Cortical dynamics during naturalistic sensory stimulations: Experiments and models

Journal of Physiology Paris

Volumn 105, Issue 1-3, 2011, Pages 2-15

  Mazzoni, Alberto ^a   Brunel, Nicolas ^b,c,d   Cavallari, Stefano ^a   Logothetis, Nikos K ^d,e   Panzeri, Stefano ^a  

^a ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

^b CNRS   (France)

^c ISI FOUNDATION   (Italy)

^d MAX PLANCK INSTITUTE FOR BIOLOGICAL CYBERNETICS   (Germany)

^e UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Gamma band; Integrate and fire; LFP modeling; Mutual information; Natural movies; Neural code; Oscillations; Recurrent networks; Spike timing; Vision

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; AUDIOVISUAL EQUIPMENT; BINOCULAR VISION; BRAIN ELECTROPHYSIOLOGY; BRAIN FUNCTION; CONCEPTUAL FRAMEWORK; CONTROLLED STUDY; EXPERIMENTAL STUDY; GAMMA RHYTHM; LOCAL FIELD POTENTIAL; MACACA MULATTA; NERVE CELL NETWORK; NONHUMAN; OSCILLATION; QUANTITATIVE ANALYSIS; SIMULATION; SPIKE WAVE; STRIATE CORTEX; VISUAL INFORMATION; VISUAL STIMULATION;

ACTION POTENTIALS; ANIMALS; BRAIN WAVES; ELECTROENCEPHALOGRAPHY; EVOKED POTENTIALS, VISUAL; MACACA; MODELS, NEUROLOGICAL; NEURONS; PHOTIC STIMULATION; VISUAL CORTEX; VISUAL PERCEPTION;

EID: 82555166020     PISSN: 09284257     EISSN: 17697115     Source Type: Journal    
DOI: 10.1016/j.jphysparis.2011.07.014     Document Type: Article

References (107)

