Stimulus detection rate and latency, firing rates and 1-40Hz oscillatory power are modulated by infra-slow fluctuations in a bistable attractor network model

NeuroImage

Volumn 83, Issue , 2013, Pages 458-471

  Lundqvist, Mikael ^a,b   Herman, Pawel ^a,b   Palva, Matias ^c   Palva, Satu ^c   Silverstein, David ^a,b   Lansner, Anders ^a,b  

^a ROYAL INSTITUTE OF TECHNOLOGY   (Sweden)

^b STOCKHOLM UNIVERSITY   (Sweden)

^c UNIVERSITY OF HELSINKI   (Finland)

Author keywords

Attractor network; Computational model; Detection rate; Oscillation; Slow fluctuation; Threshold stimulus detection task

Indexed keywords

ARTICLE; ATTRACTOR NETWORK; BETA RHYTHM; BRAIN FUNCTION; DELTA RHYTHM; FIRING RATE; GAMMA RHYTHM; INFRA SLOW FLUCTUATION; LATENT PERIOD; NERVE CELL NETWORK; NERVOUS SYSTEM PARAMETERS; NEUROMODULATION; NEURONAL OSCILLATION; PRIORITY JOURNAL; PSYCHOPHYSICS; RESPONSE TIME; SENSORY STIMULATION; STIMULUS DETECTION; STIMULUS RESPONSE; TASK PERFORMANCE; THETA RHYTHM; ACTION POTENTIAL; ANIMAL; BIOLOGICAL MODEL; BIOLOGICAL RHYTHM; COMPUTER SIMULATION; FEEDBACK SYSTEM; HUMAN; NERVE CELL; OSCILLOMETRY; PHYSIOLOGY; PROCEDURES; REACTION TIME; SYNAPTIC TRANSMISSION;

ACTION POTENTIALS; ANIMALS; BIOLOGICAL CLOCKS; COMPUTER SIMULATION; FEEDBACK, PHYSIOLOGICAL; HUMANS; MODELS, NEUROLOGICAL; NERVE NET; NEURONS; OSCILLOMETRY; REACTION TIME; SYNAPTIC TRANSMISSION;

EID: 84881227115     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2013.06.080     Document Type: Article

References (99)

