Abstract
Functional networks in the human brain have been investigated using electrophysiological methods (EEG/MEG, LFP, and MUA) and steady-state paradigms that apply periodic luminance or contrast modulation to drive cortical networks. We have used this approach with fMRI to characterize a cortical network driven by a checkerboard reversing at a fixed frequency. We found that the fMRI signals in voxels located in occipital cortex were increased by checkerboard reversal at frequencies ranging from 3 to 14 Hz. In contrast, the response of a cluster of voxels centered on basal medial frontal cortex depended strongly on the reversal frequency, consistently exhibiting a peak in the response for specific reversal frequencies between 3 and 5 Hz in each subject. The fMRI signals at the frontal voxels were positively correlated indicating a homogeneous cluster. Some of the occipital voxels were positively correlated to the frontal voxels apparently forming a large-scale functional network. Other occipital voxels were negatively correlated to the frontal voxels, suggesting a functionally distinct network. The results provide preliminary fMRI evidence that during visual stimulation, input frequency can be varied to engage different functional networks.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Bendat JS, Piersol A (2000) Random data: analysis and measurement procedures, 3rd edn. Wiley, NY
Bland M (2000) An introduction to medical statistics, 3rd edn. Oxford University Press, New York
Brainard DH (1997) The psychophysics toolbox. Spat Vis 10:433–436
Chen Y, Seth AK, Gally JA, Edelman GM (2003) The power of human brain magnetoencephalographic signals can be modulated up or down by changes in an attentive visual task. Proc Natl Acad Sci USA 100:3501–3506
Daniel W (1978) Applied nonparametric statistics. Houghton, Mifflin
Ding J, Sperling G, Srinivasan R (2006) Attentional modulation of SSVEP power depends on the network tagged by the flicker frequency. Cereb Cortex 16:1016–1029
Engel AK, Fries P, Singer W (2001) Dynamic predictions: oscillations and synchrony in top-down processing. Nat Rev Neurosci 2:704–716
Fischl B, Sereno MI, Dale AM (1999) Cortical surface-based analysis II: inflation, flattening, and a surface-based coordinate system. Neuroimage 9:179–194
Fox PT, Raichle ME (1984) Stimulus rate dependence of regional cerebral blood flow in human striate cortex, demonstrated by positron emission tomography. J Neurophysiol 51:1109–1120
Gusnard DA, Akbudak E, Shulman GL, Raichle ME (2001) Medial prefrontal cortex and self-referential mental activity: relation to a default mode of brain function. PNAS USA 98:4259–4264
Habeck CG, Srinivasan R (2000) Natural solutions to the problem of functional integration. Behav Brain Sci 23:402–403
Hagenbeek RE, Rombouts SARB, van Dijk BW, Barkhof F (2002) Determination of individual stimulus-response curves in the visual cortex. Hum Brain Mapp 17:244–250
Herrmann CS (2001) EEG responses to 1–100 Hz flicker: resonance phenomena in visual cortex and their potential correlation to cognitive phenomena. Exp Brain Res 137:346–353
Knyazeva MG, Fornari E, Meuli R, Maeder P (2006) Interhemispheric integration at different spatial scales: the evidence from EEG coherence and FMRI. J Neurophysiol 96:259–275
Kreig WJS (1973) Architectonics of human cerebral fiber systems. Brain Books, Evanston, IL
Kreig WJS (1963) Connections of the cerebral cortex. Brain Books, Evanston, IL
Kwong KK, Belliveau JW, Chesler DA, Goldberg IE, Weisskoff RM, Poncelet BP, Kennedy DN, Hoppel BE, Cohen MS, Turner R, Cheng HM, Brady TJ, Rosen BR (1992) Dynamic magnetic resonance imaging during primary sensory stimulation. PNAS USA 89:5675–5679
Mentis MJ, Alexander GE, Grady CL, Horowitz B, Krasuski J, Pietrini P, Strassburger T, Hampel H, Schapiro MB, Rapoport SI (1997) Frequency variation of a pattern-flash visual stimulus during PET differentially activates brain from striate through frontal cortex. Neuroimage 5:116–128
Muller MM, Teder W, Hillyard SA (1997) Magnetoencephalographic recording of steady-state visual evoked cortical activity. Brain Topogr 9:163–168
Nakayama K, Mackeben M (1982) Steady-state visual evoked potentials in the alert primate. Vision Res 22:1261–1271
Narici L, Portin K, Salmelin R, Hari R (1998) Responsiveness of human cortical activity to rhythmical stimulation: a three-modality whole cortex neuromagnetic investigation 7:209–223
Nunez PL (1981) Electric fields of the brain: the neurophysics of EEG. Oxford, NY
Nunez PL (1995) Neocortical dynamics and human EEG rhythms. Oxford, NY