1. Amit J.A., Brunel N., Tsodyks M.V. Correlations of cortical Hebbian reverberations: theory versus experiment. J. Neurosci. 1994, 14(11):6435-6445.
2. Baddeley R., Abbott L.F., Booth M.C., Sengpiel F., Freeman T., Wakeman E.A., Rolls E.T. Responses of neurons in primary and inferior temporal visual cortices to natural scenes. Proc. Biol. Sci. 1997, 264(1389):1775-1783.
3. Bedard C., Kroger H., Destexhe A. Does the 1/f frequency scaling of brain signals reflect self-organized critical states?. Phys. Rev. Lett. 2006, 97(11):118102.
4. Belitski A., Gretton A., Magri C., Murayama Y., Montemurro M.A., Logothetis N.K., Panzeri S. Low-frequency local field potentials and spikes in primary visual cortex convey independent visual information. J. Neurosci. 2008, 28(22):5696-5709.
5. Belitski A., Panzeri S., Magri C., Logothetis N.K., Kayser C. Sensory information in local field potentials and spikes from visual and auditory cortices: time scales and frequency bands. J. Comput. Neurosci. 2010, 29(3):533-545.
6. Benucci A., Ringach D.L., Carandini M. Coding of stimulus sequences by population responses in visual cortex. Nat. Neurosci. 2009, 12(10):1317-1324.
7. Berens P., Keliris G.A., Ecker A.S., Logothetis N.K., Tolias A.S. Comparing the feature selectivity of the gamma-band of the local field potential and the underlying spiking activity in primate visual cortex. Front. Syst. Neurosci. 2008, 2:2.
8. Bragin A., Jando G., Nadasdy Z., Hetke J., Wise K., Buzsaki G. Gamma (40-100Hz) oscillation in the hippocampus of the behaving rat. J. Neurosci. 1995, 15(1 Pt 1):47-60.
9. Breakspear M., Jirsa V., Deco G. Computational models of the brain: from structure to function. Neuroimage 2010, 52(3):727-730.
10. Brunel N. Dynamics of sparsely connected networks of excitatory and inhibitory spiking neurons. J. Comput. Neurosci. 2000, 8(3):183-208.
11. Brunel N., Wang X.J. What determines the frequency of fast network oscillations with irregular neural discharges? I. Synaptic dynamics and excitation-inhibition balance. J. Neurophysiol. 2003, 90(1):415-430.
12. Buehlmann A., Deco G. The neuronal basis of attention: rate versus synchronization modulation. J. Neurosci. 2008, 28(30):7679-7686.
13. Bullock T.H. Signals and signs in the nervous system: the dynamic anatomy of electrical activity is probably information-rich. Proc. Natl. Acad. Sci. USA 1997, 94(1):1-6.
14. Buonomano D.V., Maass W. State-dependent computations: spatiotemporal processing in cortical networks. Nat. Rev. Neurosci. 2009, 10(2):113-125.
15. Buszaki G. Rhythms of the Brain 2006, Oxford University Press, New York.
16. Buzsaki G., Draguhn A. Neuronal oscillations in cortical networks. Science 2004, 304(5679):1926-1929.
17. Canolty R.T., Edwards E., Dalal S.S., Soltani M., Nagarajan S.S., Kirsch H.E., Berger M.S., Barbaro M.N., Knight R.T. High gamma power is phase-locked to theta oscillations in human neocortex. Science 2006, 313(5793):1626-1628.
18. Chandrasekaran C., Turesson H.K., Brown C.H., Ghazanfar A.A. The influence of natural scene dynamics on auditory cortical activity. J. Neurosci. 2010, 30(42):13919-13931.
19. Dan Y., Atick J.J., Reid R.C. Efficient coding of natural scenes in the lateral geniculate nucleus: experimental test of a computational theory. J. Neurosci. 1996, 16(10):3351-3362.
20. David F.O., Hugues E., Cenier T., Fourcaud-Trocme N., Buonviso N. Specific entrainment of mitral cells during gamma oscillation in the rat olfactory bulb. PLoS Comput. Biol. 2009, 5(10):e1000551.
21. Deco G., Jirsa V.K., Robinson P.A., Breakspear M., Friston K. The dynamic brain: from spiking neurons to neural masses and cortical fields. PLoS Comput. Biol. 2008, 4(8):e1000092.
22. Derrington A.M., Lennie P. Spatial and temporal contrast sensitivities of neurones in lateral geniculate nucleus of macaque. J. Physiol. 1984, 357:219-240.
23. Desbordes G., Jin J., Weng C., Lesica N.A., Stanley G.B., Alonso J.M. Timing precision in population coding of natural scenes in the early visual system. PLoS Biol. 2008, 6(12):e324.
24. Donoghue J.P. Bridging the brain to the world: a perspective on neural interface systems. Neuron 2008, 60(3):511-521.
25. Douglas R.J., Martin K.A. A functional microcircuit for cat visual cortex. J. Physiol. (Lond.) 1991, 440:735-769.
26. Fairhall A.L., Lewen G.D., Bialek W., de Ruyter Van Steveninck R.R. Efficiency and ambiguity in an adaptive neural code. Nature 2001, 412(6849):787-792.