1. Aladjalova N.A. Infra-slow rhythmic oscillations of the steady potential of the cerebral cortex. Nature 1957, 179:957-959.
2. Albrecht D., Gabriel S. Very slow oscillations of activity in geniculate neurones of urethane-anaesthetized rats. Neuroreport 1994, 5:1909-1912.
3. Allers K.A., Ruskin D.N., Bergstrom D.A., Freeman L.E., Ghazi L.J., Tierney P.L., Walters J.R. Multisecond periodicities in basal ganglia firing rates correlate with theta bursts in transcortical and hippocampal EEG. J. Neurophysiol. 2002, 87:1118-1122.
4. Amit D.J., Brunel N. Model of global spontaneous activity and local structured activity during delay periods in cerebral cortex. Cereb. Cortex 1997, 7:237-252.
5. Beck D.B., Kastner S. Top-down and bottom-up mechanisms in biasing competition in human brain. Vision Res. 2009, 49:1154-1165.
6. Binzegger T., Douglas R.J., Martin K.A.C. Topology and dynamics of the canonical circuit of cat V1. Neural Netw. 2009, 22:1071-1078.
7. Biswal B., Yetkin F.Z., Haughton V.M., Hyde J.S. Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn. Reson. Med. 1995, 34:537-541.
8. Bollimunta A., Chen Y., Schroeder C.E., Ding M. Neural mechanisms of cortical alpha oscillations in awake-behaving macaques. J. Neurosci. 2008, 28:9976-9988.
9. Bollimunta A., Mo J., Schroeder C.E., Ding M. Neuronal mechanisms and attentional modulation of corticothalamic alpha oscillations. J. Neurosci. 2011, 31:4935-4943.
10. Brookes M.J., Woolrich M., Luckhoo H., Price D., Hale J.R., Stephenson M.C., Barnes G.R., Smith S.M., Morris P.G. Investigating the electrophysiological basis of resting state networks using magnetoencephalography. Proc. Natl. Acad. Sci. 2011, 108:16783-16788.
11. Brunel N., Hakim V. Fast global oscillations in networks of integrate-and-fire neurons with low firing rates. Neural Comput. 1999, 11:1621-1671.
12. 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, 90:415-430.
13. Bruns A., Eckhorn R. Task-related coupling from high- to low-frequency signals among visual cortical areas in human subdural recordings. Int. J. Psychophysiol. 2004, 51:97-116.
14. Buffalo A.E., Fries P., Landman R., Buschman T.J., Desimone R. Laminar differences in gamma and alpha coherence in the ventral stream. Proc. Natl. Acad. Sci. 2011, 108:11262-11267.
15. Canolty R.T., Edwards E., Dalai 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.
16. Carnevale N.T., Hines M.L. The Neuron Book 2006, Cambridge University Press.
17. Chrobak J.J., Buszaki G. Gamma oscillations in the entorhinal cortex of the freely behaving rat. J. Neurosci. 1998, 18:388-398.
18. Deco G., Jirsa V. Ongoing cortical activity at rest: criticality, multistability, and ghost attractors. J. Neurosci. 2012, 32:3366-3375.
19. Deco G., Thiele A. Attention - oscillations and neuropharmacology. Eur. J. Neurosci. 2009, 30:347-354.
20. Deco G., Jirsa V., McIntosh A.R., Sporns O., Kötter R. Key role of coupling, delay, and noise in resting brain fluctuations. Proc. Natl. Acad. Sci. 2009, 106:10302-10307.
21. Dehaene S., Changeux J.-P. Experimental and theoretical approaches to conscious processing. Neuron 2011, 70:200-227.
22. Dehaene S., Changeux J.-P., Naccache L., Saccur J., Sergent C. Conscious, preconscious, and subliminal processing: a testable taxonomy. TICS 2006, 10:204-211.
23. Djurfeldt M., Lundqvist M., Johansson C., Rehn M., Ekeberg Ö., Lansner A. Brain-scale simulation of the neocortex on the IBM Blue Gene/L supercomputer. IBM J. Res. Dev. 2008, 52:31-41.
24. Fisher N.I. Statistical Analysis of Circular Data 1995, Cambridge UP, Cambridge, UK.
25. Fransén E., Lansner A. Low spiking rates in a population of mutually exciting pyramidal cells. Network 1995, 6:271-288.
26. Fransson P. Spontaneous low-frequency BOLD signal fluctuations: an fMRI investigation of the resting-state default mode of brain function hypothesis. Hum. Brain Mapp. 2005, 26:15-29.
27. Freyer F., Aquino K., Robinson P.A., Ritter P., Breakspear M. Bistability and non-Gaussian fluctuations in spontaneous cortical activity. J. Neurosci. 2009, 29:8512-8524.
28. 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.
29. Ghosh A., Rho Y., McIntosh A.R., Kötter R., Jirsa V.K. Noise during rest enables the exploration of the brain's dynamic repertoire. PLoS Comput. Biol. 2008, 4:e1000196. 10.1371/journal.pcbi.1000196.
