Attentional Stimulus Selection through Selective Synchronization between Monkey Visual Areas

Neuron

Volumn 75, Issue 5, 2012, Pages 875-888

  Bosman, Conrado A ^a,b   Schoffelen, Jan Mathijs ^a   Brunet, Nicolas ^a   Oostenveld, Robert ^a   Bastos, Andre M ^a,c,d   Womelsdorf, Thilo ^a   Rubehn, Birthe ^e   Stieglitz, Thomas ^e   De Weerd, Peter ^a,f   Fries, Pascal ^a,c  

^a RADBOUD UNIVERSITY   (Netherlands)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c ERNST STRÜNGMANN INSTITUTE ESI FOR NEUROSCIENCE IN COOPERATION WITH MAX PLANCK SOCIETY   (Germany)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF FREIBURG   (Germany)

^f MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; CORTICAL SYNCHRONIZATION; ELECTROCORTICOGRAPHY; FREQUENCY MODULATION; GAMMA RHYTHM; HAPLORHINI; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; RECEPTIVE FIELD; RESPONSE TIME; SECONDARY VISUAL CORTEX; SELECTIVE ATTENTION; STIMULUS RESPONSE; STRIATE CORTEX; VISUAL AREA V3; VISUAL AREA V4; VISUAL CORTEX; VISUAL FIELD; VISUAL STIMULATION;

ANIMALS; ATTENTION; BRAIN MAPPING; CORTICAL SYNCHRONIZATION; ELECTRIC STIMULATION; MACACA; VISUAL CORTEX; VISUAL PATHWAYS; VISUAL PERCEPTION;

EID: 84865986209     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2012.06.037     Document Type: Article

References (64)

