The stimulus-evoked population response in visual cortex of awake monkey is a propagating wave

Nature Communications

Volumn 5, Issue , 2014, Pages

  Muller, Lyle ^a   Reynaud, Alexandre ^b   Chavane, Frédéric ^b   Destexhe, Alain ^a  

^a Unite de Neurosciences Integratives et Computationnelles   (France)

^b AIX MARSEILLE UNIVERSITÉ   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ACOUSTIC EMISSION; NEUROLOGY; NUMERICAL MODEL; PRIMATE; RELIABILITY ANALYSIS; WAVE PROPAGATION;

ANIMAL EXPERIMENT; ARTICLE; ELECTROENCEPHALOGRAM; EVOKED RESPONSE; EYE MOVEMENT; EYE POSITION; HAPLORHINI; MALE; MULTICHANNEL RECORDER; NERVE CELL NETWORK; NONHUMAN; RESPONSE TIME; SECONDARY VISUAL CORTEX; SPATIOTEMPORAL ANALYSIS; STIMULUS EVOKED POPULATION RESPONSE; STIMULUS RESPONSE; STRIATE CORTEX; VISUAL CORTEX; VISUAL STIMULATION; VOLTAGE SENSITIVE DYE IMAGING; WAKEFULNESS; ANIMAL; BIOLOGICAL MODEL; EVOKED VISUAL RESPONSE; EYE FIXATION; PHOTOSTIMULATION; PHYSIOLOGY; RHESUS MONKEY;

PYRAZOLE DERIVATIVE; RH1691; THIAZOLE DERIVATIVE;

ANIMALS; EVOKED POTENTIALS, VISUAL; EYE MOVEMENTS; FIXATION, OCULAR; MACACA MULATTA; MODELS, NEUROLOGICAL; PHOTIC STIMULATION; PYRAZOLES; THIAZOLES; VISUAL CORTEX;

EID: 84899642261     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms4675     Document Type: Article

References (69)