30. Girard P., Hupé J.M., Bullier J. Feedforward and feedback connections between areas V1 and V2 of the monkey have similar rapid conduction velocities. J. Neurophysiol. 2001, 85:1328-1331.
31. Goldman R.I., Stern J.M., Engel J., Cohen M.S. Simultaneous EEG and fMRI of the alpha rhythm. Neuroreport 2002, 13:2487-2492.
32. Greicius M.D., Krasnow B., Reiss A.L., Menon V. Functional connectivity in the resting brain: a network analysis of the default mode hypothesis. Proc. Natl. Acad. Sci. 2003, 100:253-258.
33. Hanslmayr S., Aslan A., Staudigl T., Klimesch W., Herrmann C.S., Bäuml K.-H. Prestimulus oscillations predict visual perception performance between and within subjects. Neuroimage 2007, 37:1465-1473.
34. Honey J.C., Kötter R., Breakespear M., Sporns O. Network structure of cerebral cortex shapes functional connectivity on multiple time scales. Proc. Natl. Acad. Sci. 2007, 104:10240-10245.
35. Hughes S.W., Crunelli V. Thalamic mechanisms of EEG alpha rhythms and their pathological implications. Neuroscientist 2005, 11:357-372.
36. Hughes S.W., Lorincz M.L., Parri H.R., Crunelli V. Infraslow (<0.1Hz) oscillations in thalamic relay nuclei basic mechanisms and significance to health and disease states. Prog. Brain Res. 2011, 193:145-162.
37. Jones S.R., Pinto D.J., Kaper T.J., Kopell N. Alpha-frequency rhythms desynchronize over long cortical distances: a modeling study. J. Comput. Neurosci. 2000, 27:271-291.
38. Jones S.R., Pritchett D.L., Stufflebeam S.M., Hamalainen M., Moore C.I. Neural correlates of tactile detection: a combined MEG and biophysically based computational modeling study. J. Neurosci. 2007, 27:10751-10764.
39. Jones S.R., Pritchett D.L., Sikora M.A., Stufflebeam S.M., Hämäläinen M., Moore C.I. Quantitative analysis and biophysically realistic neural modeling of the MEG Mu rhythm: rhythmogenesis and modulation of sensory-evoked responses. J. Neurophysiol. 2009, 102:3554-3572.
40. Kampa B.M., Letzkus J.J., Stuart G.J. Cortical feed-forward networks for binding different streams of sensory information. Nat. Neurosci. 2006, 9:1472-1473.
41. Karameh F.N., Dahleh M.A., Brown E.N., Massaquoi S.G. Modeling the contribution of lamina 5 neuronal and network dynamics to low frequency EEG phenomena. Biol. Cybern. 2006, 95:289-310.
42. Kendrick K.M., Zhan Y., Fisher H., Nicol A.U., Zhang X., Feng J. Learning alters the theta amplitude, theta-gamma coupling and neural synchronization in inferotemporal cortex. BMC Neurosci. 2011, 12:55.
43. Klausberger T., Somogyi P. Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. Science 2008, 321:53-57.
44. Klimesch W. EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis. Brain Res. Rev. 1999, 29:169-195.
45. Klimesch W., Sauseng P. EEG alpha oscillations: the inhibition-timing hypothesis. Brain Res. Rev. 2007, 53:63-88.
46. Krishnamurthy P., Silberberg G., Lansner A. A cortical attractor network with Martinotti cells driven by facilitating synapses. PLoS One 2012, 7:e30752. 10.1371/journal.pone.0030752.
47. Lachaux J.P., Rodriguez E., Martinerie J., Varela F.J. Measuring phase synchrony in brain signals. Hum. Brain Mapp. 1999, 8:194-208.
48. 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, 94:1904-1911.
49. Lee T.S., Yang C.F., Romero R.D., Mumford D. Neural activity in early visual cortex reflects behavioral experience and higher-order perceptual saliency. Nat. Neurosci. 2002, 5:589-597.
50. Leopold D.A., Murayama Y., Logothetis N.K. Very slow activity fluctuations in monkey visual cortex: implications for functional brain imaging. Cereb. Cortex 2003, 13:422-433.
51. Linkenkaer-Hansen K., Nikouline V.V., Palva J.M., Ilmoniemi R.J. Long-range temporal correlations and scaling behavior in human brain oscillations. J. Neurosci. 2001, 21:1370-1371.
52. Linkenkaer-Hansen K., Nikulin V.V., Palva S., Ilmoniemi R.J., Palva M. Prestimulus oscillations enhance psychophysical performance in humans. J. Neurosci. 2004, 24:10186-10190.
53. Lörincz M.L., Geall F., Bao Y., Crunelli V., Huges S.W. ATP-dependent infra-slow (<0.2Hz) oscillations in thalamic networks. PLoS One 2009, 4:e4447.
