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Cited by 194Visual perception and processing mechanismsAdvanced MRI Techniques and ApplicationsAdvanced Neuroimaging Techniques and Applications

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Layer-Specific fMRI Reflects Different Neuronal Computations at Different Depths in Human V1

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Olman, Cheryl A., Harel, Noam, Feinberg, David A., He, Sheng, Zhang, Peng, Ugurbil, Kamil, Yacoub, Essa·2012·PLoS ONE
DOI 10.1371/journal.pone.0032536PMC PMC3308958
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Abstract

Recent work has established that cerebral blood flow is regulated at a spatial scale that can be resolved by high field fMRI to show cortical columns in humans. While cortical columns represent a cluster of neurons with similar response properties (spanning from the pial surface to the white matter), important information regarding neuronal interactions and computational processes is also contained within a single column, distributed across the six cortical lamina. A basic understanding of underlying neuronal circuitry or computations may be revealed through investigations of the distribution of neural responses at different cortical depths. In this study, we used T(2)-weighted imaging with 0.7 mm (isotropic) resolution to measure fMRI responses at different depths in the gray matter while human subjects observed images with either recognizable or scrambled (physically impossible) objects. Intact and scrambled images were partially occluded, resulting in clusters of activity distributed across primary visual cortex. A subset of the identified clusters of voxels showed a preference for scrambled objects over intact; in these clusters, the fMRI response in middle layers was stronger during the presentation of scrambled objects than during the presentation of intact objects. A second experiment, using stimuli targeted at either the magnocellular or the parvocellular visual pathway, shows that laminar profiles in response to parvocellular-targeted stimuli peak in more superficial layers. These findings provide new evidence for the differential sensitivity of high-field fMRI to modulations of the neural responses at different cortical depths.

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Crossref · 10.1371/journal.pone.0032536

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Figures

Figure 1 Volume coverage and activation of fMRI experiment with 0.7 mm resolution. Left: location of functional data is illustrated on a sagittal section. Right: activation maps from a single subject in response to both intact (bottom left, black outline) and scrambled objects (contrast is all-stimuli vs. blank, p<0.01, uncorrected, minimum cluster size 4 voxels).
Figure 1 Volume coverage and activation of fMRI experiment with 0.7 mm resolution. Left: location of functional data is illustrated on a sagittal section. Right: activation maps from a single subject in response to both intact (bottom left, black outline) and scrambled objects (contrast is all-stimuli vs. blank, p<0.01, uncorrected, minimum cluster size 4 voxels).CC BY · PubMed Central
Figure 2 Laminar profiles of BOLD responses for significantly modulated voxels in V1. a.) Solid lines represent mean across repeated scans, shading indicates standard error across scans. Dashed lines represent average fMRI response in WM voxels. Significance threshold for defining activated voxels was adjusted for each subject to ensure a minimum of 300 voxels were included in the profile. S1: 1014/3287 voxels in V1 had p<0.001 (estimated by permutation analysis), 7 scans were averaged per condition; S2: 332/2036 V1 voxels with p<0.01, 5 scans per condition; S3: 325/1429 voxels in V1 with p<0.05, 5 scans per condition. b.) The control experiment included a set of scans in which the contrast of the intact objects reduced (image on top, right; blue laminar profiles). S4: 825/2953 of V1 voxels with p<0.001, 7 scans per condition; S5: 317/2126 of V1 voxels with p<0.05, 4 scans per condition.
Figure 2 Laminar profiles of BOLD responses for significantly modulated voxels in V1. a.) Solid lines represent mean across repeated scans, shading indicates standard error across scans. Dashed lines represent average fMRI response in WM voxels. Significance threshold for defining activated voxels was adjusted for each subject to ensure a minimum of 300 voxels were included in the profile. S1: 1014/3287 voxels in V1 had p<0.001 (estimated by permutation analysis), 7 scans were averaged per condition; S2: 332/2036 V1 voxels with p<0.01, 5 scans per condition; S3: 325/1429 voxels in V1 with p<0.05, 5 scans per condition. b.) The control experiment included a set of scans in which the contrast of the intact objects reduced (image on top, right; blue laminar profiles). S4: 825/2953 of V1 voxels with p<0.001, 7 scans per condition; S5: 317/2126 of V1 voxels with p<0.05, 4 scans per condition.CC BY · PubMed Central
Figure 3 An example of a selected cluster of significantly modulated voxels. Voxels most strongly modulated by stimulus presentation (p<0.001) are shown overlaid on the T1-weighted anatomical reference, illustrating adherence of activation to GM. Map on lower right indicates probability that part of an intact or scrambled object occurred in each region of the visual field; image subtends ±7.6°. Green arrows indicate one region of interes and corresponding visual field location. Laminar profiles are shown with shading indicating standard error, 7 scans.
Figure 3 An example of a selected cluster of significantly modulated voxels. Voxels most strongly modulated by stimulus presentation (p<0.001) are shown overlaid on the T1-weighted anatomical reference, illustrating adherence of activation to GM. Map on lower right indicates probability that part of an intact or scrambled object occurred in each region of the visual field; image subtends ±7.6°. Green arrows indicate one region of interes and corresponding visual field location. Laminar profiles are shown with shading indicating standard error, 7 scans.CC BY · PubMed Central
Figure 4 Differential laminar profiles of clusters sorted according to whether the average response to intact or scrambled objects was greater. a.) Regions of interest responding more strongly to intact objects were observed in 4 scanning sessions (colors of thin trace indicate different subjects). No main effect of depth is observed, although there is a statistically insignificant pattern of stronger responses to objects in deeper layers. b.) Regions of interest responding more strongly to objects were observed in 3 scanning sessions.
Figure 4 Differential laminar profiles of clusters sorted according to whether the average response to intact or scrambled objects was greater. a.) Regions of interest responding more strongly to intact objects were observed in 4 scanning sessions (colors of thin trace indicate different subjects). No main effect of depth is observed, although there is a statistically insignificant pattern of stronger responses to objects in deeper layers. b.) Regions of interest responding more strongly to objects were observed in 3 scanning sessions.CC BY · PubMed Central
Figure 5 Visual responses to parvocellular-targeted stimuli are maximally differentiated from magnocellular-targeted stimuli in superficial gray matter. Full-field visual stimuli were targeted at the parvocellular pathway (P stim: 2 Hz contrast-reversing circular gratings composed of 1 cycle per degree iso-luminant red and green checks) and the magnocellular pathway (M stim: 15 Hz contrast-reversing gratings with 0.3 cycles per degree sinusoidal luminance modulation). Green lines indicate estimated BOLD response to P stimuli (shading indicates standard error across 6 or 8 scans in each subject, respectively); black lines indicate estimated BOLD response to M stimuli. Asterisks indicate significance at a given cortical depth (p<0.05, paired t-test, corrected for 10 comparisons in the 5 depth bins, 2 subjects); daggers indicate p<0.1, corrected.
Figure 5 Visual responses to parvocellular-targeted stimuli are maximally differentiated from magnocellular-targeted stimuli in superficial gray matter. Full-field visual stimuli were targeted at the parvocellular pathway (P stim: 2 Hz contrast-reversing circular gratings composed of 1 cycle per degree iso-luminant red and green checks) and the magnocellular pathway (M stim: 15 Hz contrast-reversing gratings with 0.3 cycles per degree sinusoidal luminance modulation). Green lines indicate estimated BOLD response to P stimuli (shading indicates standard error across 6 or 8 scans in each subject, respectively); black lines indicate estimated BOLD response to M stimuli. Asterisks indicate significance at a given cortical depth (p<0.05, paired t-test, corrected for 10 comparisons in the 5 depth bins, 2 subjects); daggers indicate p<0.1, corrected.CC BY · PubMed Central

