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Functional MRI mapping neuronal inhibition and excitation at columnar level in human visual cortex

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Abstract

The capability of non-invasively mapping neuronal excitation and inhibition at the columnar level in human is vital in revealing fundamental mechanisms of brain functions. Here, we show that it is feasible to simultaneously map inhibited and excited ocular dominance columns (ODCs) in human primary visual cortex by combining high-resolution fMRI with the mechanism of binocular inhibitory interaction induced by paired monocular stimuli separated by a desired time delay. This method is based on spatial differentiation of fMRI signal responses between inhibited and excited ODCs that can be controlled by paired monocular stimuli. The feasibility and reproducibility for mapping both inhibited and excited ODCs have been examined. The results conclude that fMRI is capable of non-invasively mapping both excitatory and inhibitory neuronal processing at the columnar level in the human brain. This capability should be essential in studying the neural circuitry and brain function at the level of elementary cortical processing unit.

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References

  • Adriany G, Pfeuffer J, Yacoub E, Van de Moortele PF, Shmuel A, Anderson P, Hu X, Vaughan JT, Ugurbil K (2001) A half-volume transmit/receive coil combination for 7 Tesla applications. In: 9th International society for magnetic resonance in medicine annual meeting, Glasgow, UK, p 1097

  • Bandettini PA, Wong EC, Hinks RS, Tikofsky RS, Hyde JS (1992) Time course EPI of human brain function during task activation. Magn Reson Med 25:390–397

    Article  CAS  PubMed  Google Scholar 

  • Bandettini PA, Jesmanowicz A, Wong EC, Hyde JS (1993) Processing strategies for time-course data sets in functional MRI of the human brain. Magn Reson Med 30:161–173

    Article  CAS  PubMed  Google Scholar 

  • Blasdel GG, Lund JS, Fitzpatrick D (1985) Intrinsic connections of macaque striate cortex: axonal projections of cells outside lamina 4C. J Neurosci 5:3350–3369

    CAS  PubMed  Google Scholar 

  • Buchert M, Greenlee MW, Rutschmann RM, Kraemer FM, Luo F, Hennig J (2002) Functional magnetic resonance imaging evidence for binocular interactions in human visual cortex. Exp Brain Res 145:334–339

    Article  CAS  PubMed  Google Scholar 

  • Chen W, Zhu XH (2001) Correlation of activation sizes between lateral geniculate nucleus and primary visual cortex in humans. Magn Reson Med 45:202–205

    Article  CAS  PubMed  Google Scholar 

  • Chen W, Kato T, Zhu XH, Strupp J, Ogawa S, Ugurbil K (1998) Mapping of lateral geniculate nucleus activation during visual stimulation in human brain using fMRI. Magn Reson Med 39:89–96

    Article  CAS  PubMed  Google Scholar 

  • Chen W, Zhu XH, Thulborn KR, Ugurbil K (1999) Retinotopic mapping of lateral geniculate nucleus in humans using functional magnetic resonance imaging. Proc Natl Acad Sci USA 96:2430–2434

    Article  CAS  PubMed  Google Scholar 

  • Cheng K, Waggoner RA, Tanaka K (2001) Human ocular dominance columns as revealed by high-field functional magnetic resonance imaging. Neuron 32:359–374

    Article  CAS  PubMed  Google Scholar 

  • Das A, Gilbert CD (1999) Topography of contextual modulations mediated by short-range interactions in primary visual cortex. Nature 399:655–661

    Article  CAS  PubMed  Google Scholar 

  • Engel SA, Rumelhart DE, Wandell BA, Lee AT, Glover GH, Chichilnisky EJ, Shadlen MN (1994) fMRI of human visual cortex. Nature 369:525

    Article  CAS  PubMed  Google Scholar 

  • Eysel U (1999) Turning a corner in vision research. Nature 399(641):643–644

    Google Scholar 

  • Glover GH (1999) Deconvolution of impulse response in event-related BOLD fMRI. Neuroimage 9:416–429

    Article  CAS  PubMed  Google Scholar 

  • Goodyear BG, Menon RS (2001) Brief visual stimulation allows mapping of ocular dominance in visual cortex using fMRI. Hum Brain Mapp 14:210–217

    Article  CAS  PubMed  Google Scholar 

  • Goodyear BG, Nicolle DA, Menon RS (2002) High resolution fMRI of ocular dominance columns within the visual cortex of human amblyopes. Strabismus 10:129–136