27. Felsen G., Dan Y. A natural approach to studying vision. Nat. Neurosci. 2005, 8(12):1643-1646.
28. Fisher N.I. Statistical Analysis of Circular Data 1993, Cambridge University press, Cambridge.
29. Fix J., Rougier N., Alexandre F. From physiological principles to computational models of the cortex. J. Physiol. (Paris) 2007, 101(1-3):32-39.
30. Friedman-Hill S., Maldonado P.E., Gray C.M. Dynamics of striate cortical activity in the alert macaque: I. Incidence and stimulus-dependence of gamma-band neuronal oscillations. Cereb. Cortex 2000, 10(11):1105-1116.
31. Friston K.J. Bayesian estimation of dynamical systems: an application to fMRI. Neuroimage 2002, 16(2):513-530.
32. Friston K.J., Trujillo-Barreto N., Daunizeau J. DEM: a variational treatment of dynamic systems. Neuroimage 2008, 41(3):849-885.
33. Geisler W.S. Visual perception and the statistical properties of natural scenes. Annu. Rev. Psychol. 2008, 59:167-192.
34. Gieselmann M.A., Thiele A. Comparison of spatial integration and surround suppression characteristics in spiking activity and the local field potential in macaque V1. Eur. J. Neurosci. 2008, 28(3):447-459.
35. Gil Z., Amitai Y. Properties of convergent thalamocortical and intracortical synaptic potentials in single neurons of neocortex. J. Neurosci. 1996, 16(20):6567-6578.
36. Goense J.B., Logothetis N.K. Neurophysiology of the BOLD fMRI signal in awake monkeys. Curr. Biol. 2008, 18(9):631-640.
37. Goense J.B., Ku S.P., Merkle H., Tolias A.S., Logothetis N.K. FMRI of the temporal lobe of the awake monkey at 7T. Neuroimage 2008, 39(3):1081-1093.
38. Gupta A., Wang Y., Markram H. Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex. Science 2000, 287(5451):273-278.
39. Gustafsonn B. Afterpotentials and transduction properties in different types of central neurones. Arch. Ital. Biol. 1984, 122:17-30.
40. Harada Y., Takahashi T. The calcium component of the action potential in spinal motoneurons of the rat. J. Physiol. (Lond.) 1983, 335:89-100.
41. Harris K.D. Neural signatures of cell assembly organization. Nat. Rev. Neurosci. 2005, 6(5):399-407.
42. Harris K.D., Henze D.A., Hirase H., Leinekugel X., Dragoi G., Czurko A., Buzsaki G. Spike train dynamics predicts theta-related phase precession in hippocampal pyramidal cells. Nature 2002, 417(6890):738-741.
43. Hasson U., Malach R., Heeger D.J. Reliability of cortical activity during natural stimulation. Trends Cogn. Sci. 2009, 14(1):40-48.
44. He B.J., Zempel J.M., Snyder A.Z., Raichle M.E. The temporal structures and functional significance of scale-free brain activity. Neuron 2010, 66(3):353-369.
45. Henrie J.A., Shapley R. LFP power spectra in V1 cortex: the graded effect of stimulus contrast. J. Neurophysiol. 2005, 94(1):479-490.
46. Huxter J., Burgess N., O'Keefe J. Independent rate and temporal coding in hippocampal pyramidal cells. Nature 2003, 425(6960):828-832.
47. Jensen O., Colgin L.L. Cross-frequency coupling between neuronal oscillations. Trends Cogn. Sci. 2007, 11(7):267-269.
48. Jones A.K., Qi L.Y., Fujirawa T., Luthra S.K., Ashburner J., Bloomfield P., Cunningham V.J., Itoh M., Fukuda H., Jones T. In vivo distribution of opioid receptors in man in relation to the cortical projections of the medial and lateral pain systems measured with positron emission tomography. Neurosci. Lett. 1991, 126(1):25-28.
49. Kamondi A., Acsady L., Wang X.J., Buzsaki G. Theta oscillations in somata and dendrites of hippocampal pyramidal cells in vivo: activity-dependent phase-precession of action potentials. Hippocampus 1998, 8(3):244-261.
50. Katzner S., Nauhaus I., Benucci A., Bonin V., Ringach D.L., Carandini M. Local origin of field potentials in visual cortex. Neuron 2009, 61:35-41.
51. Kayser C., Konig P. Stimulus locking and feature selectivity prevail in complementary frequency ranges of V1 local field potentials. Eur. J. Neurosci. 2004, 19(2):485-489.
52. Kayser C., Montemurro M.A., Logothetis N.K., Panzeri S. Spike-phase coding boosts and stabilizes information carried by spatial and temporal spike patterns. Neuron 2009, 61(4):597-608.
53. Lakatos P., Shah A.S., Knuth K.H., Ulbert I., Karmos G., Schroeder C.E. An oscillatory hierarchy controlling neuronal excitability and stimulus processing in the auditory cortex. J. Neurophysiol. 2005, 94(3):1904-1911.
54. Lakatos P., Karmos G., Mehta A.D., Ulbert I., Schroeder C.E. Entrainment of neuronal oscillations as a mechanism of attentional selection. Science 2008, 320(5872):110-113.