1. Akam T., Kullmann D.M. Oscillations and filtering networks support flexible routing of information. Neuron 2010, 67:308-320.
2. Barone P., Batardiere A., Knoblauch K., Kennedy H. Laminar distribution of neurons in extrastriate areas projecting to visual areas V1 and V4 correlates with the hierarchical rank and indicates the operation of a distance rule. J. Neurosci. 2000, 20:3263-3281.
3. Bichot N.P., Rossi A.F., Desimone R. Parallel and serial neural mechanisms for visual search in macaque area V4. Science 2005, 308:529-534.
4. Börgers C., Kopell N.J. Gamma oscillations and stimulus selection. Neural Comput. 2008, 20:383-414.
5. Bosman C.A., Womelsdorf T., Desimone R., Fries P. A microsaccadic rhythm modulates gamma-band synchronization and behavior. J. Neurosci. 2009, 29:9471-9480.
6. Bragin A., Jandó G., Nádasdy Z., Hetke J., Wise K., Buzsáki G. Gamma (40-100 Hz) oscillation in the hippocampus of the behaving rat. J. Neurosci. 1995, 15:47-60.
7. Buehlmann A., Deco G. Optimal information transfer in the cortex through synchronization. PLoS Comput. Biol. 2010, 6:e1000934.
8. Buffalo E.A., Fries P., Landman R., Buschman T.J., Desimone R. Laminar differences in gamma and alpha coherence in the ventral stream. Proc. Natl. Acad. Sci. USA 2011, 108:11262-11267.
9. Buschman T.J., Miller E.K. Top-down versus bottom-up control of attention in the prefrontal and posterior parietal cortices. Science 2007, 315:1860-1862.
10. Busse L., Katzner S., Treue S. Temporal dynamics of neuronal modulation during exogenous and endogenous shifts of visual attention in macaque area MT. Proc. Natl. Acad. Sci. USA 2008, 105:16380-16385.
11. Canolty R.T., Edwards E., Dalal S.S., Soltani M., Nagarajan S.S., Kirsch H.E., Berger M.S., Barbaro N.M., Knight R.T. High gamma power is phase-locked to theta oscillations in human neocortex. Science 2006, 313:1626-1628.
12. Chalk M., Herrero J.L., Gieselmann M.A., Delicato L.S., Gotthardt S., Thiele A. Attention reduces stimulus-driven gamma frequency oscillations and spike field coherence in V1. Neuron 2010, 66:114-125.
13. Colgin L.L., Denninger T., Fyhn M., Hafting T., Bonnevie T., Jensen O., Moser M.B., Moser E.I. Frequency of gamma oscillations routes flow of information in the hippocampus. Nature 2009, 462:353-357.
14. Dhamala M., Rangarajan G., Ding M. Analyzing information flow in brain networks with nonparametric Granger causality. Neuroimage 2008, 41:354-362.
15. Engel A.K., König P., Kreiter A.K., Singer W. Interhemispheric synchronization of oscillatory neuronal responses in cat visual cortex. Science 1991, 252:1177-1179.
16. Engel A.K., Kreiter A.K., König P., Singer W. Synchronization of oscillatory neuronal responses between striate and extrastriate visual cortical areas of the cat. Proc. Natl. Acad. Sci. USA 1991, 88:6048-6052.
17. Fell J., Klaver P., Lehnertz K., Grunwald T., Schaller C., Elger C.E., Fernández G. Human memory formation is accompanied by rhinal-hippocampal coupling and decoupling. Nat. Neurosci. 2001, 4:1259-1264.
18. Fries P. A mechanism for cognitive dynamics: neuronal communication through neuronal coherence. Trends Cogn. Sci. 2005, 9:474-480.
19. Fries P. Neuronal gamma-band synchronization as a fundamental process in cortical computation. Annu. Rev. Neurosci. 2009, 32:209-224.
20. Fries P., Reynolds J.H., Rorie A.E., Desimone R. Modulation of oscillatory neuronal synchronization by selective visual attention. Science 2001, 291:1560-1563.
21. Fries P., Nikolić D., Singer W. The gamma cycle. Trends Neurosci. 2007, 30:309-316.
22. Fries P., Womelsdorf T., Oostenveld R., Desimone R. The effects of visual stimulation and selective visual attention on rhythmic neuronal synchronization in macaque area V4. J. Neurosci. 2008, 28:4823-4835.
23. Gattass R., Nascimento-Silva S., Soares J.G., Lima B., Jansen A.K., Diogo A.C., Farias M.F., Botelho M.M., Mariani O.S., Azzi J., Fiorani M. Cortical visual areas in monkeys: location, topography, connections, columns, plasticity and cortical dynamics. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2005, 360:709-731.
24. Gray C.M., König P., Engel A.K., Singer W. Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties. Nature 1989, 338:334-337.
25. Gregoriou G.G., Gotts S.J., Zhou H., Desimone R. High-frequency, long-range coupling between prefrontal and visual cortex during attention. Science 2009, 324:1207-1210.
26. Henrie J.A., Shapley R. LFP power spectra in V1 cortex: the graded effect of stimulus contrast. J. Neurophysiol. 2005, 94:479-490.
27. Hipp J.F., Engel A.K., Siegel M. Oscillatory synchronization in large-scale cortical networks predicts perception. Neuron 2011, 69:387-396.
28. Hoogenboom N., Schoffelen J.M., Oostenveld R., Parkes L.M., Fries P. Localizing human visual gamma-band activity in frequency, time and space. Neuroimage 2006, 29:764-773.
29. Hoogenboom N., Schoffelen J.M., Oostenveld R., Fries P. Visually induced gamma-band activity predicts speed of change detection in humans. Neuroimage 2010, 51:1162-1167.
30. Kamiński M., Ding M., Truccolo W.A., Bressler S.L. Evaluating causal relations in neural systems: granger causality, directed transfer function and statistical assessment of significance. Biol. Cybern. 2001, 85:145-157.
31. Landau A.N., Fries P. Attention samples stimuli rhythmically. Curr. Biol. 2012, 22:1000-1004.
32. Lee H., Simpson G.V., Logothetis N.K., Rainer G. Phase locking of single neuron activity to theta oscillations during working memory in monkey extrastriate visual cortex. Neuron 2005, 45:147-156.
