From Prestimulus Alpha Oscillation to Visual-evoked Response: An Inverted-U Function and Its Attentional Modulation

Journal of Cognitive Neuroscience - Tập 23 Số 6 - Trang 1379-1394 - 2011
Rajasimhan Rajagovindan1, Mingzhou Ding
1University of Florida, Gainesville, FL 32611, USA

Tóm tắt

Abstract Understanding the relation between prestimulus neural activity and subsequent stimulus processing has become an area of active investigation. Computational modeling, as well as in vitro and in vivo single-unit recordings in animal preparations, have explored mechanisms by which background synaptic activity can influence the responsiveness of cortical neurons to afferent input. How these mechanisms manifest in humans is not well understood. Although numerous EEG/MEG studies have considered the role of prestimulus alpha oscillations in the genesis of visual-evoked potentials, no consensus has emerged, and divergent reports continue to appear. The present work addresses this problem in three stages. First, a theoretical model was developed in which the background synaptic activity and the firing rate of a neural ensemble are related through a sigmoidal function. The derivative of this function, referred to as local gain, has an inverted-U shape and is postulated to be proportional to the trial-by-trial response evoked by a transient stimulus. Second, the theoretical model was extended to noninvasive studies of human visual processing, where the model variables are reinterpreted in terms of ongoing EEG oscillations and event-related potentials. Predictions were derived from the model and tested by recording high-density scalp EEG from healthy volunteers performing a trial-by-trial cued spatial visual attention task. Finally, enhanced stimulus processing by attention was linked to an increase in the overall slope of the sigmoidal function. The commonly observed reduction of alpha magnitude with attention was interpreted as signaling a shift of the underlying neural ensemble toward an optimal excitability state that enables the increase in global gain.

Từ khóa


Tài liệu tham khảo

Abbott, 1997, Synaptic depression and cortical gain control., Science, 275, 220, 10.1126/science.275.5297.221

Araya, 2006, Dendritic spines linearize the summation of excitatory potentials., Proceedings of the National Academy of Sciences, U.S.A., 103, 18799, 10.1073/pnas.0609225103

Babiloni, 2006, Pre- and poststimulus alpha rhythms are related to conscious visual perception: A high-resolution EEG study., Cerebral Cortex, 16, 1690, 10.1093/cercor/bhj104

Bastiaansen, 2001, Anticipatory attention: An event-related desynchronization approach., International Journal of Psychophysiology, 43, 91, 10.1016/S0167-8760(01)00181-7

Bollimunta, 2008, Neuronal mechanisms of cortical alpha oscillations in awake-behaving macaques., Journal of Neuroscience, 28, 9976, 10.1523/JNEUROSCI.2699-08.2008

Brandt, 1991, The relationship between prestimulus alpha-amplitude and visual evoked-potential amplitude., International Journal of Neuroscience, 61, 261, 10.3109/00207459108990744

Brandt, 1991, Pre-stimulus spectral EEG patterns and the visual evoked-response., Electroencephalography and Clinical Neurophysiology, 80, 16, 10.1016/0168-5597(91)90037-X

Bressler, 2008, Top–down control of human visual cortex by frontal and parietal cortex in anticipatory visual spatial attention., Journal of Neuroscience, 28, 10056, 10.1523/JNEUROSCI.1776-08.2008

Callaway, 1998, Local circuits in primary visual cortex of the macaque monkey., Annual Review of Neuroscience, 21, 47, 10.1146/annurev.neuro.21.1.47

Capotosto, 2009, Frontoparietal cortex controls spatial attention through modulation of anticipatory alpha rhythms., Journal of Neuroscience, 29, 5863, 10.1523/JNEUROSCI.0539-09.2009

Cash, 1999, Linear summation of excitatory inputs by CA1 pyramidal neurons., Neuron, 22, 383, 10.1016/S0896-6273(00)81098-3

Chance, 2002, Gain modulation from background synaptic input., Neuron, 35, 773, 10.1016/S0896-6273(02)00820-6

