Skip to main content
Search
Search
    Quick Search anywhere
    Quick search in Citations
Advanced Search
Skip main navigationClose Drawer MenuOpen Drawer Menu
Previous article
Next article
Article

Trial-to-Trial Variability in Evoked Neural Responses Exhibits a Very Low Frequency Temporal Signature

A Magnetoencephalography Study

Published Online:June 09, 2010https://doi.org/10.1027/0269-8803/a000002

Abstract

In functional magnetic resonance (fMRI) studies, the blood oxygen level dependent (BOLD) signal displays intrinsic spontaneous and task-independent very low frequency (VLF) oscillations (< 0.1 Hz). Most prominent during rest, when they persist into task sessions they can predict trial-to-trial variability in both evoked behavior and brain responses by providing a baseline onto which deterministic responses elicited by the task are superimposed. Moreover, evidence in the literature tentatively suggests that this VLF activity may not be present in the data as distinct, independent source(s) per se, but rather as a mechanism that modulates and perhaps even governs underlying brain processes. Here, we use electrophysiology to investigate the intertrial variability observed in magnetoencephalographic (MEG) event-related field (ERF) components, and to examine whether this variability exhibits a VLF time signature in order to indirectly infer information about the underlying slow waves. The focus is on the visual component, the M100, understood to be regulated by attention. We also explored whether individual differences in the M100 VLF pattern varies as a function of attention deficit/hyperactivity disorder (ADHD) by comparing 11 cases against 11 controls. The M100 component was extracted from the data using a recently introduced blind-source separation technique – space-time independent component analysis (ST-ICA) – which allowed trial-by-trial analysis to be performed on the M100 for proper assessment of VLF modulation. Our results demonstrate, for the first time, the ability of this signal-processing method to isolate relevant components from multidimensional, noisy, ERF data recorded from a highly dense 148-channel MEG system. The intertrial variability in the amplitude and latency of the M100 responses exhibits a slow wave pattern (< 0.1 Hz). However, there was no evidence that the degree of VLF modulation was different in ADHD participants. The role of this VLF activity in brain function is discussed.

References

  • American Psychiatric Association . (2000). Diagnostic and statistical manual of mental disorders (DSM-IV-TR). Washington, DC: Author. First citation in articleGoogle Scholar

  • Arieli, A. , Sterkin, A. , Grinvald, A. , Aertsen, A. (1996). Dynamics of ongoing activity: Explanation of the large variability in evoked cortical responses. Science, 273, 1868–1871. First citation in articleCrossref, Google Scholar

  • Auer, A. P. (2008). Spontaneous low-frequency blood oxygenation level-dependent fluctuations and functional connectivity analysis of the “resting” brain. Magnetic Resonance Imaging, 26, 1055–1064. First citation in articleCrossref, Google Scholar

  • Azouz, R. , Gray, C. M. (1999). Cellular mechanisms contributing to response variability of cortical neurons in vivo. Journal of Neuroscience, 19, 2209–2223. First citation in articleGoogle Scholar

  • Barratt, W. (2006). The Barratt simplified measure of social status (BSMSS) measuring SES. Unpublished manuscript, Indiana State University, Terre Haute, IN, USA. First citation in articleGoogle Scholar

  • Biswal, B. B. , Yetkin, F. Z. , Haughton, V. M. , Hyde, J. S. (1995). Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magnetic Resonance in Medicine, 34, 537–541. First citation in articleCrossref, Google Scholar

  • Broyd, S. J. , Demanuele, C. , Debener, S. , Helps, S. K. , James, C. J. , Sonuga-Barke, E. J. S. (2009). Default-mode brain dysfunction in mental disorders: A systematic review. Neuroscience and Biobehavioral Reviews, 33, 279–296. First citation in articleCrossref, Google Scholar

  • Buzsaki, G. , Draguhn, A. (2004). Neuronal oscillations in cortical networks. Science, 304, 1926–1929. First citation in articleGoogle Scholar

  • Castellanos, F. X. , Sonuga-Barke, E. J. S. , Scheres, A. , Di Martino, A. , Hyde, C. , Walters, J. (2005). Varieties of Attention-deficit/hyperactivity disorder-related intraindividual variability. Biological Psychiatry, 57, 1416–1423. First citation in articleCrossref, Google Scholar

