Spatiotopic adaptation in visual areas
Open accessAbstract
UNLABELLED: The ability to perceive the visual world around us as spatially stable despite frequent eye movements is one of the long-standing mysteries of neuroscience. The existence of neural mechanisms processing spatiotopic information is indispensable for a successful interaction with the external world. However, how the brain handles spatiotopic information remains a matter of debate. We here combined behavioral and fMRI adaptation to investigate the coding of spatiotopic information in the human brain. Subjects were adapted by a prolonged presentation of a tilted grating. Thereafter, they performed a saccade followed by the brief presentation of a probe. This procedure allowed dissociating adaptation aftereffects at retinal and spatiotopic positions. We found significant behavioral and functional adaptation in both retinal and spatiotopic positions, indicating information transfer into a spatiotopic coordinate system. The brain regions involved were located in ventral visual areas V3, V4, and VO. Our findings suggest that spatiotopic representations involved in maintaining visual stability are constructed by dynamically remapping visual feature information between retinotopic regions within early visual areas. SIGNIFICANCE STATEMENT: Why do we perceive the visual world as stable, although we constantly perform saccadic eye movements? We investigated how the visual system codes object locations in spatiotopic (i.e., external world) coordinates. We combined visual adaptation, in which the prolonged exposure to a specific visual feature alters perception, with fMRI adaptation, where the repeated presentation of a stimulus leads to a reduction in the BOLD amplitude. Functionally, adaptation was found in visual areas representing the retinal location of an adaptor but also at representations corresponding to its spatiotopic position. The results suggest that an active dynamic shift transports information in visual cortex to counteract the retinal displacement associated with saccade eye movements.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The brain uses visual information in both retinotopic and spatiotopic coordinate systems.
“Although action and perception use the transformed spatiotopic coordinates, there is experimental evidence that the brain uses visual information in both retinotopic [9] and spatiotopic [10] coordinate systems.”
From Eye movements and the perceived location of phosphenes generated by intracranial primary visual cortex stimulation in the blind (2021) · cites this paper as [10]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Fischl, B. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2012.01.021 · Cited by 9,526 · see citing works
A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data
Eickhoff, S. B., Stephan, K. E., Mohlberg, H., Grefkes, C., Fink, G. R., Amunts, K., & Zilles, K. (2005) · NeuroImage · doi:10.1016/j.neuroimage.2004.12.034 · Cited by 4,033 · see citing works
Self-citationBorders of Multiple Visual Areas in Humans Revealed by Functional Magnetic Resonance Imaging
Sereno, M. I., Dale, A. M., Reppas, J. B., Kwong, K. K., Belliveau, J. W., Brady, T. J., Rosen, B. R., & Tootell, R. B. H. (1995) · Science · doi:10.1126/science.7754376 · Cited by 2,658 · see citing works
The updating of the representation of visual space in parietal cortex by intended eye movements
Duhamel, J.-R., Colby, C. L., & Goldberg, M. E. (1992) · Science · doi:10.1126/science.1553535 · Cited by 1,966 · see citing works
Retinotopic organization in human visual cortex and the spatial precision of functional MRI
Engel, S. A. (1997) · Cerebral Cortex · doi:10.1093/cercor/7.2.181 · Cited by 1,606 · see citing works
PEST: Efficient Estimates on Probability Functions
Taylor, M. M., & Creelman, C. D. (1967) · The Journal of the Acoustical Society of America · doi:10.1121/1.1910407 · Cited by 1,173 · see citing works
Zipser, D., & Andersen, R. A. (1988) · Nature · doi:10.1038/331679a0 · Cited by 1,172 · see citing works
Mapping striate and extrastriate visual areas in human cerebral cortex.