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Research works printed but not linked: 2

  1. G Adriany, 2001, A half-volume transmit/receive coil combination for 7 Tesla applications., Glasgow, 1097
  2. DA Feinberg, 2008, Sub-millimeter single-shot 3D GRASE with inner volume selection for T2-weighted fMRI applications at 7 Tesla., Toronto

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Metadata

Authors
Olman, C. A., Harel, N., Feinberg, D. A., He, S., Zhang, P., Ugurbil, K., & Yacoub, E.
Affiliations
  • University of Minnesota (US)
  • Advanced MRI Technologies (United States) (US)
Corresponding author
Yacoub, Essa
ORCID
Venue
PLoS ONE
Publisher
Public Library of Science (PLoS)
Published
2012-03-20
Volume
7
Issue
3
Pages
e32536
ISSN
1932-6203 (ISSN-L)
DOI
10.1371/journal.pone.0032536
PMC
PMC3308958
OpenAlex
W2062819254
Cited by
194
References
37
Citations by year
2026: 4 · 2025: 14 · 2024: 13 · 2023: 8 · 2022: 9 · 2021: 21 · 2020: 18 · 2019: 12 · 2018: 11 · 2017: 25 · 2016: 22 · 2015: 12 · 2014: 8 · 2013: 13 · 2012: 3
FWCI
5.89
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • RePEc: Research Papers in Economics (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Figshare (submittedVersion, cc-by)
Funders
  • National Science Foundation (P30 NS057091, 9907842)
  • W. M. Keck Foundation
  • National Institutes of Health (S10 RR1395, RR08079)
  • National Institute of Mental Health (R01MH070800)
  • National Eye Institute (R01EY015261)
  • National Institute of Neurological Disorders and Stroke (R44NS063537, P30NS057091)
  • National Institute of Biomedical Imaging and Bioengineering (R01EB008645, R01EB000331)
  • National Center for Research Resources (S10-RR1395, P41RR001395, P41RR008079, P41RR08079)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
  • Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced MRI Techniques and Applications
  • Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced Neuroimaging Techniques and Applications
Keywords
primary visual cortex, cortical depth, high-field fMRI, visual object recognition, occlusion, magnocellular pathway, parvocellular pathway, neural circuits
MeSH terms
Adult, Brain Mapping, Cerebral Cortex, Cerebrovascular Circulation, Data Interpretation, Statistical, Female, Humans, Image Processing, Computer-Assisted, Magnetic Resonance Imaging, Male, Neurons, Oxygen

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