55. Ledoux E., Brunel N. Dynamics of networks of excitatory and inhibitory neurons in response to time-dependent inputs. Front. Comput. Neurosci. 2011, 5.
56. 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(1):147-156.
57. Leppa M., Korvenoja A., Carlson S., Timonen P., Martinkauppi S., Ahonen J., Rosenberg P.H., Aronen H.J., Kalso E. Acute opioid effects on human brain as revealed by functional magnetic resonance imaging. Neuroimage 2006, 31(2):661-669.
58. Lisman J. The theta/gamma discrete phase code occuring during the hippocampal phase precession may be a more general brain coding scheme. Hippocampus 2005, 15(7):913-922.
59. Logothetis N.K. The neural basis of the blood-oxygen-level-dependent functional magnetic resonance imaging signal. Philos. Trans. Roy. Soc. B - Biol. Sci. 2002, 357(1424):1003-1037.
60. Logothetis N.K. The underpinnings of the BOLD functional magnetic resonance imaging signal. J. Neurosci. 2003, 23(10):3963-3971.
61. Logothetis N.K. What we can do and what we cannot do with fMRI. Nature 2008, 453(7197):869-878.
62. Logothetis N.K., Guggenberger H., Peled S., Pauls J. Functional imaging of the monkey brain. Nat. Neurosci. 1999, 2(6):555-562.
63. Logothetis N., Merkle H., Augath M., Trinath T., Ugurbil K. Ultra high-resolution fMRI in monkeys with implanted RF coils. Neuron 2002, 35(2):227-242.
64. Logothetis N.K., Murayama Y., Augath M., Steffen T., Werner J., Oeltermann A. How not to study spontaneous activity. Neuroimage 2009, 45(4):1080-1089.
65. Lund J.S., Yoshioka T., Levitt J.B. Substrates for Interlaminar Connection in Area V1 of Macaque Monkey Cerebral Cortex in Primary Visual Cortex in Primates 1994, Plenum Press, New York.
66. Lundstrom B.N., Fairhall A.L. Decoding stimulus variance from a distributional neural code of interspike intervals. J. Neurosci. 2006, 26(35):9030-9037.
67. Luo H., Poeppel D. Phase patterns of neuronal responses reliably discriminate speech in human auditory cortex. Neuron 2007, 54(6):1001-1010.
68. Magri C., Whittingstall K., Singh V., Logothetis N.K., Panzeri S. A toolbox for the fast information analysis of multiple-site LFP, EEG and spike train recordings. BMC Neurosci. 2009, 10:81.
69. Markram H., Lubke J., Frotscher M., Roth A., Sakmann B. Physiology and anatomy of synaptic connections between thick tufted pyramidal neurones in the developing rat neocortex. J. Physiol. 1997, 500(Pt 2):409-440.
70. Mazzoni A., Broccard F.D., Garcia-Perez E., Bonifazi P., Ruaro M.E., Torre V. On the dynamics of the spontaneous activity in neuronal networks. PLoS ONE 2007, 2(5):e439.
71. Mazzoni A., Panzeri S., Logothetis N.K., Brunel N. Encoding of naturalistic stimuli by local field potential spectra in networks of excitatory and inhibitory neurons. PLoS Comput. Biol. 2008, 4(12):e1000239.
72. Mazzoni A., Whittingstall K., Brunel N., Logothetis N.K., Panzeri S. Understanding the relationships between spike rate and delta/gamma frequency bands of LFPs and EEGs using a local cortical network model. Neuroimage 2010, 52(3):956-972.
73. Mehta M.R., Lee A.K., Wilson M.A. Role of experience and oscillations in transforming a rate code into a temporal code. Nature 2002, 417(6890):741-746.
74. Mitzdorf U. Current source-density method and application in cat cerebral cortex: investigation of evoked potentials and EEG phenomena. Physiol. Rev. 1985, 65(1):37-100.
75. Montemurro M.A., Panzeri S., Maravall M., Alenda A., Bale M.R., Brambilla M., Petersen R.S. Role of precise spike timing in coding of dynamic vibrissa stimuli in somatosensory thalamus. J. Neurophysiol. 2007, 98(4):1871-1882.
76. Montemurro M.A., Senatore R., Panzeri S. Tight data-robust bounds to mutual information combining shuffling and model selection techniques. Neural Comput. 2007, 19(11):2913-2957.
77. Montemurro M.A., Rasch M.J., Murayama Y., Logothetis N.K., Panzeri S. Phase-of-firing coding of natural visual stimuli in primary visual cortex. Curr. Biol. 2008, 18(5):375-380.
78. Murakami S., Okada Y. Contributions of principal neocortical neurons to magnetoencephalography and electroencephalography signals. J. Physiol. 2006, 575(Pt 3):925-936.
79. Muthukumaraswamy S.D., Singh K.D., Swettenham J.B., Jones D.K. Visual gamma oscillations and evoked responses: variability, repeatability and structural MRI correlates. Neuroimage 2010, 49(4):3349-3357.