Nunez PL (2000) Towards a quantitative description of neocortical dynamic function and EEG. Behav Brain Sci 23:371–437
Nunez PL, Silberstein RB (2000) On the relationship of synaptic activity to macroscopic measurements: does co-registration of EEG with fMRI make sense? Brain Topogr 13:79–96
Nunez PL, Srinivasan R (2006) Electric fields of the brain: the neurophysics of EEG, 2nd edn. Oxford University Press, New York
Rager G, Singer W (1998) The response of the cat visual cortex to flicker stimuli of variable frequency. Eur J Neurosci 10:1856–1877
Regan D (1977) Steady-state evoked potentials. J Opt Soc Am 67:1475–1489
Regan D (1989) Human brain electrophysiology. Elsevier, New York
Saad ZS, Ropelia KM, Cox RW, DeYoe EA (2001) Analysis and use of fMRI response delays. Hum Brain Mapp 13:74–93
Schmolesky MT, Wang Y, Hanes DP, Thompson KG, Leutgeb S, Schall JD, Leventhal AG (1998) Signal timing across the macaque visual system. J Neurophysiol 79:3272–3278
Shmuel A, Yacoub E, Pfeuffer J, Van der Moortele PF, Adriany G, Hu X, Ugurbil K (2002) Sustained negative BOLD, blood flow, and oxygen consumption response and its coupling to positive response in the human brain. Neuron 36:1195–1210
Silberstein RB, Nunez PL, Pipingas A, Harris P, Danieli F (2001) Steady state visually evoked potential (SSVEP) topography in a graded working memory task. Int J Psychophysiol 42:219–232
Silberstein RB (1995) Steady state visually evoked potentials, brain resonances and cognitive processes. In: Nunez PL (ed) Neocortical dynamics and human EEG rhythms. Oxford University Press, New York
Silberstein RB, Danieli F, Nunez PL (2003) Fronto-parietal evoked potential synchronization is increased during mental rotation. Neuroreport 14:67–71
Silberstein RB, Song J, Nunez PL, Park W (2004) Dynamic sculpting of brain functional connectivity is correlated with performance. Brain Topogr 16:249–254
Singer W (1999a) Striving for coherence. Nature 397:391–393
Singer W (1999b) Neural synchrony, a versatile code for the definition of relations? Neuron 24:49–65
Singh M, Kim S, Kim TS (2003) Correlation between BOLD-fMRI and EEG signal changes in response to visual stimulus frequency in humans. Magn Reson Med 49:108–114
Srinivasan R (2004) Internal and external neural synchronization during conscious perception. Int J Bifurcat Chaos 19:1–18
Srinivasan R, Bibi FA, Nunez PL (2006) Steady-state visual evoked potentials: distributed local sources and wave-like dynamics are sensitive to flicker frequency. Brain Topogr 18:167–187
Srinivasan R, Nunez PL, Silberstein RB (1998) Spatial filtering and neocortical dynamics: estimates of EEG coherence. IEEE Trans Biomed Eng 45:814–826
Srinivasan R, Nunez PL, Tucker DM, Silberstein RB, Cadusch PJ (1996) Spatial sampling and filtering of EEG with spline laplacians to estimate cortical potentials. Brain Topogr 8:355–366
Srinivasan R, Petrovic S (2006) MEG phase follows conscious perception during binocular rivalry induced by visual stream segregation. Cereb Cortex 16:597–608
Srinivasan R, Russell DP, Edelman GM, Tononi G (1999) Increased synchronization of neuromagnetic responses during conscious perception. J Neurosci 19:5435–5448
Talairach J, Tournoux P (1988) Co-planar stereotaxic atlas of the human brain. Thieme Medical Publishers, New York
Thomas CG, Menon RS (1998) Amplitude response and stimulus presentation frequency response of human primary visual cortex using BOLD EPI at 4T. Magn Reson Med 40:203–209
Tononi G, Srinivasan R, Russell DP, Edelman GM (1998) Investigating neural correlates of conscious perception by frequency-tagged neuromagnetic responses. Proc Natl Acad Sci USA 95:3198–3203
Tyler CW, Apkarian P, Nakayama K (1978) Multiple spatial frequency tuning of electrical responses from the human visual cortex. Exp Brain Res 33:535–550
von Stein A, Chiang C, Konig P (2000) Top-down processing mediated by interareal synchronization. Proc Natl Acad Sci USA 97:14748–14753
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 38:301–313
Acknowledgments
This research was supported by a Visiting Fellowship from the Novartis Consumer Health Foundation to RS, a grant from the NIH R01-MH68004 and by Swiss National Science Foundation Grant No 31-63894.00.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Srinivasan, R., Fornari, E., Knyazeva, M.G. et al. fMRI responses in medial frontal cortex that depend on the temporal frequency of visual input. Exp Brain Res 180, 677–691 (2007). https://doi.org/10.1007/s00221-007-0886-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-007-0886-3