  • Davies, M. E. , James, C. J. (2007). Source separation using single-channel ICA. Signal Processing, 87, 1819–1832. First citation in articleCrossref, Google Scholar

  • Davies, M. , James, C. J. , Wang, S. (2007). Space-time ICA and EM brain signals. In M. E. Davies, C. J. James, S. A. Abdallah, M. D. Plumbley (Eds.), Proceedings of the 7th International Conference on Independent Component Analysis and Signal Separation, London, UK (pp. 577–584). Berlin: Springer-Verlag. First citation in articleCrossref, Google Scholar

  • Debener, S. , Ullsperger, M. , Siegel, M. , Fiehler, K. , von Cramon, D. Y. , Engel, A. K. (2006). Single-trial EEG/fMRI reveals the dynamics of cognitive function. Trends in Cognitive Sciences, 10, 558–563. First citation in articleCrossref, Google Scholar

  • Demanuele, C. , James, C. J. , Capilla, A. , Sonuga-Barke, E. J. S. (2008). Extracting event-related field components through space-time ICA: A study of MEG recordings from children with ADHD and controls. In J. Vander Sloten, P. Verdonck, M. Nyssen, J. Haueisen (Eds.), Proceedings of the 4th European Conference of the International Federation for Medical and Biological Engineering, Antwerp, Belgium (IFMBE Proceedings, 22) (pp. 38–42). Berlin: Springer-Verlag. First citation in articleGoogle Scholar

  • Di Martino, A. , Ghaffari, M. , Curchack, J. , Reiss, P. , Hyde, C. , Vannucci, M. , ... Castellanos, F. X. (2008). Decomposing intrasubject variability in children with attention-deficit/hyperactivity disorder. Biological Psychiatry, 64, 607–614. First citation in articleCrossref, Google Scholar

  • Fergusson, D. , Horwood, L. , Lynskey, M. (1994). The childhoods of multiple problem adolescents: A 15-year longitudinal study. Australian and New Zealand Journal of Psychiatry, 35, 1123–1140. First citation in articleGoogle Scholar

  • Fiser, J. , Chiu, C. , Weliky, M. (2004). Small modulation of ongoing cortical dynamics by sensory input during natural vision. Nature, 431, 573–578. First citation in articleCrossref, Google Scholar

  • Fox, M. D. , Raichle, M. E. (2007). Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nature Neuroscience Reviews, 8, 700–711. First citation in articleCrossref, Google Scholar

  • Fox, M. D. , Snyder, A. Z. , Vincent, J. L. , Corbetta, M. , Van Essen, D. C. , Raichle, M. E. (2005). The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proceedings of the National Academy of Science USA, 102, 9673–9678. First citation in articleGoogle Scholar

  • Fox, M. , Snyder, A. , Vincent, J. , Raichle, M. (2007). Intrinsic fluctuations within cortical systems account for intertrial variability in human behavior. Neuron, 56, 171–184. First citation in articleCrossref, Google Scholar

  • Fox, M. D. , Snyder, A. Z. , Zacks, J. M. , Raichle, M. E. (2006). Coherent spontaneous activity accounts for trial-to-trial variability in human evoked brain responses. Nature Neuroscience, 9, 23–25. First citation in articleCrossref, Google Scholar

  • Fransson, P. (2005). Spontaneous low-frequency signal fluctuations: An fMRI investigation of the resting-state default mode of brain function hypothesis. Human Brain Mapping, 26, 15–29. First citation in articleGoogle Scholar

  • Fransson, P. (2006). How default is the default mode of brain function? Further evidence from intrinsic signal fluctuations. Neuropsychologia, 44, 2836–2845. First citation in articleCrossref, Google Scholar

  • Heinrich, H. , Moll, G. H. , Dickhaus, H. , Kolev, V. , Yordanova, J. , Rothenberger, A. (2001). Time-on-task analysis using wavelet networks in an event-related potential study on attention-deficit hyperactivity disorder. Clinical Neurophysiology, 112, 1280–1287. First citation in articleCrossref, Google Scholar