80. Nicolelis A.L.M., Lebedev M.A. Principles of neural ensemble physiology underlying the operation of brian-machine interfaces. Nat. Rev. Neurosci. 2009, 10:530-540.
81. O'Keefe J., Recce M.L. Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 1993, 3(3):317-330.
82. Panzeri S., Petroni F., Petersen R.S., Diamond M.E. Decoding neuronal population activity in rat somatosensory cortex: role of columnar organization. Cereb. Cortex 2003, 13(1):45-52.
83. Panzeri S., Senatore R., Montemurro M.A., Petersen R.S. Correcting for the sampling bias problem in spike train information measures. J. Neurophysiol. 2007, 98(3):1064-1072.
84. Panzeri S., Magri C., Logothetis N.K. On the use of information theory for the analysis of the relationship between neural and imaging signals. Magn. Reson. Imaging 2008, 26(7):1015-1025.
85. Panzeri S., Brunel N., Logothetis N.K., Kayser C. Sensory neural codes using multiplexed temporal scales. Trends Neurosci. 2010, 33(3):111-120.
86. Percival D.B., Walden A.T. Spectral Analysis for Physical Applications: Multitaper and Conventional Univariate Techniques 1993, Cambridge University Press, Cambridge, UK.
87. Pettersen K.H., Hagen E., Einevoll G.T. Estimation of population firing rates and current source densities from laminar electrode recordings. J. Comput. Neurosci. 2008, 24(3):291-313.
88. Pfeiffer A., Pasi A., Mehraein P., Herz A. Opiate receptor binding sites in human brain. Brain Res. 1982, 248(1):87-96.
89. Rasch M.J., Gretton A., Murayama Y., Maass W., Logothetis N.K. Inferring spike trains from local field potentials. J. Neurophysiol. 2008, 99:1461-1476.
90. Ray S., Maunsell J.H. Differences in gamma frequencies across visual cortex restrict their possible use in computation. Neuron 2010, 67(5):885-896.
91. Reinagel P. How do visual neurons respond in the real world?. Curr. Opin. Neurobiol. 2001, 11(4):437-442.
92. Rust N.C., Movshon J.A. In praise of artifice. Nat. Neurosci. 2005, 8(12):1647-1650.
93. Schroeder C.E., Lakatos P. Low-frequency neuronal oscillations as instruments of sensory selection. Trends Neurosci. 2009, 32(1):9-18.
94. Schyns P.G., Thut G., Gross J. Cracking the code of oscillatory activity. PLoS Biol. 2011, 9(5):e1001064.
95. Senkowski D., Gomez-Ramirez M., Lakatos P., Wylie G.R., Molholm S., Schroeder C.E., Foxe J.J. Multisensory processing and oscillatory activity: analyzing non-linear electrophysiological measures in humans and simians. Exp. Brain Res. 2007, 177(2):184-195.
96. Sereno M.E., Trinath T., Augath M., Logothetis N.K. Three-dimensional shape representation in monkey cortex. Neuron 2002, 33(4):635-652.
97. Shapley R., Kaplan E., Soodak R. Spatial summation and contrast sensitivity of X and Y cells in the lateral geniculate nucleus of the macaque. Nature 1981, 292:543-545.
98. Simoncelli E.P. Vision and the statistics of the visual environment. Curr. Opin. Neurobiol. 2003, 13(2):144-149.
99. Smyth D., Willmore B., Baker G.E., Thompson I.D., Tolhurst D.J. The receptive-field organization of simple cells in primary visual cortex of ferrets under natural scene stimulation. J. Neurosci. 2003, 23(11):4746-4759.
100. 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(2):1241-1253.
101. Talbot J.D., Marrett S., Evans A.C., Meyer E., Bushnell M.C., Duncan G.H. Multiple representations of pain in human cerebral cortex. Science 1991, 251(4999):1355-1358.
102. Treves A., Panzeri S., Rolls E.T., Booth M., Wakeman E.A. Firing rate distributions and efficiency of information transmission of inferior temporal cortex neurons to natural visual stimuli. Neural Comput. 1999, 11(3):601-632.
103. Tuckwell H.C. Introduction to Theoretical Neurobiology 1988, Cambridge University Press, Cambridge, UK.
104. de Ruyter van Steveninck R.R., Lewen G.D., Strong S.P., Koberle R., Bialek W. Reproducibility and variability in neural spike trains. Science 1997, 275(5307):1805-1808.
105. Whittingstall K., Logothetis N.K. Frequency-band coupling in surface EEG reflects spiking activity in monkey visual cortex. Neuron 2009, 64(2):281-289.
106. Zappe A.C., Uludag K., Logothetis N.K. Direct measurement of oxygen extraction with fMRI using 6% CO2 inhalation. Magn. Reson. Imaging 2008, 26(7):961-967.
107. Zappe A.C., Uludag K., Oeltermann A., Ugurbil K., Logothetis N.K. The influence of moderate hypercapnia on neural activity in the anesthetized nonhuman primate. Cereb. Cortex 2008, 18(11):2666-2673.