Patterns of Cortical Oscillations Organize Neural Activity into Whole-Brain Functional Networks Evident in the fMRI BOLD Signal

Jennifer C Whitman, Lawrence M Ward, Todd S Woodward, Jennifer C Whitman, Lawrence M Ward, Todd S Woodward

Abstract

Recent findings from electrophysiology and multimodal neuroimaging have elucidated the relationship between patterns of cortical oscillations evident in EEG/MEG and the functional brain networks evident in the BOLD signal. Much of the existing literature emphasized how high-frequency cortical oscillations are thought to coordinate neural activity locally, while low-frequency oscillations play a role in coordinating activity between more distant brain regions. However, the assignment of different frequencies to different spatial scales is an oversimplification. A more informative approach is to explore the arrangements by which these low- and high-frequency oscillations work in concert, coordinating neural activity into whole-brain functional networks. When relating such networks to the BOLD signal, we must consider how the patterns of cortical oscillations change at the same speed as cognitive states, which often last less than a second. Consequently, the slower BOLD signal may often reflect the summed neural activity of several transient network configurations. This temporal mismatch can be circumvented if we use spatial maps to assess correspondence between oscillatory networks and BOLD networks.

Keywords: BOLD; connectivity; electrophysiology; oscillation; synchronization.

References

    1. Arthurs O. J., Boniface S. (2002). How well do we understand the neural origins of the fMRI BOLD signal? Trends Neurosci. 25, 27–3110.1016/S0166-2236(00)01995-0
    1. Belluscio M. A., Mizuseki K., Schmidt R., Kempter R., Buzsaki G. (2012). Cross-frequency phase-phase coupling between theta and gamma oscillations in the hippocampus. J. Neurosci. 32, 423–43510.1523/JNEUROSCI.4122-11.2012
    1. Brookes M. J., Wood J. R., Stevenson C. M., Zumer J. M., White T. P., Liddle P. F., et al. (2011). Changes in brain network activity during working memory tasks: a magnetoencephalography study. Neuroimage 55, 1804–181510.1016/j.neuroimage.2010.10.074
    1. Burgess A. P. (2012). Towards a unified understanding of event-related changes in the EEG: the Firefly model of synchronization through cross-frequency phase modulation. PLoS ONE 7:e45630.10.1371/journal.pone.0045630
    1. Burns S., Xing D., Shapley R. M. (2011). Is gamma-band activity in the local field potential of V1 cortex a “clock” or filtered noise? J. Neurosci. 31, 9658–966410.1523/JNEUROSCI.0660-11.2011
    1. Canolty R. T., Edwards E., Dalal S. S., Soltani M., Nagarajan S. S., Kirsch H. E., et al. (2006). High gamma power is phase-locked to theta oscillations in human neocortex. Science 313, 1626–162810.1126/science.1128115
    1. Colgin L. L., Denninger T., Fyhn M., Hafting T., Bonnevie T., Jensen O., et al. (2009). Frequency of gamma oscillations routes flow of information in the hippocampus. Nature 462, 353–35710.1038/nature08573
    1. Contreras D., Llinas R. (2001). Voltage-sensitive dye imaging of neocortical spatiotemporal dynamics to afferent activation frequency. J. Neurosci. 21, 9403–9413
    1. Corbetta M., Patel G., Shulman G. L. (2008). The reorienting system of the human brain: from environment to theory of mind. Neuron 58, 306–32410.1016/j.neuron.2008.04.017
    1. Doesburg S. M., Green J. J., McDonald J. J., Ward L. M. (2009a). From local inhibition to long-range integration: a functional dissociation of alpha-band synchronization across cortical scales in visuospatial attention. Brain Res. 1303, 97–11010.1016/j.brainres.2009.09.069
    1. Doesburg S. M., Green J. J., McDonald J. J., Ward L. M. (2009b). Rhythms of consciousness: binocular rivalry reveals large-scale oscillatory network dynamics mediating visual perception. PLoS ONE 4:e6142.10.1371/journal.pone.0006142
    1. Doesburg S. M., Roggeveen A. B., Kitajo K., Ward L. M. (2008). Large-scale gamma-band phase synchronization and selective attention. Cereb. Cortex 18, 386–39610.1093/cercor/bhm073
