title: Causal relationships between frequency bands of extracellular signals in visual cortex revealed by an information theoretic analysis.
abstract: Characterizing how different cortical rhythms interact and how their interaction changes with sensory stimulation is important to gather insights into how these rhythms are generated and what sensory function they may play. Concepts from information theory, such as Transfer Entropy (TE), offer principled ways to quantify the amount of causation between different frequency bands of the signal recorded from extracellular electrodes; yet these techniques are hard to apply to real data. To address the above issues, in this study we develop a method to compute fast and reliably the amount of TE from experimental time series of extracellular potentials. The method consisted in adapting efficiently the calculation of TE to analog signals and in providing appropriate sampling bias corrections. We then used this method to quantify the strength and significance of causal interaction between frequency bands of field potentials and spikes recorded from primary visual cortex of anaesthetized macaques, both during spontaneous activity and during binocular presentation of naturalistic color movies. Causal interactions between different frequency bands were prominent when considering the signals at a fine (ms) temporal resolution, and happened with a very short (ms-scale) delay. The interactions were much less prominent and significant at coarser temporal resolutions. At high temporal resolution, we found strong bidirectional causal interactions between gamma-band (40-100 Hz) and slower field potentials when considering signals recorded within a distance of 2 mm. The interactions involving gamma bands signals were stronger during movie presentation than in absence of stimuli, suggesting a strong role of the gamma cycle in processing naturalistic stimuli. Moreover, the phase of gamma oscillations was playing a stronger role than their amplitude in increasing causations with slower field potentials and spikes during stimulation. The dominant direction of causality was mainly found in the direction from MUA or gamma frequency band signals to lower frequency signals, suggesting that hierarchical correlations between lower and higher frequency cortical rhythms are originated by the faster rhythms.
authors.affiliation: Max Plack Institute for Biological Cybernetics, Spemannstrasse 38, 72076, Tuebingen, Germany. michel.besserve@tuebingen.mpg.de
authors.forename: Michel
authors.initials: M
authors.lastname: Besserve
authors.forename: Bernhard
authors.initials: B
authors.lastname: Schölkopf
authors.forename: Nikos K
authors.initials: NK
authors.lastname: Logothetis
authors.forename: Stefano
authors.initials: S
authors.lastname: Panzeri
mesh_terms: D000465:Algorithms; D000818:Animals; D015982:Bias; D003627:Data Interpretation, Statistical; D004569:Electroencephalography; D019277:Entropy; D005071:Evoked Potentials / Q000502:physiology*; D005110:Extracellular Space / Q000502:physiology*; D007257:Information Theory; D016014:Linear Models; D008251:Macaca; D008959:Models, Neurological; D010775:Photic Stimulation; D014793:Visual Cortex / Q000502:physiology*
references.citation: Neuroimage. 2005 Apr 1;25(2):383-94
references.pmid: 15784416
references.citation: Neural Comput. 2006 Apr;18(4):749-59
references.pmid: 16494689
references.citation: Int J Neurosci. 1987 Mar;33(1-2):33-59
references.pmid: 3610492
references.citation: Network. 1996;7(1):87-107
references.pmid: 29480146
references.citation: Nature. 1989 Mar 23;338(6213):334-7
references.pmid: 2922061
references.citation: J Neurophysiol. 2007 Mar;97(3):2533-43
references.pmid: 17202243
references.citation: Phys Rev E Stat Nonlin Soft Matter Phys. 2002 Nov;66(5 Pt 1):051903
references.pmid: 12513519
references.citation: Biophys J. 2008 Feb 1;94(3):784-802
references.pmid: 17921225
references.citation: Phys Rev E Stat Nonlin Soft Matter Phys. 2004 Jun;69(6 Pt 2):066138
references.pmid: 15244698
references.citation: Biol Cybern. 1991;65(3):203-10
references.pmid: 1912013
references.citation: Nature. 2008 Jun 12;453(7197):869-78
references.pmid: 18548064
references.citation: Neuron. 2009 Feb 26;61(4):597-608
references.pmid: 19249279
references.citation: Cereb Cortex. 2004 Mar;14(3):300-13
references.pmid: 14754869
references.citation: Curr Biol. 2008 Mar 11;18(5):375-80
references.pmid: 18328702