  • Helps, S. K. , Broyd, S. J. , James, C. J. , Karl, A. , Sonuga-Barke, E. J. S. (in press). The attenuation of very low frequency brain oscillations in transitions from a rest state to active attention. Journal of Psychophysiology. First citation in articleGoogle Scholar

  • Helps, S. K. , James, C. , Debener, S. , Karl, A. , Sonuga-Barke, E. J. S. (2008). Very low frequency EEG oscillations and the resting brain in young adults: A preliminary study of localization, stability and association with symptoms of inattention. Journal of Neural Transmission, 115, 279–285. First citation in articleCrossref, Google Scholar

  • Hillyard, S. A. , Anllo-Vento, L. (1998). Event-related brain potentials in the study of visual selective attention. Proceedings of the National Academy of Science USA, 95, 781–787. First citation in articleGoogle Scholar

  • Hillyard, S. A. , Kutas, M. (2002). Event-related potentials and magnetic fields in the human brain. In L. K. Davis, D. Charney, J. T. Coyle, C. B. Nemeroff (Eds.), Neuropsychopharmacology: The fifth generation of progress (pp. 427–439). MA: Lippincott Williams & Wilkins. First citation in articleGoogle Scholar

  • Hyvärinen, A. , Karhunen, J. , Oja, E. (2001). Independent component analysis. New York: Wiley. First citation in articleCrossref, Google Scholar

  • Ivannikov, A. , Karkkainen, T. , Ristaniemi, T. , Lyytinen, H. (2007). Extraction of ERP from EEG Data. Proceedings of the 9th IEEE International Symposium on Signal Processing and Applications, 1–4. First citation in articleGoogle Scholar

  • James, C. J. (2008). Contrasting spatial, temporal and spatio-temporal ICA applied to ictal EEG recordings. Proceedings of the 30th IEEE EMBS Annual International Conference, Vancouver, Canada, 3336–3339. First citation in articleGoogle Scholar

  • James, C. J. , Hesse, C. W. (2005). Independent component analysis for biomedical signals. Physiological Measurement, 26, 15–39. First citation in articleCrossref, Google Scholar

  • James, C. J. , Lowe, D. (2001). Single-channel analysis of electromagnetic brain signals through ICA in a dynamical systems framework. Proceedings of the 23rd IEEE EMBS Annual International Conference, Turkey, 1974–1977. First citation in articleGoogle Scholar

  • James, C. J. , Abasolo, D. , Gupta, D. (2007). Space-time ICA versus Ensemble ICA for ictal EEG analysis with component differentiation via Lempel-Ziv complexity. Proceedings of the 29th IEEE EMBS Annual International Conference, Lyon, France, 5473–5476. First citation in articleGoogle Scholar

  • James, C. J. , Gibson, O. , Davies, M. (2006). On the analysis of single versus multiple channels of electromagnetic brain signals. Artificial Intelligence in Medicine, 37, 131–143. First citation in articleCrossref, Google Scholar

  • Jasper, H. H. (1958). The 10–20 electrode system of the International Federation. Electroencephalography and Clinical Neurophysiology, 10, 371–5. First citation in articleGoogle Scholar

  • Jiménez-González, A. , James, C. J. (2009). Extracting sources from noisy abdominal phonograms: A single-channel blind source separation method. Medical and Biological Engineering and Computing, 47, 655–664. First citation in articleCrossref, Google Scholar

  • Johnson, K. A. , Kelly, S. P. , Bellgrove, M. A. , Barry, E. , Cox, M. , Gill, M. , Robertson, I. H. (2007). Response variability in Attention Deficit Hyperactivity Disorder: Evidence of neuropsychological heterogeneity. Neuropsychologia, 45, 630–638. First citation in articleCrossref, Google Scholar

  • Johnstone, S. J. , Barry, R. J. , Dimoska, A. (2003). Event-related slow-wave activity in two subtypes of attention-deficit/hyperactivity disorder. Clinical Neurophysiology, 114, 504–514. First citation in articleCrossref, Google Scholar