1. Ribary, U. et al. Magnetic field tomography of coherent thalamocortical 40-Hz oscillations in humans. Proc. Natl Acad. Sci. USA 88, 11037-11041 (1991). (Pubitemid 21915974)
2. Chavane, F. et al. The visual cortical association field: a Gestalt concept or a psychophysiological entity? J. Physiol. Paris 94, 333-342 (2000). (Pubitemid 32110918)
3. Maynard, E., Nordhausen, C. & Normann, R. The Utah intracortical electrode array: a recording structure for potential brain-computer interfaces. Electroencephalogr. Clin. Neurophysiol. 102, 228-239 (1997). (Pubitemid 27165391)
4. Grinvald, A. & Hildesheim, R. VSDI: a new era in functional imaging of cortical dynamics. Nat. Rev. Neurosci. 5, 874-885 (2004). (Pubitemid 39482156)
5. Grinvald, A., Lieke, E., Frostig, R. & Hilesheim, R. Cortical point-spread function and long-range lateral interactions revealed by real-time optical imaging of macaque monkey primary visual cortex. J. Neurosci. 14, 2545-2568 (1994). (Pubitemid 24140884)
6. Bringuier, V., Chavane, F., Glaeser, L. & Frégnac, Y. Horizontal propagation of visual activity in the synaptic integration field of area 17 neurons. Science 283, 695-699 (1999).
7. Jancke, D., Chavane, F., Naaman, S. & Grinvald, A. Imaging cortical correlates of illusion in early visual cortex. Nature 428, 423-426 (2004). (Pubitemid 38419687)
8. Roland, P. et al. Cortical feedback depolarization waves: a mechanism of top-down influence on early visual areas. Proc. Natl Acad. Sci. USA 103, 12586-12591 (2006). (Pubitemid 44267302)
9. Benucci, A., Frazor, R. & Carandini, M. Standing waves and traveling waves distinguish two circuits in visual cortex. Neuron 55, 103-117 (2007). (Pubitemid 46990820)
10. Xu, W., Huang, X., Takagaki, K. & Wu, J. Compression and reflection of visually evoked cortical waves. Neuron 55, 119-129 (2007). (Pubitemid 46990819)
11. Han, F., Caporale, N. & Dan, Y. Reverberation of recent visual experience in spontaneous cortical waves. Neuron 60, 321-327 (2008).
12. Huang, X. et al. Spiral wave dynamics in neocortex. Neuron 68, 978-990 (2010).
13. Gao, X. et al. Interactions between two propagating waves in rat visual cortex. Neuroscience 216, 57-59 (2012).
14. Stroh, A. et al. Making waves: initiation and propagation of corticothalamic Ca2+ waves in vivo. Neuron 77, 1136-1150 (2013).
15. Gabriel, A. & Eckhorn, R. A multi-channel correlation method detects traveling g-waves in monkey visual cortex. J. Neurosci. Methods 131, 171-184 (2003). (Pubitemid 37491472)
16. Rubino, D., Robbins, K. & Hatsopoulos, N. Propagating waves mediate information transfer in the motor cortex. Nat. Neurosci. 9, 1549-1557 (2006). (Pubitemid 44862664)
17. Witte, R., Rousche, P. & Kipke, D. Fast wave propagation in auditory cortex of an awake cat using a chronic microelectrode array. J. Neural. Eng. 4, 68-78 (2007). (Pubitemid 46603798)
18. Ferezou, I. et al. Spatiotemporal dynamics of cortical sensorimotor integration in behaving mice. Neuron 56, 907-923 (2007). (Pubitemid 350181347)
19. Mohajerani, M., McVea, D., Fingas, M. & Murphy, T. Mirrored bilateral slowwave cortical activity within local circuits revealed by fast bihemispheric voltage-sensitive dye imaging in anesthetized and awake mice. J. Neurosci. 30, 3745-3751 (2010).
20. Mohajerani, M. et al. Spontaneous cortical activity alternates between motifs defined by regional axonal projections. Nat. Neurosci. 16, 1426-1435 (2013).
21. Ermentrout, G. & Kleinfeld, D. Traveling electrical waves in cortex: insights from phase dynamics and speculation on a computational role. Neuron 29, 33-44 (2001). (Pubitemid 32108720)
22. Shoham, D. et al. Imaging cortical dynamics at high spatial and temporal resolution with novel blue voltage-sensitive dyes. Neuron 24, 791-802 (1999). (Pubitemid 30017659)
23. Slovin, H., Arieli, A., Hildesheim, R. & Grinvald, A. Long-term voltage-sensitive dye imaging reveals cortical dynamics in behaving monkeys. J. Neurophysiol. 88, 3421-3428 (2002).
24. Chen, Y., Geisler, W. & Seidemann, E. Optimal decoding of correlated neural population responses in the primate visual cortex. Nat. Neurosci. 9, 1412-1420 (2006). (Pubitemid 44646214)
25. Sit, Y., Chen, Y., Geisler, W., Miikkulainen, R. & Seidemann, E. Complex dynamics of V1 population responses explained by a simple gain-control model. Neuron 64, 943-956 (2009).
26. Reynaud, A., Masson, G. & Chavane, F. Dynamics of local input normalization result from balanced short- and long-range interactions in area V1. J. Neurosci. 32, 12558-12569 (2012).
27. Alexander, D. M. et al. Traveling waves and trial averaging: The nature of single-trial and averaged brain responses in large-scale cortical signals. Neuroimage 73, 95-112 (2013).
28. Reynaud, A., Takerkart, S., Masson, G. & Chavane, F. Linear model decomposition for voltage-sensitive dye imaging signals: application in awake behaving monkey. Neuroimage 54, 1196-1210 (2011).
29. Gabor, D. Theory of communication. Part 1: the analysis of information. J. Inst. Elec. Eng. -Part 3 93, 429-441 (1946).
30. Feldman, M. Hilbert Transform Applications in Mechanical Vibration 1st edn (Wiley, 2011).
31. González-Burgos, G., Barrionuevo, G. & Lewis, D. Horizontal synaptic connections in monkey prefrontal cortex: an in vitro electrophysiological study. Cereb. Cortex. 10, 82-92 (2000). (Pubitemid 30022835)
32. Girard, P., Hupé, J. & Bullier, J. Feedforward and feedback connections between areas V1 and V2 of the monkey have similar rapid conduction velocities. J. Neurophysiol. 85, 1328-1331 (2001). (Pubitemid 32209619)
33. Prechtl, J., Cohen, L., Pesaran, B., Mitra, P. & Kleinfeld, D. Visual stimuli induce waves of electrical activity in turtle cortex. Proc. Natl Acad. Sci. USA 94, 7621-7626 (1997). (Pubitemid 27345366)