54. Lundqvist M., Rehn M., Djurfeldt M., Lansner A. Attractor dynamics in a modular network model of neocortex. Network 2006, 17:253-276.
55. Lundqvist M., Compte A., Lansner A. Bistable, irregular firing and population oscillations in a modular attractor memory network. PLoS Comput. Biol. 2010, 6:e1000803. 10.1371/journal.pcbi.1000803.
56. Lundqvist M., Herman P., Lansner A. Theta and gamma power increases and alpha/beta power decreases with memory load in an attractor network model. J. Cogn. Neurosci. 2011, 23:3008-3020.
57. Lundqvist M., Herman P., Lansner A. Variability of spike firing during theta-coupled replay of memories in a simulated attractor network. Brain Res. 2012, 1434:152-161.
58. Mantini D., Perrucci M.G., Del Gratta C., Romani G.L., Corbetta M. Electrophysiological signatures of resting state networks in the human brain. Proc. Natl. Acad. Sci. 2007, 104:13170-13175.
59. Mo J., Schroeder C.E., Ding M. Attentional modulation of alpha oscillations in macaque inferotemporal cortex. J. Neurosci. 2011, 31:878-882.
60. Monto S., Palva S., Voipio J., Palva J.M. Very slow EEG fluctuations predict the dynamics of stimulus detection and oscillation amplitudes in humans. J. Neurosci. 2008, 28:8268-8272.
61. Muir D.R., Da Costa N.M.A., Girardin C.C., Naaman S., Omer D.B., Ruesch E., Grinvald A., Douglas R.J. Embedding of cortical representations by the superficial patch system. Cereb. Cortex 2011, 10.1093/cercor/bhq290.
62. Nir Y., Mukamel R., Dinstein I., Privman E., Harel M., Fisch L., Gelbard-Sagiv H., Kipervasser S., Andelman F., Neufeld M.Y., Kramer U., Arieli A., Fried I., Malach R. Interhemispheric correlations of slow spontaneous neuronal fluctuations revealed in human sensory cortex. Nat. Neurosci. 2008, 11:1100-1108.
63. Norton S., Jewett R.E. Frequencies of slow potential oscillations in the cortex of cats. Electroencephalogr. Clin. Neurophysiol. 1965, 19:377-386.
64. Okun M., Naim A., Lampl I. The subthreshold relation between cortical local field potential and neuronal firing unveiled by intracellular recordings in awake rats. J. Neurosci. 2010, 30:4440-4448.
65. 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, 10.1155/2011/156869.
66. Palva S., Palva J.M. New vistas for alpha-frequency band oscillations. Trends Neurosci. 2007, 30:150-158.
67. Palva J.M., Palva S. Infra-slow fluctuations in electrophysiological recordings, blood-oxygenation-level-dependent signals, and psychophysical time series. Neuroimage 2012, 62:2201-2211.
68. Palva J.M., Palva S., Kaila K. Phase synchrony among neuronal oscillations in the human cortex. J. Neurosci. 2005, 25:3962-3972.
69. Palva S., Linkenkaer-Hansen K., Näätänen Palva J.M. Early neural correlates of conscious somatosensory perception. J. Neurosci. 2005, 25:5248-5258.
70. Palva J.M., Monto S., Kulashekhar S., Palva S. Neural synchrony reveals working memory networks and predicts individual memory capacity. Proc. Natl. Acad. Sci. 2010, 107:7580-7585.
71. Penttonen M., Nurminen N., Miettinen R., Sirviö J., Henze D.A., Csicsvári J., Buszáki G. Ultra-slow oscillation (0.025Hz) triggers hippocampal afterdischarges in Wistar rats. Neuroscience 1999, 94:735-743.
72. Peters A., Yilmaz E. Neurological organization in area 17 of cat visual cortex. Cereb. Cortex 1993, 3:49-68.
73. Pfurtscheller G., Stancák A., Neuper C. Event-related synchronization (ERS) in the alpha band: an electrophysiological correlate of cortical idling. Int. J. Psychophysiol. 1996, 24:39-46.
74. Power J.D., Cohen A.L., Nelson S.M., Gagan S.W., Barnes K.A., Church J.A., Vogel A.C., Laumann T.O., Miezen F.M., Schlaggar B.L., Petersen S.E. Functional network organization of the human brain. Neuron 2011, 72:665-678.
75. Rajagovianan R., Ding M. From prestimulus alpha oscillation to visual-evoked response: an inverted-U function and its attentional modulation. J. Cogn. Neurosci. 2010, 23:1379-1394.
76. Robinson P.A., Rennie C.J., Wright J.J. Propagation and stability of waves of electrical activity in the cerebral cortex. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 1997, 56:826-840.
77. Robinson P.A., Rennie C.J., Wright J.J., Bahramali H., Gordon E., Rowe D.L. Prediction of electroencephalographic spectra from neurophysiology. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 2001, 63:1-18.