  • Jonkman, L. M. , Kemner, C. , Verbaten, M. N. , Koelega, H. S. , Camfferman, G. , Gaag, R. J. , ... van Engeland, H. (1997). Event-related potentials and performance of attention-deficit hyperactivity disorder: Children and normal controls in auditory and visual selective attention tasks. Biological Psychiatry, 41, 595–611. First citation in articleCrossref, Google Scholar

  • Jonkman, L. M. , Kenemans, J. , Kemner, C. , Verbaten, M. , van Engeland, H. (2004). Dipole source localization of event-related brain activity indicative of an early visual selective attention deficit in ADHD children. Journal of Clinical Neurophysiology, 115, 1537–1549. First citation in articleCrossref, Google Scholar

  • Jung, T.-P. , Makeig, S. , Westerfield, M. , Townsend, J. , Courchesne, E. , Sejnowski, T. J. (2001). Analysis and visualization of single-trial event-related potentials. Human Brain Mapping, 14, 166–185. First citation in articleCrossref, Google Scholar

  • Karayanidis, F. , Robaey, P. , Bourassa, M. , De Koning, D. , Geoffroy, G. , Pelletier, G. (2000). ERP differences in visual attention processing between ADHD and control boys in the absence of performance differences. Psychophysiology, 37, 319–333. First citation in articleCrossref, Google Scholar

  • Kolev, V. , Yordanova, J. (1997). Analysis of phase-locking is informative for studying event-related EEG activity. Biological Cybernetics, 76, 229–235. First citation in articleCrossref, Google Scholar

  • Laufs, H. , Krakow, K. , Sterzer, P. , Eger, E. , Beyerle, A. , Salek-Haddadi, A. , Kleinschmidt, A. (2003). Electroencephalographic signatures of attentional and cognitive default modes in spontaneous brain activity at rest. In M. E. Raichle (Ed.), Proceedings of the National Academy of Science USA, 100, 11053–11058. First citation in articleGoogle Scholar

  • Leistner, S. , Sander, T. , Burghoff, M. , Curio, G. , Trahms, L. , Mackert, B.-M. (2007). Combined MEG and EEG methodology for noninvasive recording of infraslow activity in the human cortex. Clinical Neurophysiology, 118, 2774–2780. First citation in articleCrossref, Google Scholar

  • Makeig, S. , Debener, S. , Onton, J. , Delorme, A. (2004). Mining event-related brain dynamics. Trends in Cognitive Science, 8, 204–210. First citation in articleCrossref, Google Scholar

  • Makeig, S. , Jung, T.-P. , Bell, A. J. , Ghahremani, D. , Sejnowski, J. (1997). Blind separation of auditory event-related brain responses into independent components. Neurobiology, 94, 10979–10984. First citation in articleGoogle Scholar

  • Makeig, S. , Westerfield, M. , Townsend, J. , Jung, T.-P. , Courchesne, E. , Sejnowski, T. J. (1999). Functionally independent components of early event-related potentials in a visual spatial attention task. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences, 354, 1135–1144. First citation in articleCrossref, Google Scholar

  • Max, J. E. , Schachar, R. J. , Levin, H. S. , Ewing-Cobbs, L. , Chapman, S. B. , Dennis, M. , ... Landis, J. (2005). Predictors of Attention-Deficit/Hyperactivity Disorder within 6 months after pediatric traumatic brain injury. Journal of the American Academy of Child and Adolescent Psychiatry, 44, 1032–1040. First citation in articleCrossref, Google Scholar

  • Monto, S. , Palva, S. , Voipio, J. , Palva, J. M. (2008). Very slow EEG fluctuations predict the dynamics of stimulus detection and oscillation amplitudes in humans. Journal of Neuroscience, 28, 8268–8272. First citation in articleCrossref, Google Scholar

  • Mulas, F. , Capilla, A. , Fernández, S. , Etchepareborda, M. C. , Campo, P. , Maestú, F. , ... Ortiz, T. (2006). Shifting-related brain magnetic activity in attention-deficit/hyperactivity disorder. Biological Psychiatry, 59, 373–379. First citation in articleCrossref, Google Scholar

  • Muller, K.-R. , Vigario, R. , Meinecke, F. , Ziehe, A. (2004). Blind source separation techniques for decomposing event-related brain signals. International Journal of Bifurcation and Chaos, 14, 773–791. First citation in articleCrossref, Google Scholar