    1. 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. Proc. Natl. Acad. Sci. U.S.A. 102, 9673–967810.1073/pnas.0409470102
    1. Fries P. (2005). A mechanism for cognitive dynamics: neuronal communication through neuronal coherence. Trends Cogn. Sci. (Regul. Ed.) 9, 474–48010.1016/j.tics.2005.08.011
    1. Gray C. M., Konig P., Engel A. K., Singer W. (1989). Oscillatory responses in cat visual-cortex exhibit inter-columnar synchronization which reflects global stimulus properties. Nature 338, 334–33710.1038/338334a0
    1. Gray C. M., Singer W. (1989). Stimulus-specific neuronal oscillations in orientation columns of cat visual-cortex. Proc. Natl. Acad. Sci. U.S.A. 86, 1698–170210.1073/pnas.86.7.2267
    1. He B. J., Raichle M. E. (2009). The fMRI signal, slow cortical potential and consciousness. Trends Cogn. Sci. (Regul. Ed.) 13, 302–30910.1016/j.tics.2009.04.004
    1. He B. J., Snyder A. Z., Zempel J. M., Smyth M. D., Raichle M. E. (2008). Electrophysiological correlates of the brain’s intrinsic large-scale functional architecture. Proc. Natl. Acad. Sci. U.S.A. 105, 16039–1604410.1073/pnas.0710631105
    1. Hipp J. F., Engel A. K., Siegel M. (2011). Oscillatory synchronization in large-scale cortical networks predicts perception. Neuron 69, 387–39610.1016/j.neuron.2010.12.027
    1. Jensen O., Colgin L. L. (2007). Cross-frequency coupling between neuronal oscillations. Trends Cogn. Sci. (Regul. Ed.) 11, 267–26910.1016/j.tics.2007.05.003
    1. Lippert M. T., Steudel T., Ohl F., Logothetis N. K., Kayser C. (2010). Coupling of neural activity and fMRI-BOLD in the motion area MT. Magn. Reson. Imaging 28, 1087–109410.1016/j.mri.2009.12.028
    1. Lisman J. E., Idiart M. A. (1995). Storage of 7+/-2 short-term memories in oscillatory subcycles. Science 267, 1512–151510.1126/science.7878473
    1. Logothetis N. K., Pauls J., Augath M., Trinath T., Oeltermann A. (2001). Neurophysiological investigation of the basis of the fMRI signal. Nature 412, 150–15710.1038/35084005
    1. Magri C., Schridde U., Murayama Y., Panzeri S., Logothetis N. K. (2012). The amplitude and timing of the BOLD signal reflects the relationship between local field potential power at different frequencies. J. Neurosci. 32, 1395–140710.1523/JNEUROSCI.3985-11.2012
    1. Maier A., Adams G. K., Aura C., Leopold D. A. (2010). Distinct superficial and deep laminar domains of activity in the visual cortex during rest and stimulation. Front. Syst. Neurosci. 4:31.10.3389/fnsys.2010.00031
    1. Mukamel R., Gelbard H., Arieli A., Hasson U., Fried I., Malach R. (2005). Coupling between neuronal firing, field potentials, and fMR1 in human auditory cortex. Science 309, 951–95410.1126/science.1110913
    1. Niessing J., Ebisch B., Schmidt K. E., Niessing M., Singer W., Galuske R. A. W. (2005). Hemodynamic signals correlate tightly with synchronized gamma oscillations. Science 309, 948–95110.1126/science.1110948
    1. Nir Y., Fisch L., Mukamel R., Gelbard-Sagiv H., Arieli A., Fried I., et al. (2007). Coupling between neuronal firing rate, gamma LFP, and BOLD fMRI is related to interneuronal correlations. Curr. Biol. 17, 1275–128510.1016/j.cub.2007.06.066
    1. Schölvinck M. L., Maier A., Ye F. Q., Duyn J. H., Leopold D. A. (2010). Neural basis of global resting-state fMRI activity. Proc. Natl. Acad. Sci. U.S.A. 107, 10238–1024310.1073/pnas.0913110107
    1. Varela F., Lachaux J. P., Rodriguez E., Martinerie J. (2001). The brainweb: phase synchronization and large-scale integration. Nat. Rev. Neurosci. 2, 229–23910.1038/35067550
    1. von Stein A., Sarnthein J. (2000). Different frequencies for different scales of cortical integration: from local gamma to long range alpha/theta synchronization. Int. J. Psychophysiol. 38, 301–31310.1016/S0167-8760(00)00172-0
    1. Wang L., Saalmann Y. B., Pinsk M. A., Arcaro M. J., Kastner S. (2012). Electrophysiological low-frequency coherence and cross-frequency coupling contribute to BOLD connectivity. Neuron 76, 1010–102010.1016/j.neuron.2012.09.033

Source: PubMed

3
Tilaa