    Article  PubMed  Google Scholar 

  • Haase A (1990) Snapshot FLASH MRI. Applications to T1, T2, and chemical-shift imaging. Magn Reson Med 13:77–89

    Article  CAS  PubMed  Google Scholar 

  • Haynes JD, Deichmann R, Rees G (2005) Eye-specific effects of binocular rivalry in the human lateral geniculate nucleus. Nature 438:496–499

    Article  CAS  PubMed  Google Scholar 

  • Hitchcock PF, Hickey TL (1980) Ocular dominance columns: evidence for their presence in humans. Brain Res 182:176–179

    Article  CAS  PubMed  Google Scholar 

  • Horton JC, Hedley-Whyte ET (1984) Mapping of cytochrome oxidase patches and ocular dominance columns in human visual cortex. Philos Trans R Soc Lond B Biol Sci 304:255–272

    Article  CAS  PubMed  Google Scholar 

  • Horton JC, Dagi LR, McCrane EP, de Monasterio FM (1990) Arrangement of ocular dominance columns in human visual cortex. Arch Ophthalmol 108:1025–1031

    CAS  PubMed  Google Scholar 

  • Hubel DH (1988) Eye, brain and vision. Scientific American Library, New York

    Google Scholar 

  • Hubel DH, Wiesel TN (1962) Receptive fields, binocular interaction and functional architecture in the cat’s visual cortex. J Physiol 160:106–154

    CAS  PubMed  Google Scholar 

  • Hubel DH, Wiesel TN (1968) Receptive fields and functional architecture of monkey striate cortex. J Physiol 195:215–243

    CAS  PubMed  Google Scholar 

  • Katz LC, Gilbert CD, Wiesel TN (1989) Local circuits and ocular dominance columns in monkey striate cortex. J Neurosci 9:1389–1399

    CAS  PubMed  Google Scholar 

  • Kennedy C, Des Rosiers MH, Sakurada O, Shinohara M, Reivich M, Jehle JW, Sokoloff L (1976) Metabolic mapping of the primary visual system of the monkey by means of the autoradiographic [14C]deoxyglucose technique. Proc Natl Acad Sci USA 73:4230–4234

    Article  CAS  PubMed  Google Scholar 

  • Kwong KK, Belliveau JW, Chesler DA, Goldberg IE, Weisskoff RM, Poncelet BP, Kennedy DN, Hoppel BE, Cohen MS, Turner R et al (1992) Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation. Proc Natl Acad Sci USA 89:5675–5679

    Article  CAS  PubMed  Google Scholar 

  • Leopold DA, Logothetis NK (1996) Activity changes in early visual cortex reflect monkeys’ percepts during binocular rivalry. Nature 379:549–553

    Article  CAS  PubMed  Google Scholar 

  • Logothetis NK, Schall JD (1989) Neuronal correlates of subjective visual perception. Science 245:761–763

    Article  CAS  PubMed  Google Scholar 

  • Lund JS, Angelucci A, Bressloff PC (2003) Anatomical substrates for functional columns in macaque monkey primary visual cortex. Cereb Cortex 13:15–24

    Article  PubMed  Google Scholar 

  • Menon RS, Goodyear BG (1999) Submillimeter functional localization in human striate cortex using BOLD contrast at 4 Tesla: implications for the vascular point-spread function. Magn Reson Med 41:230–235

    Article  CAS  PubMed  Google Scholar 

  • Menon RS, Ogawa S, Strupp JP, Ugurbil K (1997) Ocular dominance in human V1 demonstrated by functional magnetic resonance imaging. J Neurophysiol 77:2780–2787

    CAS  PubMed  Google Scholar 

  • Mitchison G, Crick F (1982) Long axons within the striate cortex: their distribution, orientation, and patterns of connection. Proc Natl Acad Sci USA 79:3661–3665

    Article  CAS  PubMed  Google Scholar 

  • Ogawa S, Tank DW, Menon R, Ellermann JM, Kim SG, Merkle H, Ugurbil K (1992) Intrinsic signal changes accompanying sensory stimulation: functional brain mapping with magnetic resonance imaging. Proc Natl Acad Sci USA 89:5951–5955

    Article  CAS  PubMed  Google Scholar 

  • Ogawa S, Lee TM, Stepnoski R, Chen W, Zhu XH, Ugurbil K (2000) An approach to probe some neural systems interaction by functional MRI at neural time scale down to milliseconds. Proc Natl Acad Sci USA 97:11026–11031