  • Nakagawa, S. , Ueno, S. , Imada, T. (1999). Measurements and source estimation of extremely low frequency brain magnetic fields in a short-term memory task by a whole-head neurogradiometer. IEEE Transactions on Magnetics, 35, 4130–4132. First citation in articleCrossref, Google Scholar

  • Ozdag, M. , Yorbik, O. , Ulas, U. , Hamamcioglu, K. , Vural, O. (2004). Effect of methylphenidate on auditory event related potential in boys with attention deficit hyperactivity disorder. International Journal of Pediatric Otorhinolaryngology, 68, 1267–1272. First citation in articleCrossref, Google Scholar

  • Perchet, C. , Revol, O. , Fourneret, O. , Mauguiere, F. , Garcia-Larrea, L. (2001). Attention shift and anticipatory mechanisms in hyperactive children: An ERP study using Posner paradigm. Biological Psychiatry, 50, 44–57. First citation in articleCrossref, Google Scholar

  • Polanczyk, G. , de Lima, M. S. , Horta, B. L. , Biederman, J. , Rohde, L. A. (2007). The worldwide prevalence of ADHD: A systematic review and metaregression analysis. American Journal of Psychiatry, 164, 942–8. First citation in articleCrossref, Google Scholar

  • Rama, P. , Carlson, S. , Kekoni, J. , Hamalainen, H. (1995). A spatial oculomotor memory-task performance produces a task-related slow-shift in human electroencephalography. Electroencephalography and Clinical Neurophysiology, 94, 371–380. First citation in articleCrossref, Google Scholar

  • Reynolds, C. R. , Kamphaus, R. W. (1992). Behavior assessment system for children (BASC). Circle Pines, MN: American Guidance Services (Ags). First citation in articleGoogle Scholar

  • Reynolds, C. R. , Kamphaus, R. W. (2004). BASC: Sistema de evaluación de la conducta en niños y adolescentes [Evaluation system on the behavior of children and adolescents] (Spanish adaptation). Madrid: TEA. First citation in articleGoogle Scholar

  • Ruckin, D. S. , Canoune, H. , Johnson, R. , Ritter, W. (1990). Working memory and preparation elicit different patterns of slow wave event-related brain potentials. Psychobiology, 32, 399–410. First citation in articleGoogle Scholar

  • Shmuel, A. , Leopold, D. A. (2008). Neuronal correlated of spontaneous fluctuations in fMRI signals in monkey visual cortex: Implications for functional connectivity at rest. Human Brain Mapping, 29, 751–61. First citation in articleCrossref, Google Scholar

  • Sonuga-Barke, E. J. S. , Castellanos, F. X. (2007). Spontaneous attentional fluctuations in impaired states and pathological conditions: A neurobiological hypothesis. Neuroscience and Biobehavioral Reviews, 31, 977–986. First citation in articleGoogle Scholar

  • Vanhatalo, S. , Palva, J. M. , Holmes, M. D. , Miller, J. W. , Voipio, J. , Kaila, K. (2004). Infraslow oscillations modulate excitability and interictal epileptic activity in the human cortex during sleep. In M. E. Raichle (Ed.), Proceedings of the National Academy of Science USA, 101, 5053–5057. First citation in articleGoogle Scholar

  • Wall, M. E. , Rechtsteiner, A. , Rocha, L. M. (2003). Singular value decomposition and principal component analysis. In D. P. Berrar, W. Dubitzky, M. Granzow (Eds.), A practical approach to microarray data analysis (pp. 91–109). New Mexico, MA: Kluwer, Norwell. First citation in articleCrossref, Google Scholar

  • Welch, P. D. (1967). The use of fast Fourier transform for the estimation of power spectra: A method based on time averaging over short, modified periodograms. IEEE Transactions on Audio Electroacoustics, AU-15, 70–73. First citation in articleCrossref, Google Scholar

  • Xiaorong, G. , Neng, X. , Bo, H. , Shangkai, G. , Fusheng, Y. (2004). Optimal selection of independent components for event-related brain electrical potential enhancement. IEEE International Workshop on Biomedical Circuits and Systems, 1–4. First citation in articleGoogle Scholar