortical neurons. J.Neurophysiol. 2001, 85:1969-1985.
52. van Kerkoerle T., Self M.W., Dagnino B., Gariel-Mathis M.A., Poort J., van der Togt C., Roelfsema P.R. Alpha and gamma oscillations characterize feedback and feedforward processing in monkey visual cortex. Proc. Natl. Acad. Sci. USA 2014, 111:14332-14341.
53. Vinck M., Battaglia F.P., Womelsdorf T., Pennartz C. Improved measures of phase-coupling between spikes and the Local Field Potential. J.Comput. Neurosci. 2012, 33:53-75.
54. Vinck M., Womelsdorf T., Buffalo E.A., Desimone R., Fries P. Attentional modulation of cell-class-specific gamma-band synchronization in awake monkey area v4. Neuron 2013, 80:1077-1089.
55. Wang Q., Gao E., Burkhalter A. Gateways of ventral and dorsal streams in mouse visual cortex. J.Neurosci. 2011, 31:1905-1918.
56. Whittington M.A., Traub R.D., Jefferys J.G. Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation. Nature 1995, 373:612-615.
57. Womelsdorf T., Lima B., Vinck M., Oostenveld R., Singer W., Neuenschwander S., Fries P. Orientation selectivity and noise correlation in awake monkey area V1 are modulated by the gamma cycle. Proc. Natl. Acad. Sci. USA 2012, 109:4302-4307.
58. Zagha E., Casale A.E., Sachdev R.N., McGinley M.J., McCormick D.A. Motor cortex feedback influences sensory processing by modulating network state. Neuron 2013, 79:567-578.
59. Zhang S., Xu M., Kamigaki T., Hoang Do J.P., Chang W.C., Jenvay S., Miyamichi K., Luo L., Dan Y. Selective attention. Long-range and local circuits for top-down modulation of visual cortex processing. Science 2014, 345:660-665.
60. Zhou M., Liang F., Xiong X.R., Li L., Li H., Xiao Z., Tao H.W., Zhang L.I. Scaling down of balanced excitation and inhibition by active behavioral states in auditory cortex. Nat. Neurosci. 2014, 17:841-850.