The Segmentation of Proto-Objects in the Monkey Primary Visual Cortex
Open accessAbstract
During visual perception, the brain enhances the representations of image regions that belong to figures and suppresses those that belong to the background. Natural images contain many regions that initially appear to be part of a figure when analyzed locally (proto-objects) but are actually part of the background if the whole image is considered. These proto-grounds must be correctly assigned to the background to allow correct shape identification and guide behavior. To understand how the brain resolves this conflict between local and global processing, we recorded neuronal activity from the primary visual cortex (V1) of macaque monkeys while they discriminated between n/u shapes that have a central proto-ground region. We studied the fine-grained spatiotemporal profile of neural activity evoked by the n/u shape and found that neural representation of the object proceeded from a coarse-to-fine resolution. Approximately 100 ms after the stimulus onset, the representation of the proto-ground region was enhanced together with the rest of the n/u surface, but after ∼115 ms, the proto-ground was suppressed back to the level of the background. Suppression of the proto-ground was only present in animals that had been trained to perform the shape-discrimination task, and it predicted the choice of the animal on a trial-by-trial basis. Attention enhanced figure-ground modulation, but it had no effect on the strength of proto-ground suppression. The results indicate that the accuracy of scene segmentation is sharpened by a suppressive process that resolves local ambiguities by assigning proto-grounds to the background.
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?
Multiple tethered wired UEAs have been implanted in the visual cortex of monkeys and these implants allow monkeys to recognize simple shapes, motions, and letters.
“Multiple tethered wired UEAs have been already implanted in the visual cortex of monkeys (14, 40, 46) and these UEA implants allow monkeys to recognize simple shapes, motions, and letters (14).”
From Visual percepts evoked with an intracortical 96-channel microelectrode array inserted in human occipital cortex (2021) · cites this paper as [40]
Training history and surgical details (p. 14) reports multiple microelectrode arrays implanted over the monkeys’ V1, and the Introduction (p. 5) reports that the monkeys discriminated n/u shapes. The arrays recorded neural activity; the paper does not say they enabled recognition, nor does it report recognition of motion or other letters. (LLM, conf=0.88)
Experimental — accuracy not yet measuredPrevious studies in monkeys and humans demonstrated that the thresholds for phosphene perception in areas V1 and V2 are similar and that the quality of the percepts elicited is comparable.
“Previous studies in monkeys and humans demonstrated that the thresholds for phosphene perception in areas V1 and V2 are similar and that the quality of the percepts that are elicited are comparable (14, 3840).”
From Visual percepts evoked with an intracortical 96-channel microelectrode array inserted in human occipital cortex (2021) · cites this paper as [40]
The In Brief section (p. 2) and Introduction (p. 5) describe recordings of V1 activity during shape discrimination in monkeys. A search for phosphene thresholds, V2, and the quality of stimulation-elicited percepts found no passage addressing the claimed comparison between V1 and V2 in monkeys and humans. (LLM, conf=0.76)
Experimental — accuracy not yet measuredThese implants in monkey visual cortex are providing a better understanding of how the brain enhances the representations of visual objects in different visual regions.
“these implants are providing a better understanding of how the brain enhances the representations of visual objects in different visual regions (Klink et al., 2017; Self et al., 2019).”
From Toward Long-Term Communication With the Brain in the Blind by Intracortical Stimulation: Challenges and Future Prospects (2020) · cites this paper as Self et al., 2019
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
Principles Of Gestalt Psychology
Koffka, K. (2013) · Routledge eBooks · doi:10.4324/9781315009292 · Cited by 4,281 · see citing works
Laws of organization in perceptual forms.