Chung, 2002, Short-term depression at thalamocortical synapses contributes to rapid adaptation of cortical sensory responses in vivo., Neuron, 34, 437, 10.1016/S0896-6273(02)00659-1

Clark, 1996, Spatial selective attention affects early extrastriate but not striate components of the visual evoked potential., Journal of Cognitive Neuroscience, 8, 387, 10.1162/jocn.1996.8.5.387

Dehaene, 2005, Ongoing spontaneous activity controls access to consciousness: A neuronal model for inattentional blindness., PLoS Biology, 3, 910, 10.1371/journal.pbio.0030141

Destexhe, 2001, Fluctuating synaptic conductances recreate in vivo-like activity in neocortical neurons., Neuroscience, 107, 13, 10.1016/S0306-4522(01)00344-X

Di Russo, 2003, Source analysis of event-related cortical activity during visuo-spatial attention., Cerebral Cortex, 13, 486, 10.1093/cercor/13.5.486

Di Russo, 2002, Cortical sources of the early components of the visual evoked potential., Human Brain Mapping, 15, 95, 10.1002/hbm.10010

Ergenoglu, 2004, Alpha rhythm of the EEG modulates visual detection performance in humans., Cognitive Brain Research, 20, 376, 10.1016/j.cogbrainres.2004.03.009

Ferree, 2006, Spherical splines and average referencing in scalp electroencephalography., Brain Topography, 19, 43, 10.1007/s10548-006-0011-0

Fischer, 2008, Arousal and attention: Self-chosen stimulation optimizes cortical excitability and minimizes compensatory effort., Journal of Cognitive Neuroscience, 20, 1443, 10.1162/jocn.2008.20101

Foxe, 1998, Parieto-occipital similar to 10 Hz activity reflects anticipatory state of visual attention mechanisms., NeuroReport, 9, 3929, 10.1097/00001756-199812010-00030

Freeman, 1979, Non-linear gain mediating cortical stimulus–response relations., Biological Cybernetics, 33, 237, 10.1007/BF00337412

Garrido, 2007, Evoked brain responses are generated by feedback loops., Proceedings of the National Academy of Sciences, U.S.A., 104, 20961, 10.1073/pnas.0706274105

Gilbert, 1983, Functional-organization of the visual-cortex., Progress in Brain Research, 58, 209, 10.1016/S0079-6123(08)60022-9

Goldman, 2002, Simultaneous EEG and fMRI of the alpha rhythm., NeuroReport, 13, 2487, 10.1097/00001756-200212200-00022

Haider, 2007, Enhancement of visual responsiveness by spontaneous local network activity in vivo., Journal of Neurophysiology, 97, 4186, 10.1152/jn.01114.2006

Hanslmayr, 2007, Prestimulus oscillations predict visual perception performance between and within subjects., Neuroimage, 37, 1465, 10.1016/j.neuroimage.2007.07.011

Hanslmayr, 2007, Alpha phase reset contributes to the generation of ERPs., Cerebral Cortex, 17, 1, 10.1093/cercor/bhj129

Heilman, 2000, Neglect and related disorders., Seminars in Neurology, 20, 463, 10.1055/s-2000-13179

Heinze, 1994, Combined spatial and temporal imaging of brain activity during visual selective attention in humans., Nature, 372, 543, 10.1038/372543a0

Hillyard, 1998, Sensory gain control (amplification) as a mechanism of selective attention: Electrophysiological and neuroimaging evidence., Philosophical Transactions of the Royal Society of London, Series B, Biological Sciences, 353, 1257, 10.1098/rstb.1998.0281

Ho, 2000, Synaptic background activity enhances the responsiveness of neocortical pyramidal neurons., Journal of Neurophysiology, 84, 1488, 10.1152/jn.2000.84.3.1488

Jagadeesh, 1993, Linearity of summation of synaptic potentials underlying direction selectivity in simple cells of the cat visual cortex., Science, 262, 1901, 10.1126/science.8266083