33. Maris E., Schoffelen J.M., Fries P. Nonparametric statistical testing of coherence differences. J. Neurosci. Methods 2007, 163:161-175.
34. Mitra P.P., Pesaran B. Analysis of dynamic brain imaging data. Biophys. J. 1999, 76:691-708.
35. Moran J., Desimone R. Selective attention gates visual processing in the extrastriate cortex. Science 1985, 229:782-784.
36. Muthukumaraswamy S.D., Edden R.A., Jones D.K., Swettenham J.B., Singh K.D. Resting GABA concentration predicts peak gamma frequency and fMRI amplitude in response to visual stimulation in humans. Proc. Natl. Acad. Sci. USA 2009, 106:8356-8361.
37. Nalatore H., Ding M., Rangarajan G. Mitigating the effects of measurement noise on Granger causality. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 2007, 75:031123.
38. Nichols T.E., Holmes A.P. Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum. Brain Mapp. 2002, 15:1-25.
39. Oostenveld R., Fries P., Maris E., Schoffelen J.M. FieldTrip: Open source software for advanced analysis of MEG, EEG, and invasive electrophysiological data. Comput. Intell. Neurosci. 2011, 2011:156869.
40. Otero-Millan J., Troncoso X.G., Macknik S.L., Serrano-Pedraza I., Martinez-Conde S. Saccades and microsaccades during visual fixation, exploration, and search: foundations for a common saccadic generator. J. Vis. 2008, 8:21-1-18.
41. Popescu A.T., Popa D., Paré D. Coherent gamma oscillations couple the amygdala and striatum during learning. Nat. Neurosci. 2009, 12:801-807.
42. Ray S., Maunsell J.H. Differences in gamma frequencies across visual cortex restrict their possible use in computation. Neuron 2010, 67:885-896.
43. Reynolds J.H., Chelazzi L. Attentional modulation of visual processing. Annu. Rev. Neurosci. 2004, 27:611-647.
44. Reynolds J.H., Chelazzi L., Desimone R. Competitive mechanisms subserve attention in macaque areas V2 and V4. J. Neurosci. 1999, 19:1736-1753.
45. Roelfsema P.R., Engel A.K., König P., Singer W. Visuomotor integration is associated with zero time-lag synchronization among cortical areas. Nature 1997, 385:157-161.
46. Rubehn B., Bosman C., Oostenveld R., Fries P., Stieglitz T. A MEMS-based flexible multichannel ECoG-electrode array. J. Neural Eng. 2009, 6:036003.
47. Schoffelen J.M., Oostenveld R., Fries P. Neuronal coherence as a mechanism of effective corticospinal interaction. Science 2005, 308:111-113.
48. Schoffelen J.M., Poort J., Oostenveld R., Fries P. Selective movement preparation is subserved by selective increases in corticomuscular gamma-band coherence. J. Neurosci. 2011, 31:6750-6758.
49. Siegel M., Donner T.H., Oostenveld R., Fries P., Engel A.K. Neuronal synchronization along the dorsal visual pathway reflects the focus of spatial attention. Neuron 2008, 60:709-719.
50. Sigurdsson T., Stark K.L., Karayiorgou M., Gogos J.A., Gordon J.A. Impaired hippocampal-prefrontal synchrony in a genetic mouse model of schizophrenia. Nature 2010, 464:763-767.
51. Singer W., Gray C.M. Visual feature integration and the temporal correlation hypothesis. Annu. Rev. Neurosci. 1995, 18:555-586.
52. Swettenham J.B., Muthukumaraswamy S.D., Singh K.D. Spectral properties of induced and evoked gamma oscillations in human early visual cortex to moving and stationary stimuli. J. Neurophysiol. 2009, 102:1241-1253.
53. Tallon-Baudry C., Bertrand O., Fischer C. Oscillatory synchrony between human extrastriate areas during visual short-term memory maintenance. J. Neurosci. 2001, 21:RC177.
54. Tallon-Baudry C., Mandon S., Freiwald W.A., Kreiter A.K. Oscillatory synchrony in the monkey temporal lobe correlates with performance in a visual short-term memory task. Cereb. Cortex 2004, 14:713-720.
55. Taylor K., Mandon S., Freiwald W.A., Kreiter A.K. Coherent oscillatory activity in monkey area v4 predicts successful allocation of attention. Cereb. Cortex 2005, 15:1424-1437.
56. Tiesinga P.H., Sejnowski T.J. Mechanisms for phase shifting in cortical networks and their role in communication through coherence. Front. Hum. Neurosci. 2010, 4:196.
57. Treue S., Maunsell J.H. Attentional modulation of visual motion processing in cortical areas MT and MST. Nature 1996, 382:539-541.
58. van Elswijk G., Maij F., Schoffelen J.M., Overeem S., Stegeman D.F., Fries P. Corticospinal beta-band synchronization entails rhythmic gain modulation. J. Neurosci. 2010, 30:4481-4488.
59. van Pelt S., Boomsma D.I., Fries P. Magnetoencephalography in twins reveals a strong genetic determination of the peak frequency of visually induced γ-band synchronization. J. Neurosci. 2012, 32:3388-3392.
60. Vinck M., Lima B., Womelsdorf T., Oostenveld R., Singer W., Neuenschwander S., Fries P. Gamma-phase shifting in awake monkey visual cortex. J. Neurosci. 2010, 30:1250-1257.
61. von Stein A., Chiang C., König P. Top-down processing mediated by interareal synchronization. Proc. Natl. Acad. Sci. USA 2000, 97:14748-14753.
62. Womelsdorf T., Fries P., Mitra P.P., Desimone R. Gamma-band synchronization in visual cortex predicts speed of change detection. Nature 2006, 439:733-736.
63. Womelsdorf T., Schoffelen J.M., Oostenveld R., Singer W., Desimone R., Engel A.K., Fries P. Modulation of neuronal interactions through neuronal synchronization. Science 2007, 316:1609-1612.
64. Zeitler M., Fries P., Gielen S. Assessing neuronal coherence with single-unit, multi-unit, and local field potentials. Neural Comput. 2006, 18:2256-2281.