Wertheimer, M. (1938) · Kegan Paul, Trench, Trubner & Company eBooks · doi:10.1037/11496-005 · Cited by 1,507 · see citing works
Attention improves performance primarily by reducing interneuronal correlations
Cohen, M. R., & Maunsell, J. H. R. (2009) · Nature Neuroscience · doi:10.1038/nn.2439 · Cited by 1,126 · see citing works
The Dynamic Representation of Scenes
Rensink, R. A. (2000) · Visual Cognition · doi:10.1080/135062800394667 · Cited by 1,079 · see citing works
Neuronal responses to static texture patterns in area V1 of the alert macaque monkey
Knierim, J. J., & Essen, D. C. V. (1992) · Journal of Neurophysiology · doi:10.1152/jn.1992.67.4.961 · Cited by 1,052 · see citing works
A relationship between behavioral choice and the visual responses of neurons in macaque MT
Britten, K. H., Newsome, W. T., Shadlen, M. N., Celebrini, S., & Movshon, J. A. (1996) · Visual Neuroscience · doi:10.1017/s095252380000715x · Cited by 1,049 · see citing works
The neurophysiology of figure-ground segregation in primary visual cortex
Lamme, V. (1995) · The Journal of Neuroscience · doi:10.1523/jneurosci.15-02-01605.1995 · Cited by 946 · see citing works
Contextual modulation in primary visual cortex
Zipser, K., Lamme, V. A. F., & Schiller, P. H. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-22-07376.1996 · Cited by 873 · see citing works
Coding of Border Ownership in Monkey Visual Cortex
Zhou, H., Friedman, H. S., & von der Heydt, R. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-17-06594.2000 · Cited by 727 · see citing works
Principles of Gestalt Psychology.
Reiser, O. L., & Koffka, K. (1936) · The Philosophical Review · doi:10.2307/2180493 · Cited by 497 · see citing works
Two distinct modes of sensory processing observed in monkey primary visual cortex (V1)
Supèr, H., Spekreijse, H., & Lamme, V. A. F. (2001) · Nature Neuroscience · doi:10.1038/85170 · Cited by 467 · see citing works
CORTICAL ALGORITHMS FOR PERCEPTUAL GROUPING
Roelfsema, P. R. (2006) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.29.051605.112939 · Cited by 426 · see citing works
Self-citationCavanaugh, J. R., Bair, W., & Movshon, J. A. (2002) · Journal of Neurophysiology · doi:10.1152/jn.00693.2001 · Cited by 426 · see citing works
Orientation-selective inhibition from beyond the classic visual receptive field
Nelson, J. I., & Frost, B. J. (1978) · Brain Research · doi:10.1016/0006-8993(78)90937-x · Cited by 396 · see citing works
Decision-related activity in sensory neurons reflects more than a neuron’s causal effect
Nienborg, H., & Cumming, B. G. (2009) · Nature · doi:10.1038/nature07821 · Cited by 360 · see citing works
Cue-Invariant Shape Selectivity of Macaque Inferior Temporal Neurons
Sáry, G., Vogels, R., & Orban, G. A. (1993) · Science · doi:10.1126/science.8493538 · Cited by 311 · see citing works
Lamme, V. A. F. (1999) · Cerebral Cortex · doi:10.1093/cercor/9.4.406 · Cited by 262 · see citing works
Figure—Ground Segregation in a Recurrent Network Architecture
Roelfsema, P. R., Lamme, V. A. F., Spekreijse, H., & Bosch, H. (2002) · Journal of Cognitive Neuroscience · doi:10.1162/08989290260045756 · Cited by 254 · see citing works
Self-citationDistinct Roles of the Cortical Layers of Area V1 in Figure-Ground Segregation
Self, M. W., van Kerkoerle, T., Supèr, H., & Roelfsema, P. R. (2013) · Current Biology · doi:10.1016/j.cub.2013.09.013 · Cited by 249 · see citing works
Self-citationExperience-dependent sharpening of visual shape selectivity in inferior temporal cortex.