Jansen, 1991, The effect of the phase of prestimulus alpha activity on the averaged visual evoked response., Electroencephalography and Clinical Neurophysiology, 80, 241, 10.1016/0168-5597(91)90107-9

Jones, 2000, Alpha-frequency rhythms desynchronize over long cortical distances: A modeling study., Journal of Computational Neuroscience, 9, 271, 10.1023/A:1026539805445

Jones, 2008, Influence of pre-stimulus somatosensory mu-rhythm on evoked response gain: A combined MEG and computational modeling study., Society for Neuroscience Meeting Abstract

Kelly, 2006, Increases in alpha oscillatory power reflect an active retinotopic mechanism for distracter suppression during sustained visuospatial attention., Journal of Neurophysiology, 95, 3844, 10.1152/jn.01234.2005

Klimesch, 2009, The functional relevance of phase reset: A comment to Risner et al. (2009): The visual evoked potential of surface alpha rhythm phase., Neuroimage, 47, 5, 10.1016/j.neuroimage.2009.03.070

Klimesch, 2007, EEG alpha oscillations: The inhibition-timing hypothesis., Brain Research Reviews, 53, 63, 10.1016/j.brainresrev.2006.06.003

Lakatos, 2008, Entrainment of neuronal oscillations as a mechanism of attentional selection., Science, 320, 110, 10.1126/science.1154735

Lakatos, 2005, An oscillatory hierarchy controlling neuronal excitability and stimulus processing in the auditory cortex., Journal of Neurophysiology, 94, 1904, 10.1152/jn.00263.2005

Linkenkaer-Hansen, 2004, Prestimulus oscillations enhance psychophysical performance in humans., Journal of Neuroscience, 24, 10186, 10.1523/JNEUROSCI.2584-04.2004

Luck, 2005, An introduction to the event-related potential technique.

Makeig, 2002, Dynamic brain sources of visual evoked responses., Science, 295, 690, 10.1126/science.1066168

Mangun, 1998, ERP and fMRI measures of visual spatial selective attention., Human Brain Mapping, 6, 383, 10.1002/(SICI)1097-0193(1998)6:5/6<383::AID-HBM10>3.0.CO;2-Z

Mangun, 1991, Modulations of sensory-evoked brain potentials indicate changes in perceptual processing during visual spatial priming., Journal of Experimental Psychology: Human Perception and Performance, 17, 1057

Mangun, 1997, Covariations in ERP and PET measures of spatial selective attention in human extrastriate visual cortex., Human Brain Mapping, 5, 273, 10.1002/(SICI)1097-0193(1997)5:4<273::AID-HBM12>3.0.CO;2-F

Marrufo, 2001, Temporal evolution of alpha and beta bands during visual spatial attention., Cognitive Brain Research, 12, 315, 10.1016/S0926-6410(01)00025-8

Mathewson, 2009, To see or not to see: Prestimulus phase predicts visual awareness., Journal of Neuroscience, 29, 2725, 10.1523/JNEUROSCI.3963-08.2009

Mazaheri, 2006, Posterior alpha activity is not phase-reset by visual stimuli., Proceedings of the National Academy of Sciences, U.S.A., 103, 2948, 10.1073/pnas.0505785103

McCormick, 2003, Persistent cortical activity: Mechanisms of generation and effects on neuronal excitability., Cerebral Cortex, 13, 1219, 10.1093/cercor/bhg104

Mitra, 1999, Analysis of dynamic brain imaging data., Biophysical Journal, 76, 691, 10.1016/S0006-3495(99)77236-X

Mitzdorf, 1985, Current source-density method and application in cat cerebral-cortex: Investigation of evoked-potentials and EEG phenomena., Physiological Reviews, 65, 37, 10.1152/physrev.1985.65.1.37

Niedermeyer, 1999, Electroencephalography: Basic principles, clinical applications, and related fields, 4th ed.