78. Rotstein H.G., Pervouchine D.D., Acker C.D., Gillies M.J., White J.A., Buhl E.H., Whittington M.A., Kopell N. Slow and fast inhibition and an H-current interact to create a theta rhythm in a model of CA1 interneuron network. J. Neurophysiol. 2005, 107:1509-1518.
79. Ruskin D.N., Bergstrom D.A., Tierney P.L., Walters J.R. Correlated multisecond oscillations in firing rate in the basal ganglia: modulation by dopamine and the subthalamic nucleus. Neuroscience 2003, 117:427-438.
80. Sadaghiani S., Hesselmann G., Kleinschmidt A. Distributed and antagonistic contributions of ongoing activity fluctuations of auditory stimulus detection. J. Neurosci. 2009, 29:13410-13417.
81. Sadaghiani S., Scheeringa R., Lehongre K., Morillion B., Giraud A.-L., Kleinschmidt A. Intrinsic connectivity networks, alpha oscillations and tonic alertness: a simultaneous electroencephalography/functional magnetic resonance imaging study. J. Neurosci. 2010, 30:40243-40250.
82. Silva L.R., Amitai Y., Connors B.W. Intrinsic oscillations of neocortex generated by layer 5 pyramidal neurons. Science 1991, 251:432-435.
83. Silverstein D., Lansner A. Is attentional blink a byproduct of neocortical attractors?. Front. Comput. Neurosci. 2011, 5:1-14.
84. Slepian D., Pollak H.O. Prolate spheroidal wave functions: Fourier analysis and uncertainty I. Bell Syst. Tech. J. 1961, 40:43-63.
85. Smerieri A., Rolls E.T., Feng J. Decision time, slow inhibition, and theta rhythm. J. Neurosci. 2010, 30:14173-14181.
86. Thomson D. Spectrum estimation and harmonic analysis. Proc. IEEE 1982, (70):1055-1096.
87. Thomson A.M., West D.C., Wang Y., Bannister A.P. Synaptic connections and small circuits involving excitatory and inhibitory neurons in layers 2-5 of adult rat and cat neocortex: triple intracellular recordings and biocytin labelling in vitro. Cereb. Cortex 2002, 12:936-953.
88. Tsodyks M., Pawelzik K., Markram H. Neural networks with dynamical synapses. Neural Comput. 1998, 10:821-835.
89. Ursino M., La Cara G. Travelling waves and EEG patterns during epileptic seizure: analysis with an integrate and fire neuron. J. Theor. Biol. 2006, 242:171-187.
90. Vanhatalo S., Palva J.M., Holmes M.D., Miller J.W., Voipio J., Kaila K. Infraslow oscillations modulate excitability and interictal epileptic activity in the human cortex during sleep. Proc. Natl. Acad. Sci. 2004, 101:5053-5057.
91. Vieerling-Claassen D., Cardin J.A., Moore C.I., Jones S.R. Computational modeling of distinct neocortical oscillations driven by cell-type selective optogenetic drive: separable resonant circuits controlled by low-threshold spiking and fast-spiking interneurons. Front. Hum. Neurosci. 2010, 4:198.
92. Vinck M., Battaglia F.P., Womelsdorf T., Pennartz C. Improved measures of phase-coupling between spikes and the local field potential. J. Comput. Neurosci 2011, 10.1007/s10827-011-0374-4.
93. Weiler N., Wood L., Yu J., Solla S.A., Shepherd G.M.G. Top-down laminar organization of the excitatory network in motor cortex. Nat. Neurosci. 2008, 11:360-366.
94. Werner G., Mountcastle V.B. The variability of central neural activity in a sensory system, and its implications for the central reflection of sensory events. J. Neurophysiol. 1963, 26:958-977.
95. White J.A., Banks M.I., Pearce R.A., Kopell N.J. Networks of interneurons with fast and slow gamma-aminobutyric acid type A (GABAA) kinetics provide substrate for mixed gamma-theta rhythm. Proc. Natl. Acad. Sci. 2000, 97:8128-8133.
96. Whittington M.A., Traub R.D., Kopell N., Ermentrout B., Buhl E.H. Inhibition-based rhythms: experimental and mathematical observations on network dynamics. Int. J. Psychophysiol. 2000, 38:315-336.
97. Yoshimura Y., Dantzker J.L., Callaway E.M. Excitatory cortical neurons form fine-scale functional networks. Nature 2005, 433:868-873.
98. Yuan K., Fink K.L., Winer J.A., Schreiner C.E. Local connection patterns of parvalbumin-positive inhibitory interneurons in rat primary auditory cortex. Hear. Res. 2011, 274:121-128.
99. Zhang Y., Wang X., Bressler S.L., Chen Y., Ding M. Prestimulus cortical activity is correlated with speed of visuomotor processing. J. Cogn. Neurosci. 2008, 20:1915-1925.