DeYoe, E. A., Carman, G. J., Bandettini, P. A., Glickman, S., Wieser, J., Cox, R. W., Miller, D. A., & Jay Neitz, A. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.6.2382 · Cited by 1,047 · see citing works
Engel, S. A., Rumelhart, D. E., Wandell, B. A., Lee, A. T.-J., Glover, G. H., Chichilnisky, E. J., & Shadlen, M. N. (1994) · Nature · doi:10.1038/369525a0 · Cited by 977 · see citing works
Two Retinotopic Visual Areas in Human Lateral Occipital Cortex
Larsson, J. T., & Heeger, D. J. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.1657-06.2006 · Cited by 564 · see citing works
Adaptation: from single cells to BOLD signals
Krekelberg, B., Boynton, G. M., & Wezel, R. J. A. V. (2006) · Trends in Neurosciences · doi:10.1016/j.tins.2006.02.008 · Cited by 496 · see citing works
Visual Topography of Human Intraparietal Sulcus
Swisher, J. D., Halko, M. A., Merabet, L. B., McMains, S. A., & Somers, D. C. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.0991-07.2007 · Cited by 456 · see citing works
Updating of the visual representation in monkey striate and extrastriate cortex during saccades
Nakamura, K., & Colby, C. L. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.052379899 · Cited by 438 · see citing works
Spatial Updating in Human Parietal Cortex
Merriam, E. P., Genovese, C. R., & Colby, C. L. (2003) · Neuron · doi:10.1016/s0896-6273(03)00393-3 · Cited by 305 · see citing works
Parietal neurons encoding spatial locations in craniotopic coordinates
Galletti, C., Battaglini, P. P., & Fattori, P. (1993) · Experimental Brain Research · doi:10.1007/bf00227102 · Cited by 287 · see citing works
A functional angle on some after-effects in cortical vision
Clifford, C. W. G., Wenderoth, P., & Špehar, B. (2000) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2000.1198 · Cited by 242 · see citing works
The Radial Bias: A Different Slant on Visual Orientation Sensitivity in Human and Nonhuman Primates
Sasaki, Y., Rajimehr, R., Kim, B. W., Ekstrom, L. B., Vanduffel, W., & Tootell, R. B. H. (2006) · Neuron · doi:10.1016/j.neuron.2006.07.021 · Cited by 195 · see citing works
Maps of visual space in human occipital cortex are retinotopic, not spatiotopic
Gardner, J. L., Merriam, E. P., Movshon, J. A., & Heeger, D. J. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.5476-07.2008 · Cited by 192 · see citing works
The Native Coordinate System of Spatial Attention Is Retinotopic
Golomb, J. D., Chun, M. M., & Mazer, J. A. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.2525-08.2008 · Cited by 189 · see citing works
Gaze direction controls response gain in primary visual-cortex neurons
Trotter, Y., & Celebrini, S. (1999) · Nature · doi:10.1038/18444 · Cited by 188 · see citing works
Remapping in Human Visual Cortex
Merriam, E. P., Genovese, C. R., & Colby, C. L. (2006) · Journal of Neurophysiology · doi:10.1152/jn.00189.2006 · Cited by 186 · see citing works
Spatiotopic Transfer of Visual-Form Adaptation across Saccadic Eye Movements
Melcher, D. (2005) · Current Biology · doi:10.1016/j.cub.2005.08.044 · Cited by 185 · see citing works
Modulation of Neural Stereoscopic Processing in Primate Area V1 by the Viewing Distance
Trotter, Y., Celebrini, S., Stricanne, B., Thorpe, S. J., & Imbert, M. (1992) · Science · doi:10.1126/science.1519066 · Cited by 175 · see citing works
Spatiotopic selectivity of BOLD responses to visual motion in human area MT
d’Avossa, G., Tosetti, M., Crespi, S. A., Biagi, L., Burr, D. C., & Morrone, M. C. (2006) · Nature Neuroscience · doi:10.1038/nn1824 · Cited by 166 · see citing works
Orientation-Specific Adaptation in Human Visual Cortex
Boynton, G. M., & Finney, E. M. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-25-08781.2003 · Cited by 164 · see citing works
Higher Level Visual Cortex Represents Retinotopic, Not Spatiotopic, Object Location
Golomb, J. D., & Kanwisher, N. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhr357 · Cited by 141 · see citing works
Neuronal mechanisms for visual stability: progress and problems
Wurtz, R. H., Joiner, W. M., & Berman, R. A. (2011) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2010.0186 · Cited by 140 · see citing works
Spatiotopic coding and remapping in humans
Burr, D. C., & Morrone, M. C. (2011) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2010.0244 · Cited by 139 · see citing works
Correspondences between retinotopic areas and myelin maps in human visual cortex
Abdollahi, R. O., Kolster, H., Glasser, M. F., Robinson, E. C., Coalson, T. S., Dierker, D., Jenkinson, M., Van Essen, D. C., & Orban, G. A. (2014) · NeuroImage · doi:10.1016/j.neuroimage.2014.06.042 · Cited by 126 · see citing works