Nunez, 1997, EEG coherency: 1. Statistics, reference electrode, volume conduction, Laplacians, cortical imaging, and interpretation at multiple scales., Electroencephalography and Clinical Neurophysiology, 103, 499, 10.1016/S0013-4694(97)00066-7

Paul, 2007, Optimal sustained attention is linked to the spectral content of background EEG activity: Greater ongoing tonic alpha (approximately 10 Hz) power supports successful phasic goal activation., European Journal of Neuroscience, 25, 900, 10.1111/j.1460-9568.2007.05324.x

Petersen, 2003, Interaction of sensory responses with spontaneous depolarization in layer 2/3 barrel cortex., Proceedings of the National Academy of Sciences, U.S.A., 100, 13638, 10.1073/pnas.2235811100

Rajagovindan, 2008, Decomposing neural synchrony: Toward an explanation for near-zero phase-lag in cortical oscillatory networks., PLoS ONE, 3, e3649, 10.1371/journal.pone.0003649

Rihs, 2007, Mechanisms of selective inhibition in visual spatial attention are indexed by alpha-band EEG synchronization., European Journal of Neuroscience, 25, 603, 10.1111/j.1460-9568.2007.05278.x

Risner, 2009, The visual evoked potential is independent of surface alpha rhythm phase., Neuroimage, 45, 463, 10.1016/j.neuroimage.2008.12.031

Ritter, 2009, Detecting alpha rhythm phase reset by phase sorting: Caveats to consider., Neuroimage, 47, 1, 10.1016/j.neuroimage.2009.04.031

Romei, 2007, Spontaneous fluctuations in posterior {alpha}-band EEG activity reflect variability in excitability of human visual areas., Cerebral Cortex, 18, 2010, 10.1093/cercor/bhm229

Romei, 2008, Resting electroencephalogram alpha-power over posterior sites indexes baseline visual cortex excitability., NeuroReport, 19, 203, 10.1097/WNR.0b013e3282f454c4

Sauseng, 2005, A shift of visual spatial attention is selectively associated with human EEG alpha activity., European Journal of Neuroscience, 22, 2917, 10.1111/j.1460-9568.2005.04482.x

Schroeder, 2009, Low-frequency neuronal oscillations as instruments of sensory selection., Trends in Neurosciences, 32, 918, 10.1016/j.tins.2008.09.012

Schroeder, 1991, Striate cortical contribution to the surface-recorded pattern-reversal Vep in the alert monkey., Vision Research, 31, 1143, 10.1016/0042-6989(91)90040-C

Thomson, 2007, Functional maps of neocortical local circuitry., Frontiers in Neuroscience, 1, 19, 10.3389/neuro.01.1.1.002.2007

Thomson, 1982, Spectrum estimation and harmonic analysis., Proceedings of the IEEE, 70, 1055, 10.1109/PROC.1982.12433

Thut, 2006, Alpha-band electroencephalographic activity over occipital cortex indexes visuospatial attention bias and predicts visual target detection., Journal of Neuroscience, 26, 9494, 10.1523/JNEUROSCI.0875-06.2006

Van Dijk, 2008, Prestimulus oscillatory activity in the alpha band predicts visual discrimination ability., Journal of Neuroscience, 28, 1816, 10.1523/JNEUROSCI.1853-07.2008

Wolfart, 2005, Synaptic background activity controls spike transfer from thalamus to cortex., Nature Neuroscience, 8, 1760, 10.1038/nn1591

Worden, 2000, Anticipatory biasing of visuospatial attention indexed by retinotopically specific alpha-band electroencephalography increases over occipital cortex., Journal of Neuroscience, 20, RC63, 10.1523/JNEUROSCI.20-06-j0002.2000

Zhang, 2010, Detection of a weak somatosensory stimulus: Role of the prestimulus mu rhythm and its top–down modulation., Journal of Cognitive Neuroscience, 22, 307, 10.1162/jocn.2009.21247

Zhang, 2008, Prestimulus cortical activity is correlated with speed of visuomotor processing., Journal of Cognitive Neuroscience, 20, 1915, 10.1162/jocn.2008.20132