Orientation Decoding Depends on Maps, Not Columns

The representation of orientation in primary visual cortex (V1) has been examined at a fine spatial scale corresponding to the columnar architecture. We present functional magnetic resonance imaging (fMRI) measurements providing evidence for a topographic map of orientation preference in human V1 at a much coarser scale, in register with the angular-position component of the retinotopic map of V1. This coarse-scale orientation map provides a parsimonious explanation for why multivariate pattern analysis methods succeed in decoding stimulus orientation from fMRI measurements, challenging the widely held assumption that decoding results reflect sampling of spatial irregularities in the fine-scale columnar architecture. Decoding stimulus attributes and cognitive states from fMRI measurements has proven useful for a number of applications, but our results demonstrate that the interpretation cannot assume decoding reflects or exploits columnar organization.

• Publication year

  2011

• Venue

  Journal of Neuroscience

• Publication date

  2011-03-30

• Fields of study

  Biology, Medicine, Psychology

• Identifiers
  DOI 10.1523/JNEUROSCI.5160-10.2011PMID 21451017PMCID PMC3086281
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

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• Mechanisms underlying decoding at 7 T: Ocular dominance columns, broad structures, and macroscopic blood vessels in V1 convey information on the stimulated eye

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• Orientation anisotropies in human visual cortex.

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  2008cited by this paper
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• Visual field maps in human cortex.

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• Two Retinotopic Visual Areas in Human Lateral Occipital Cortex

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• Beyond mind-reading: multi-voxel pattern analysis of fMRI data.

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• An oblique effect in human primary visual cortex

  2000influential reference
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  2000cited by this paper
• Investigation of low frequency drift in fMRI signal.

  1999influential reference
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  1997cited by this paper
• Orientation selectivity in pinwheel centers in cat striate cortex.

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  1996cited by this paper
• Mapping striate and extrastriate visual areas in human cerebral cortex.

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• Borders of multiple visual areas in humans revealed by functional magnetic resonance imaging.

  1995cited by this paper
• fMRI of human visual cortex

  1994cited by this paper
• Heuristic filtering and reliable calibration methods for video-based pupil-tracking systems

  1993cited by this paper
• Orientation bias of neurons in the lateral geniculate nucleus of macaque monkeys

  1990cited by this paper
• Brain magnetic resonance imaging with contrast-dependent oxygenation

  1990cited by this paper
• Brain magnetic resonance imaging with contrast dependent on blood oxygenation.

  1990cited by this paper
• Functional architecture of cortex revealed by optical imaging of intrinsic signals

  1986cited by this paper
• Voltage-sensitive dyes reveal a modular organization in monkey striate cortex

  1986cited by this paper
• Retinal constraints on orientation specificity in cat visual cortex

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  1985cited by this paper
• Relationship between preferred orientation and receptive field position of neurons in cat striate cortex

  1983cited by this paper
• Resolution of gratings oriented along and across meridians in peripheral vision.

  1982cited by this paper
• The orientation and direction selectivity of cells in macaque visual cortex.

  1982cited by this paper
• Analysis of orientation bias in cat retina

  1982cited by this paper
• Orientation bias of cat retinal ganglion cells

  1980cited by this paper
• Receptive-field characteristics of neurons in cat striate cortex: Changes with visual field eccentricity.

  1976cited by this paper
• Neural Basis of Orientation Perception in Primate Vision

  1974cited by this paper
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