Self-citationDistance Modulation of Neural Activity in the Visual Cortex
Dobbins, A. C., Jeo, R. M., Fiser, J., & Allman, J. M. (1998) · Science · doi:10.1126/science.281.5376.552 · Cited by 115 · see citing works
The Effect of Gaze Angle and Fixation Distance on the Responses of Neurons in V1, V2, and V4
Rosenbluth, D., & Allman, J. M. (2002) · Neuron · doi:10.1016/s0896-6273(01)00559-1 · Cited by 91 · see citing works
Spatiotopic coding of BOLD signal in human visual cortex depends on spatial attention
Crespi, S., Biagi, L., d'Avossa, G., Burr, D. C., Tosetti, M., & Morrone, M. C. (2011) · PLoS ONE · doi:10.1371/journal.pone.0021661 · Cited by 89 · see citing works
Kourtzi, Z., & Huberle, E. (2005) · NeuroImage · doi:10.1016/j.neuroimage.2005.06.017 · Cited by 88 · see citing works
McKyton, A., & Zohary, E. (2007) · Cerebral Cortex · doi:10.1093/cercor/bhl027 · Cited by 88 · cited 3× · see citing works
“Although area MT (d’Avossa et al., 2006; Crespi et al., 2011) and lateral occipital cortex (McKyton and Zohary, 2007) have been reported to contain object representations in external world coordinates, other studies seriously questioned the existence of spatiotopic maps in the human brain (Gardner…”
BackgroundSpatiotopic neural representations develop slowly across saccades
Zimmermann, E., Morrone, M. C., Fink, G. R., et al. (2013) · Current Biology · doi:10.1016/j.cub.2013.01.065 · Cited by 69 · see citing works
Self-citationSpatiotopic perceptual maps in humans: evidence from motion adaptation
Turi, M., & Burr, D. C. (2012) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2012.0637 · Cited by 65 · see citing works
Chapter 15 Selective gene expression after brain ischemia
Abe, K., & Kogure, K. (1993) · Progress in brain research · doi:10.1016/s0079-6123(08)63269-0 · Cited by 64 · see citing works
Modulation of Visual Responses by Gaze Direction in Human Visual Cortex
Merriam, E. P., Gardner, J. L., Movshon, J. A., & Heeger, D. J. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.0500-12.2013 · Cited by 51 · see citing works
How Predation and Landscape Fragmentation Affect Vole Population Dynamics
Dalkvist, T., Sibly, R. M., & Topping, C. J. (2011) · PLoS ONE · doi:10.1371/journal.pone.0022834 · Cited by 49 · see citing works
Eye position-dependent activation of neurones in striate cortex of macaque
Guo, K., & Li, C. (1997) · Neuroreport · doi:10.1097/00001756-199704140-00017 · Cited by 47 · see citing works
Privileged Processing of the Straight-Ahead Direction in Primate Area V1
Durand, J., Trotter, Y., & Celebrini, S. (2010) · Neuron · doi:10.1016/j.neuron.2010.03.014 · Cited by 45 · see citing works
Spatially Specific fMRI Repetition Effects in Human Visual Cortex
Murray, S. O., Olman, C. A., & Kersten, D. (2006) · Journal of Neurophysiology · doi:10.1152/jn.01236.2005 · Cited by 38 · see citing works
Another visual illusion involving orientation
Blake, R., Holopigian, K., & Jauch, M. (1985) · Vision Research · doi:10.1016/0042-6989(85)90225-1 · Cited by 15 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Caspi, A., Barry, M. P., Patel, U. K., Salas, M. A., Dorn, J. D., Roy, A., Niketeghad, S., Greenberg, R. J., & Pouratian, N. (2021) · Brain Stimulation · doi:10.1016/j.brs.2021.04.019 · Cited by 32 · see citing works
- Authors
- Zimmermann, E., Weidner, R., Abdollahi, R. O., & Fink, G. R.
- Affiliations
- Forschungszentrum Jülich (DE)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2016-09-14
- Volume
- 36
- Issue
- 37
- Pages
- 9526-9534
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6601937
- OpenAlex
- W2520625802
- Cited by
- 33
- References
- 43
- Citations by year
- 2026: 3 · 2025: 1 · 2024: 1 · 2023: 3 · 2022: 2 · 2021: 8 · 2020: 4 · 2019: 5 · 2018: 3 · 2017: 3
- FWCI
- 2.33
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Kölner Universitäts PublikationsServer (Universität zu Köln) (publishedVersion)
- JuSER (Forschungszentrum Jülich) (submittedVersion)
- Funders
- Deutsche Forschungsgemeinschaft (ZI 1456, ZI 1456/3-1)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Motor Control and Adaptation
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Multisensory perception and integration
- Keywords
- spatiotopic representation, retinotopic map, saccades, visual stability, adaptation aftereffects, tilted gratings, ventral visual cortex, V3, V4, VO
- MeSH terms
- Adaptation, Physiological, Adult, Analysis of Variance, Brain Mapping, Eye Movements, Female, Humans, Image Processing, Computer-Assisted, Magnetic Resonance Imaging, Male, Oxygen, Photic Stimulation, Space Perception, Visual Cortex, Visual Pathways
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review