Attentional Modulation of Cell-Class-Specific Gamma-Band Synchronization in Awake Monkey Area V4

Neuron

Volumn 80, Issue 4, 2013, Pages 1077-1089

  Vinck, Martin ^a,b,c   Womelsdorf, Thilo ^b,d   Buffalo, Elizabeth A ^e   Desimone, Robert ^f   Fries, Pascal ^a,b  

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

^b RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^c UNIVERSITY OF AMSTERDAM   (Netherlands)

^d YORK UNIVERSITY   (Canada)

^e UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^f MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN NERVE CELL; CELL FUNCTION; CELL SYNCHRONIZATION; CELL TYPE; GAMMA RHYTHM; HAPLORHINI; NONHUMAN; PRIORITY JOURNAL; SELECTIVE ATTENTION; TASK PERFORMANCE; VISUAL AREA V4; VISUAL CORTEX; VISUAL STIMULATION;

ANIMALS; ATTENTION; ELECTRODES, IMPLANTED; ELECTROENCEPHALOGRAPHY PHASE SYNCHRONIZATION; ELECTROPHYSIOLOGICAL PROCESSES; FIXATION, OCULAR; INTERNEURONS; MACACA; NERVE NET; PHOTIC STIMULATION; PYRAMIDAL CELLS; SPACE PERCEPTION; VISUAL CORTEX; VISUAL PERCEPTION;

EID: 84888062272     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2013.08.019     Document Type: Article

References (52)