    Article  CAS  PubMed  Google Scholar 

  • Sereno MI, Dale AM, Reppas JB, Kwong KK, Belliveau JW, Brady TJ, Rosen BR, Tootell RB (1995) Borders of multiple visual areas in humans revealed by functional magnetic resonance imaging. Science 268:889–893

    Article  CAS  PubMed  Google Scholar 

  • Sheinberg DL, Logothetis NK (1997) The role of temporal cortical areas in perceptual organization. Proc Natl Acad Sci USA 94:3408–3413

    Article  CAS  PubMed  Google Scholar 

  • Sillito AM, Grieve KL, Jones HE, Cudeiro J, Davis J (1995) Visual cortical mechanisms detecting focal orientation discontinuities. Nature 378:492–496

    Article  CAS  PubMed  Google Scholar 

  • Strupp JP (1996) Stimulate: a GUI based fMRI analysis software package. Neuroimage 3:S607

    Article  Google Scholar 

  • Tong F, Engel SA (2001) Interocular rivalry revealed in the human cortical blind-spot representation. Nature 411:195–199

    Article  CAS  PubMed  Google Scholar 

  • Tootell RB, Hamilton SL, Silverman MS, Switkes E (1988) Functional anatomy of macaque striate cortex. I. Ocular dominance, binocular interactions, and baseline conditions. J Neurosci 8:1500–1530

    CAS  PubMed  Google Scholar 

  • Vidyasagar TR, Pei X, Volgushev M (1996) Multiple mechanisms underlying the orientation selectivity of visual cortical neurones. Trends Neurosci 19:272–277

    Article  CAS  PubMed  Google Scholar 

  • Weliky M, Kandler K, Fitzpatrick D, Katz LC (1995) Patterns of excitation and inhibition evoked by horizontal connections in visual cortex share a common relationship to orientation columns. Neuron 15:541–552

    Article  CAS  PubMed  Google Scholar 

  • Wunderlich K, Schneider KA, Kastner S (2005) Neural correlates of binocular rivalry in the human lateral geniculate nucleus. Nat Neurosci 8:1595–1602

    Article  CAS  PubMed  Google Scholar 

  • Xiong J, Gao JH, Lancaster JL, Fox PH (1995) Clustered pixels analysis for functional MRI activation studies of the human brain. Hum Brain Mapp 3:287–301

    Article  Google Scholar 

  • Yacoub E, Shmuel A, Logothetis N, Ugurbil K (2007) Robust detection of ocular dominance columns in humans using Hahn Spin Echo BOLD functional MRI at 7 Tesla. Neuroimage 37:1161–1177

    Article  PubMed  Google Scholar 

  • Zhang N, Chen W (2006) A dynamic fMRI study of illusory double-flash effect on human visual cortex. Exp Brain Res 172:57–66

    Google Scholar 

  • Zhang N, Zhu XH, Chen W (2005) Influence of gradient acoustic noise on fMRI response in the human visual cortex. Magn Reson Med 54:258–263

    Article  PubMed  Google Scholar 

  • Zhu XH, Zhang XL, Tang S, Ogawa S, Ugurbil K, Chen W (2001) Probing fast neuronal interaction in the human ocular dominate columns based on fMRI BOLD response at 7 Tesla. In: 9th International society for magnetic resonance in medicine annual meeting, Glasgow, UK, p 287

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Acknowledgments

The authors thank Drs. Ute Goerke and Gregor Adriany for their technical assistance. This work is supported in part by NIH grants of EB00329, NS41262, MH70800-01, EB00331, P41 RR08079 and P30NS057091; the W. M. Keck Foundation.

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Authors and Affiliations

  1. Department of Radiology, Center for Magnetic Resonance Research, University of Minnesota, School of Medicine, 2021 6th Street S.E., Minneapolis, MN, 55455, USA

    Xiao-Hong Zhu, Essa Yacoub, Kamil Ugurbil & Wei Chen

  2. Center for Comparative Neuroimaging (CCNI), University of Massachusetts Medical School, 55 Lake Avenue North, Worcester, MA, 01655, USA

    Nanyin Zhang

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  1. Nanyin Zhang
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  2. Xiao-Hong Zhu
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  3. Essa Yacoub
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  4. Kamil Ugurbil
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  5. Wei Chen
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Correspondence to Nanyin Zhang or Wei Chen.

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Zhang, N., Zhu, XH., Yacoub, E. et al. Functional MRI mapping neuronal inhibition and excitation at columnar level in human visual cortex. Exp Brain Res 204, 515–524 (2010). https://doi.org/10.1007/s00221-010-2318-z

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  • DOI: https://doi.org/10.1007/s00221-010-2318-z

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