Freedman, D. J., Riesenhuber, M., Poggio, T., & Miller, E. (2005) · Cerebral Cortex · doi:10.1093/cercor/bhj100 · Cited by 241 · see citing works
Learning to Link Visual Contours
Li, W., Piëch, V., & Gilbert, C. D. (2008) · Neuron · doi:10.1016/j.neuron.2007.12.011 · Cited by 227 · see citing works
The Role of Attention in Figure-Ground Segregation in Areas V1 and V4 of the Visual Cortex
Poort, J., Raudies, F., Wannig, A., Lamme, V. A. F., Heiko Neumann, B., & Roelfsema, P. R. (2012) · Neuron · doi:10.1016/j.neuron.2012.04.032 · Cited by 222 · see citing works
Self-citationFigure-ground mechanisms provide structure for selective attention
Qiu, F. T., Sugihara, T., & von der Heydt, R. (2007) · Nature Neuroscience · doi:10.1038/nn1989 · Cited by 218 · see citing works
Contextual Modulation in Primary Visual Cortex of Macaques
Rossi, A. F., Desimone, R., & Ungerleider, L. G. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-05-01698.2001 · Cited by 194 · see citing works
Different glutamate receptors convey feedforward and recurrent processing in macaque V1
Self, M. W., Kooijmans, R. N., Supèr, H., Lamme, V. A., & Roelfsema, P. R. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1119527109 · Cited by 184 · see citing works
Self-citationChronic multiunit recordings in behaving animals: advantages and limitations
Supèr, H., & Roelfsema, P. R. (2004) · Progress in brain research · doi:10.1016/s0079-6123(04)47020-4 · Cited by 180 · see citing works
Self-citationPerceptual training continuously refines neuronal population codes in primary visual cortex
Yan, Y., Rasch, M. J., Chen, M., Xiang, X., Huang, M., Wu, S., & Li, W. (2014) · Nature Neuroscience · doi:10.1038/nn.3805 · Cited by 157 · see citing works
Distributed Neural Plasticity for Shape Learning in the Human Visual Cortex
Kourtzi, Z., Betts, L. R., Sarkheil, P., & Welchman, A. E. (2005) · PLoS Biology · doi:10.1371/journal.pbio.0030204 · Cited by 152 · see citing works
Shape recognition contributions to figure-ground reversal: Which route counts?
Peterson, M. A., Harvey, E. M., & Weidenbacher, H. J. (1991) · Journal of Experimental Psychology Human Perception & Performance · doi:10.1037//0096-1523.17.4.1075 · Cited by 126 · see citing works
Linking Neuronal and Behavioral Performance in a Reaction-Time Visual Detection Task
Palmer, C., Cheng, S.-Y., & Seidemann, E. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.1940-07.2007 · Cited by 116 · see citing works
Nienborg, H., & Cumming, B. G. (2010) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2010.05.002 · Cited by 98 · see citing works
Response profiles to texture border patterns in area V1
Nothdurft, H., Gallant, J. L., & Essen, D. C. V. (2000) · Visual Neuroscience · doi:10.1017/s0952523800173092 · Cited by 93 · see citing works
Brightness contrast as a function of figure-ground relations.
Coren, S. (1969) · Journal of Experimental Psychology · doi:10.1037/h0027435 · Cited by 85 · see citing works
Shape recognition contributions to figure-ground reversal: Which route counts?
Peterson, M. A., Harvey, E. M., & Weidenbacher, H. J. (1991) · Journal of Experimental Psychology Human Perception & Performance · doi:10.1037/0096-1523.17.4.1075 · Cited by 85 · see citing works
Poort, J., Self, M. W., van Vugt, B., Malkki, H. A. I., & Roelfsema, P. R. (2016) · Cerebral Cortex · doi:10.1093/cercor/bhw235 · Cited by 84 · see citing works
Self-citationFigure–ground organization and the emergence of proto-objects in the visual cortex
von der Heydt, R. (2015) · Frontiers in Psychology · doi:10.3389/fpsyg.2015.01695 · Cited by 76 · see citing works
Boundary assignment in a recurrent network architecture
Jehee, J. F. M., Lamme, V. A. F., & Roelfsema, P. R. (2007) · Vision Research · doi:10.1016/j.visres.2006.12.018 · Cited by 75 · see citing works
Self-citationNeural representation of transparent overlay
Qiu, F. T., & von der Heydt, R. (2007) · Nature Neuroscience · doi:10.1038/nn1853 · Cited by 72 · see citing works
Spike Synchrony Reveals Emergence of Proto-Objects in Visual Cortex