1. Barthó P., Hirase H., Monconduit L., Zugaro M., Harris K.D., Buzsáki G. Characterization of neocortical principal cells and interneurons by network interactions and extracellular features. J.Neurophysiol. 2004, 92:600-608.
2. Bartos M., Vida I., Jonas P. Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks. Nat. Rev. Neurosci. 2007, 8:45-56.
3. Bollimunta A., Chen Y., Schroeder C.E., Ding M. Neuronal mechanisms of cortical alpha oscillations in awake-behaving macaques. J.Neurosci. 2008, 28:9976-9988.
4. Börgers C., Kopell N. Effects of noisy drive on rhythms in networks of excitatory and inhibitory neurons. Neural Comput. 2005, 17:557-608.
5. Bosman C.A., Schoffelen J.M., Brunet N., Oostenveld R., Bastos A.M., Womelsdorf T., Rubehn B., Stieglitz T., De Weerd P., Fries P. Attentional stimulus selection through selective synchronization between monkey visual areas. Neuron 2012, 75:875-888.
6. Branco T., Clark B.A., Häusser M. Dendritic discrimination of temporal input sequences in cortical neurons. Science 2010, 329:1671-1675.
7. 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.
8. 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.
9. Buzsáki G., Wang X.J. Mechanisms of gamma oscillations. Annu. Rev. Neurosci. 2012, 35:203-225.
10. 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.
11. 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.
12. Cobb S.R., Buhl E.H., Halasy K., Paulsen O., Somogyi P. Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons. Nature 1995, 378:75-78.
13. Connors B.W., Gutnick M.J. Intrinsic firing patterns of diverse neocortical neurons. Trends Neurosci. 1990, 13:99-104.
14. Contreras D., Palmer L. Response to contrast of electrophysiologically defined cell classes in primary visual cortex. J.Neurosci. 2003, 23:6936-6945.
15. Csicsvari J., Hirase H., Czurkó A., Mamiya A., Buzsáki G. Oscillatory coupling of hippocampal pyramidal cells and interneurons in the behaving Rat. J.Neurosci. 1999, 19:274-287.
16. 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.
17. Lopes da Silva F.H., van Lierop T.H., Schrijer C.F., van Leeuwen W.S. Organization of thalamic and cortical alpha rhythms: spectra and coherences. Electroencephalogr. Clin. Neurophysiol. 1973, 35:627-639.
18. Eeckman F.H., Freeman W.J. Correlations between unit firing and EEG in the rat olfactory system. Brain Res. 1990, 528:238-244.
19. Engel A.K., Fries P., Singer W. Dynamic predictions: oscillations and synchrony in top-down processing. Nat. Rev. Neurosci. 2001, 2:704-716.
20. Fries P., Neuenschwander S., Engel A.K., Goebel R., Singer W. Rapid feature selective neuronal synchronization through correlated latency shifting. Nat. Neurosci. 2001, 4:194-200.
21. Fries P., Reynolds J.H., Rorie A.E., Desimone R. Modulation of oscillatory neuronal synchronization by selective visual attention. Science 2001, 291:1560-1563.
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. 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.
24. 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.
25. Grothe I., Neitzel S.D., Mandon S., Kreiter A.K. Switching neuronal inputs by differential modulations of gamma-band phase-coherence. J.Neurosci. 2012, 32:16172-16180.
26. Gulyás A.I., Szabó G.G., Ulbert I., Holderith N., Monyer H., Erdélyi F., Szabó G., Freund T.F., Hájos N. Parvalbumin-containing fast-spiking basket cells generate the field potential oscillations induced by cholinergic receptor activation in the hippocampus. J.Neurosci. 2010, 30:15134-15145.
27. Hasenstaub A., Shu Y., Haider B., Kraushaar U., Duque A., McCormick D.A. Inhibitory postsynaptic potentials carry synchronized frequency information in active cortical networks. Neuron 2005, 47:423-435.
28. Havenith M.N., Yu S., Biederlack J., Chen N.H., Singer W., Nikolić D. Synchrony makes neurons fire in sequence, and stimulus properties determine who is ahead. J.Neurosci. 2011, 31:8570-8584.
29. Henrie J.A., Shapley R. LFP power spectra in V1 cortex: the graded effect of stimulus contrast. J.Neurophysiol. 2005, 94:479-490.
30. Klausberger T., Magill P.J., Márton L.F., Roberts J.D., Cobden P.M., Buzsáki G., Somogyi P. Brain-state- and cell-type-specific firing of hippocampal interneurons invivo. Nature 2003, 421:844-848.
31. Kremkow J., Aertsen A., Kumar A. Gating of signal propagation in spiking neural networks by balanced and correlated excitation and inhibition. J.Neurosci. 2010, 30:15760-15768.
32. Leung L.S. Nonlinear feedback model of neuronal populations in hippocampal CAl region. J.Neurophysiol. 1982, 47:845-868.
33. Livingstone M.S. Oscillatory firing and interneuronal correlations in squirrel monkey striate cortex. J.Neurophysiol. 1996, 75:2467-2485.
34. Maris E., Womelsdorf T., Desimone R., Fries P. Rhythmic neuronal synchronization in visual cortex entails spatial phase relation diversity that is modulated by stimulation and attention. Neuroimage 2013, 74:99-116.
35. McCormick D.A., Connors B.W., Lighthall J.W., Prince D.A. Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. J.Neurophysiol. 1985, 54:782-806.
36. Mitchell J.F., Sundberg K.A., Reynolds J.H. Differential attention-dependent response modulation across cell classes in macaque visual area V4. Neuron 2007, 55:131-141.
37. Nolte G., Ziehe A., Nikulin V.V., Schlögl A., Krämer N., Brismar T., Müller K.R. Robustly estimating the flow direction of information in complex physical systems. Phys. Rev. Lett. 2008, 100:234101.
38. Nowak L.G., Azouz R., Sanchez-Vives M.V., Gray C.M., McCormick D.A. Electrophysiological classes of cat primary visual cortical neurons invivo as revealed by quantitative analyses. J.Neurophysiol. 2003, 89:1541-1566.
39. Phillips J.M., Vinck M., Everling S., Womelsdorf T. A long-range fronto-parietal 5- to 10-Hz network predicts "top-down" controlled guidance in a task-switch paradigm. Cereb. Cortex 2013, 10.1093/cercor/bht050.
40. Ray S., Maunsell J.H.R. Differences in gamma frequencies across visual cortex restrict their possible use in computation. Neuron 2010, 67:885-896.
41. 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.
42. Sohal V.S., Zhang F., Yizhar O., Deisseroth K. Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature 2009, 459:698-702.
43. Tiesinga P., Sejnowski T.J. Cortical enlightenment: are attentional gamma oscillations driven by ING or PING?. Neuron 2009, 63:727-732.
44. Tukker J.J., Fuentealba P., Hartwich K., Somogyi P., Klausberger T. Cell type-specific tuning of hippocampal interneuron firing during gamma oscillations invivo. J.Neurosci. 2007, 27:8184-8189.
45. van Wingerden M., Vinck M., Lankelma J.V., Pennartz C.M. Learning-associated gamma-band phase-locking of action-outcome selective neurons in orbitofrontal cortex. J.Neurosci. 2010, 30:10025-10038.
46. 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.
47. Vinck M., van Wingerden M., Womelsdorf T., Fries P., Pennartz C.M.A. The pairwise phase consistency: a bias-free measure of rhythmic neuronal synchronization. Neuroimage 2010, 51:112-122.
48. 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.
49. Wang X.J., Buzsáki G. Gamma oscillation by synaptic inhibition in a hippocampal interneuronal network model. J.Neurosci. 1996, 16:6402-6413.
50. 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.
51. Wilson H.R., Cowan J.D. Excitatory and inhibitory interactions in localized populations of model neurons. Biophys. J. 1972, 12:1-24.
52. 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.