34. Mitra, P. & Pesaran, B. Analysis of dynamic brain imaging data. Biophys. J. 76, 691-708 (1999). (Pubitemid 29264552)
35. Stettler, D., Das, A., Bennett, J. & Gilbert, C. Lateral connectivity and contextual interactions in macaque primary visual cortex. Neuron 36, 739-750 (2002). (Pubitemid 35350851)
36. Angelucci, A. et al. Circuits for local and global signal integration in primary visual cortex. J. Neurosci. 22, 8633-8646 (2002). (Pubitemid 35387603)
37. Dow, B., Snyder, A., Vautin, R. & Bauer, R. Magnification factor and receptive field size in foveal striate cortex of the monkey. Exp. Brain. Res. 44, 213-228 (1981). (Pubitemid 12227576)
38. Tehovnik, E. J. & Slocum, W. M. What delay fields tell us about striate cortex. J. Neurophysiol. 98, 559-576 (2007). (Pubitemid 47236015)
39. Van Essen, D. C., Newsome, W. T. & Maunsell, J. H. The visual field representation in striate cortex of the macaque monkey: asymmetries, anisotropies, and individual variability. Vis. Res. 24, 429-448 (1984). (Pubitemid 14106001)
40. Fisher, N. Statistical Analysis of Circular Data 1st edn (Cambridge University Press, 1993).
41. Waxman, S. & Bennett, M. Relative conduction velocities of small myelinated and non-myelinated fibres in the central nervous system. Nat. New. Biol. 238, 217-219 (1972).
42. Kennedy, H. & Bullier, J. A double-labeling investigation of the afferent connectivity to cortical areas V1 and V2 of the macaque monkey. J. Neurosci. 5, 2815-2830 (1985). (Pubitemid 16232371)
43. Ayzenshtat, I. et al. Precise spatiotemporal patterns among visual cortical areas and their relation to visual stimulus processing. J. Neurosci. 30, 11232-11245 (2010).
44. Sato, T., Nauhaus, I. & Carandini, M. Traveling waves in visual cortex. Neuron 75, 218-229 (2012).
45. Muller, L. & Destexhe, A. Propagating waves in thalamus, cortex and the thalamocortical system: experiments and models. J. Physiol. Paris 106, 222-238 (2012).
46. Bullier, J. Integrated model of visual processing. Brain. Res. Rev. 36, 96-107 (2001). (Pubitemid 33020739)
47. Takagaki, K., Zhang, C., Wu, J. & Ohl, F. Flow detection of propagating waves with temporospatial correlation of activity. J. Neurosci. Methods 200, 207-218 (2011).
48. Nauhaus, I., Busse, L., Carandini, M. & Ringrach, D. Stimulus contrast modulates functional connectivity in visual cortex. Nat. Neurosci. 12, 70-76 (2009).
49. Chemla, S. & Chavane, F. A biophysical cortical column model to study the multi-component origin of the VSDI signal. Neuroimage 53, 420-438 (2010).
50. Destexhe, A. & Paré, D. Impact of network activity on the integrative properties of neocortical pyramidal neurons in vivo. J. Neurophysiol. 81, 1531-1547 (1999). (Pubitemid 29262485)
51. Destexhe, A., Rudolph, M. & Paré, D. The high-conductance state of neocortical neurons in vivo. Nat. Rev. Neurosci. 4, 739-751 (2003). (Pubitemid 37280153)
52. Poulet, J. & Petersen, C. Internal brain state regulates membrane potential synchrony in barrel cortex of behaving mice. Nature 454, 881-885 (2008).
53. Destexhe, A., Rudolph, M., Fellous, J. & Sejnowski, T. Fluctuating synaptic conductances recreate in-vivo-like activity in neocortical neurons. Neuroscience 107, 13-24 (2001). (Pubitemid 34020681)
54. Kuhn, A., Aertsen, A. & Rotter, S. Neuronal integration of synaptic input in the fluctuation-driven regime. J. Neurosci. 24, 2345-2356 (2004). (Pubitemid 38327947)
55. Rudolph, M., Pospischil, M., Timofeev, I. & Destexhe, A. Inhibition determines membrane potential dynamics and controls action potential generation in awake and sleeping cat cortex. J. Neurosci. 27, 5280-5290 (2007). (Pubitemid 46790168)
56. Gilbert, C. Horizontal integration and cortical dynamics. Neuron 9, 1-13 (1992).
57. Grossberg, S., Mingolla, E. & Ross, W. Visual brain and visual perception: how does the cortex do perceptual grouping? Trends Neurosci. 20, 106-111 (1997). (Pubitemid 27086724)
58. Gilbert, C. Adult cortical dynamics. Physiol. Rev. 78, 467-485 (1998). (Pubitemid 28182901)
59. Raizada, R. & Grossberg, S. Towards a theory of the laminar architecture of cerebral cortex: computational clues from the visual system. Cereb. Cortex 13, 100-113 (2003). (Pubitemid 35462898)
60. Arieli, A., Grinvald, A. & Slovin, H. Dural substitute for long-term imaging of cortical activity in behaving monkeys and its clinical implications. J. Neurosci. Methods 114, 119-133 (2002). (Pubitemid 34150116)
61. Robinson, D. A method of measuring eye movement using a scleral search coil in a magnetic field. IEEE Trans. Biomed. Eng. 10, 137-145 (1963).
62. Hays, A., Richmond, B. & Optican, L. A UNIX-based multiple process system for real-time data acquisition and control. WESCON Conf. Proc. 2, 1-10 (1982).
63. Garcia, D. Robust smoothing of gridded data in one and higher dimensions with missing values. Comput. Stat. Data Anal. 54, 1167-1178 (2010).
64. Goswami, J. & Hoefel, A. Algorithms for estimating instantaneous frequency. Signal Proc. 84, 1423-1427 (2004).
65. Yger, P., Boustani, S. E., Destexhe, A. & Frégnac, Y. Topologically invariant macroscopic statistics in balanced networks of conductance-based integrateand- fire neurons. J. Comput. Neurosci. 31, 229-245 (2011).
66. Davison, A. et al. PyNN: a common interface for neuronal network simulators. Front. Neuroinform. 2, 1-10 (2009).
67. Gewaltig, M. & Diesmann, M. NEST (Neural Simulation Tool). Scholarpedia 2, 1430 (2007).
68. Jammalakadaka, S. & Sengupta, A. Topics in Circular Statistics 1st edn (World Scientific, Singapore, 2001).
69. Berens, P. CircStat: a Matlab toolbox for circular statistics. J. Stat. Softw. 31 (2009).