Martin, A. B., & von der Heydt, R. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.3590-14.2015 · Cited by 52 · see citing works
The Representation of Erroneously Perceived Stimuli in the Primary Visual Cortex
Roelfsema, P. R., & Spekreijse, H. (2001) · Neuron · doi:10.1016/s0896-6273(01)00408-1 · Cited by 51 · see citing works
Self-citationGlobally inconsistent figure/ground relations induced by a negative part
Kim, S.-H., & Feldman, J. (2009) · Journal of Vision · doi:10.1167/9.10.8 · Cited by 39 · see citing works
Learning Optimizes Decision Templates in the Human Visual Cortex
Kuai, S.-G., Levi, D. M., & Kourtzi, Z. (2013) · Current Biology · doi:10.1016/j.cub.2013.07.052 · Cited by 39 · see citing works
The “side” matters: How configurality is reflected in completion
Kogo, N., & Wagemans, J. P. (2012) · Cognitive Neuroscience · doi:10.1080/17588928.2012.727387 · Cited by 24 · see citing works
Contextual effects on perceived contrast: Figure-ground assignment and orientation contrast
Self, M. W., Mookhoek, A., Tjalma, N., & Roelfsema, P. R. (2015) · Journal of Vision · doi:10.1167/15.2.2 · Cited by 11 · see citing works
Self-citationContextual modulation in V1: the Rossi-Zipser controversy
Supr, H., & Corthout, E. (2004) · Experimental Brain Research · doi:10.1007/s00221-004-1847-8 · Cited by 10 · see citing works
Flagged first, then by citations
Research works printed but not linked: 3
- [3]3. [Marr, D. (1982). Vision (Freeman).](http://refhub.elsevier.com/S0960-9822(19)30155-1/sref3)
- [15]15. [Rubin, E. (1921). Visuell wahrgenommene Figuren (Gyldendalske).](http://refhub.elsevier.com/S0960-9822(19)30155-1/sref15)
- [25]25. [Corthout, E., and Supe ` r, H. (2004). Contextual modulation in V1: the RossiZipser controversy. Exp. Brain Res. 156 , 118-123.](http://refhub.elsevier.com/S0960-9822(19)30155-1/sref25)
Cited by
Sorted by citations
Fernández, E., Alfaro, A., Soto-Sánchez, C., Gonzalez-Lopez, P., Lozano, A. M., Peña, S., Grima, M. D., Rodil, A., Gómez, B., Chen, X., et al. (2021) · Journal of Clinical Investigation · doi:10.1172/jci151331 · Cited by 250 · see citing works
Self-citationFernández, E., Alfaro, A., & González-López, P. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.00681 · Cited by 35 · see citing works
- Authors
- Self, M. W., Jeurissen, D., van Ham, A. F., van Vugt, B., Poort, J., & Roelfsema, P. R.
- Affiliations
- Netherlands Institute for Neuroscience (NL)
- Corresponding author
- Self, Matthew W.
- Venue
- Current Biology
- Publisher
- Elsevier BV
- Published
- 2019-03
- Volume
- 29
- Issue
- 6
- Pages
- 1019-1029.e4
- ISSN
- 0960-9822 (ISSN-L)
- OpenAlex
- W2920989903
- Cited by
- 42
- References
- 45
- Citations by year
- 2026: 5 · 2025: 4 · 2024: 6 · 2023: 8 · 2022: 5 · 2021: 6 · 2020: 6 · 2019: 1 · 2018: 1
- FWCI
- 2.61
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Current Biology (publishedVersion)
- PubMed (publishedVersion)
- VU Research Portal (publishedVersion, other-oa)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
- Pure Amsterdam UMC (submittedVersion)
- KNAW research portal (Royal Academy of Art and Sciences (KNAW)) (submittedVersion)
- Apollo (University of Cambridge) (submittedVersion, cc-by-nc-nd)
- Apollo
- Funders
- NWO (823-02-010)
- European Union
- ERC (339490, 7202070, 785907)
- Human Brain Project
- Simons Foundation (414196)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
- Physical Sciences › Computer Science › Computer Vision and Pattern Recognition › Visual Attention and Saliency Detection
- Life Sciences › Neuroscience › Cognitive Neuroscience › Face Recognition and Perception
- Keywords
- proto-objects, foreground-background segmentation, primary visual cortex, global-local processing, attention, scene segmentation, macaque, spatiotemporal neural activity, shape perception
- MeSH terms
- Animals, Macaca mulatta, Male, Neurons, Pattern Recognition, Visual, Photic Stimulation, Visual Cortex
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