references.citation: Neural Comput. 2007 Apr;19(4):910-33
references.pmid: 17348767
references.citation: Neuron. 2002 Nov 14;36(4):739-50
references.pmid: 12441061
references.citation: Phys Rev E Stat Nonlin Soft Matter Phys. 2004 Nov;70(5 Pt 2):056221
references.pmid: 15600742
references.citation: J Neurosci Methods. 1993 Sep;49(3):175-9
references.pmid: 8271837
references.citation: Exp Brain Res. 1999 Nov;129(2):247-59
references.pmid: 10591899
references.citation: J Neurosci. 2003 May 15;23(10):3963-71
references.pmid: 12764080
references.citation: PLoS Comput Biol. 2008 May 30;4(5):e1000087
references.pmid: 18516243
references.citation: Hippocampus. 2005;15(7):913-22
references.pmid: 16161035
references.citation: Neuron. 2007 Sep 6;55(5):809-23
references.pmid: 17785187
references.citation: Phys Rev Lett. 2000 Jul 10;85(2):461-4
references.pmid: 10991308
references.citation: J Neurophysiol. 2003 Jul;90(1):415-30
references.pmid: 12611969
references.citation: Neuroimage. 2006 Jul 1;31(3):1051-60
references.pmid: 16545966
references.citation: J Neurophysiol. 2007 Sep;98(3):1064-72
references.pmid: 17615128
references.citation: J Neurosci Methods. 2008 Jul 15;172(1):79-93
references.pmid: 18508128
references.citation: Proc Natl Acad Sci U S A. 1993 Mar 1;90(5):2078-81
references.pmid: 8446632
references.citation: Front Syst Neurosci. 2008 Jun 17;2:2
references.pmid: 18958246
references.citation: Science. 2004 Jun 25;304(5679):1926-9
references.pmid: 15218136
references.citation: Curr Opin Neurobiol. 2001 Dec;11(6):739-44
references.pmid: 11741027
references.citation: Int J Psychophysiol. 2005 Aug;57(2):105-14
references.pmid: 15949859
references.citation: Neuron. 2002 Jan 31;33(3):325-40
references.pmid: 11832222
references.citation: Neural Comput. 2007 Nov;19(11):2913-57
references.pmid: 17883346
references.citation: J Comput Neurosci. 2005 Oct;19(2):199-221
references.pmid: 16133819
references.citation: Physiol Rev. 2003 Oct;83(4):1401-53
references.pmid: 14506309
references.citation: Phys Rev Lett. 2008 Jun 13;100(23):234101
references.pmid: 18643502
references.citation: Hippocampus. 1999;9(2):137-42
references.pmid: 10226774
references.citation: Phys Rev E Stat Nonlin Soft Matter Phys. 2006 Jun;73(6 Pt 2):066216
references.pmid: 16906955
references.citation: J Neurosci Methods. 2006 Jan 30;150(2):228-37
references.pmid: 16099512
references.citation: J Neurosci. 2008 May 28;28(22):5696-709
references.pmid: 18509031
references.citation: Proc Natl Acad Sci U S A. 2004 Jun 29;101(26):9849-54
references.pmid: 15210971
references.citation: BMC Neurosci. 2009 Jul 16;10:81
references.pmid: 19607698
references.citation: Neuroreport. 2000 Mar 20;11(4):689-92
references.pmid: 10757501
references.citation: J Physiol. 1983 Feb;335:89-100
references.pmid: 6875900
references.citation: Hippocampus. 1998;8(3):244-61
references.pmid: 9662139
references.citation: Science. 2007 Jun 15;316(5831):1609-12
references.pmid: 17569862
references.citation: Front Neurosci. 2008 Dec 15;2(2):145-54
references.pmid: 19225587
references.citation: Front Syst Neurosci. 2009 Jul 28;3:6
references.pmid: 19668700
references.citation: Brain Topogr. 1989 Fall-Winter;2(1-2):9-18
references.pmid: 2641479
references.citation: PLoS Comput Biol. 2008 Dec;4(12):e1000239
references.pmid: 19079571
references.citation: Network. 2005 Mar;16(1):35-54
references.pmid: 16350433
references.citation: Stat Med. 2007 Sep 20;26(21):3875-85
references.pmid: 17551946
references.citation: Phys Rev E Stat Phys Plasmas Fluids Relat Interdiscip Topics. 2000 May;61(5 Pt A):5142-8
references.pmid: 11031559
references.citation: Biol Cybern. 2001 Jun;84(6):463-74
references.pmid: 11417058
references.citation: Nature. 2009 Jun 4;459(7247):663-7
references.pmid: 19396156
references.citation: Nature. 2001 Jul 12;412(6843):150-7
references.pmid: 11449264
references.citation: Science. 2006 Sep 15;313(5793):1626-8
references.pmid: 16973878
references.citation: Phys Rev A Gen Phys. 1986 Sep;34(3):2427-2432
references.pmid: 9897530
references.citation: Phys Rev E Stat Nonlin Soft Matter Phys. 2006 May;73(5 Pt 1):051911
references.pmid: 16802971
references.citation: Front Integr Neurosci. 2009 May 04;3:7
references.pmid: 19503750
references.citation: Hum Brain Mapp. 1999;8(4):194-208
references.pmid: 10619414
references.citation: J Neurosci Methods. 2003 Apr 15;124(2):113-28
references.pmid: 12706841
references.citation: Neuroimage. 2005 Mar;25(1):230-42
references.pmid: 15734358