IDEAS home Printed from https://ideas.repec.org/a/plo/pbio00/0050331.html
   My bibliography  Save this article

A Neural Computation for Visual Acuity in the Presence of Eye Movements

Author

Listed:
  • Xaq Pitkow
  • Haim Sompolinsky
  • Markus Meister

Abstract

Humans can distinguish visual stimuli that differ by features the size of only a few photoreceptors. This is possible despite the incessant image motion due to fixational eye movements, which can be many times larger than the features to be distinguished. To perform well, the brain must identify the retinal firing patterns induced by the stimulus while discounting similar patterns caused by spontaneous retinal activity. This is a challenge since the trajectory of the eye movements, and consequently, the stimulus position, are unknown. We derive a decision rule for using retinal spike trains to discriminate between two stimuli, given that their retinal image moves with an unknown random walk trajectory. This algorithm dynamically estimates the probability of the stimulus at different retinal locations, and uses this to modulate the influence of retinal spikes acquired later. Applied to a simple orientation-discrimination task, the algorithm performance is consistent with human acuity, whereas naive strategies that neglect eye movements perform much worse. We then show how a simple, biologically plausible neural network could implement this algorithm using a local, activity-dependent gain and lateral interactions approximately matched to the statistics of eye movements. Finally, we discuss evidence that such a network could be operating in the primary visual cortex. : Like a camera, the eye projects an image of the world onto our retina. But unlike a camera, the eye continues to execute small, random movements, even when we fix our gaze. Consequently, the projected image jitters over the retina. In a camera, such jitter leads to a blurred image on the film. Interestingly, our visual acuity is many times sharper than expected from the motion blur. Apparently, the brain uses an active process to track the image through its jittering motion across the retina. Here, we propose an algorithm for how this can be accomplished. The algorithm uses realistic spike responses of optic nerve fibers to reconstruct the visual image, and requires no knowledge of the eye movement trajectory. Its performance can account for human visual acuity. Furthermore, we show that this algorithm could be implemented biologically by the neural circuits of primary visual cortex. Even when we hold our gaze still, small eye movements jitter the visual image of the world across the retina. The authors show how a stable and sharp image might be recovered through neural processing in the visual cortex.

Suggested Citation

  • Xaq Pitkow & Haim Sompolinsky & Markus Meister, 2007. "A Neural Computation for Visual Acuity in the Presence of Eye Movements," PLOS Biology, Public Library of Science, vol. 5(12), pages 1-14, December.
  • Handle: RePEc:plo:pbio00:0050331
    DOI: 10.1371/journal.pbio.0050331
    as

    Download full text from publisher

    File URL: https://journals.plos.org/plosbiology/article?id=10.1371/journal.pbio.0050331
    Download Restriction: no

    File URL: https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.0050331&type=printable
    Download Restriction: no

    File URL: https://libkey.io/10.1371/journal.pbio.0050331?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Austin Roorda & David R. Williams, 1999. "The arrangement of the three cone classes in the living human eye," Nature, Nature, vol. 397(6719), pages 520-522, February.
    2. Stefan Treue & Julio C. Martínez Trujillo, 1999. "Feature-based attention influences motion processing gain in macaque visual cortex," Nature, Nature, vol. 399(6736), pages 575-579, June.
    3. Uri Polat & Keiko Mizobe & Mark W. Pettet & Takuji Kasamatsu & Anthony M. Norcia, 1998. "Collinear stimuli regulate visual responses depending on cell's contrast threshold," Nature, Nature, vol. 391(6667), pages 580-584, February.
    4. Fabrizio Gabbiani & Holger G. Krapp & Christof Koch & Gilles Laurent, 2002. "Multiplicative computation in a visual neuron sensitive to looming," Nature, Nature, vol. 420(6913), pages 320-324, November.
    5. Ikuya Murakami & Patrick Cavanagh, 1998. "A jitter after-effect reveals motion-based stabilization of vision," Nature, Nature, vol. 395(6704), pages 798-801, October.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Nadav Ben-Shushan & Nimrod Shaham & Mati Joshua & Yoram Burak, 2022. "Fixational drift is driven by diffusive dynamics in central neural circuitry," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    2. Noga Mosheiff & Haggai Agmon & Avraham Moriel & Yoram Burak, 2017. "An efficient coding theory for a dynamic trajectory predicts non-uniform allocation of entorhinal grid cells to modules," PLOS Computational Biology, Public Library of Science, vol. 13(6), pages 1-19, June.
    3. Eric G. Wu & Nora Brackbill & Colleen Rhoades & Alexandra Kling & Alex R. Gogliettino & Nishal P. Shah & Alexander Sher & Alan M. Litke & Eero P. Simoncelli & E. J. Chichilnisky, 2024. "Fixational eye movements enhance the precision of visual information transmitted by the primate retina," Nature Communications, Nature, vol. 15(1), pages 1-15, December.

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Li Zhaoping & Li Zhe, 2015. "Primary Visual Cortex as a Saliency Map: A Parameter-Free Prediction and Its Test by Behavioral Data," PLOS Computational Biology, Public Library of Science, vol. 11(10), pages 1-39, October.
    2. Xie, Ying & Zhou, Ping & Yao, Zhao & Ma, Jun, 2022. "Response mechanism in a functional neuron under multiple stimuli," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 607(C).
    3. Yajiao Tang & Junkai Ji & Yulin Zhu & Shangce Gao & Zheng Tang & Yuki Todo, 2019. "A Differential Evolution-Oriented Pruning Neural Network Model for Bankruptcy Prediction," Complexity, Hindawi, vol. 2019, pages 1-21, August.
    4. Ruben Coen-Cagli & Peter Dayan & Odelia Schwartz, 2012. "Cortical Surround Interactions and Perceptual Salience via Natural Scene Statistics," PLOS Computational Biology, Public Library of Science, vol. 8(3), pages 1-18, March.
    5. Sophie Hall & Patrick Bourke & Kun Guo, 2014. "Low Level Constraints on Dynamic Contour Path Integration," PLOS ONE, Public Library of Science, vol. 9(6), pages 1-9, June.
    6. Noah C Benson & Jeremy R Manning & David H Brainard, 2014. "Unsupervised Learning of Cone Spectral Classes from Natural Images," PLOS Computational Biology, Public Library of Science, vol. 10(6), pages 1-13, June.
    7. Yan Wang & Yue Gong & Shenming Huang & Xuechao Xing & Ziyu Lv & Junjie Wang & Jia-Qin Yang & Guohua Zhang & Ye Zhou & Su-Ting Han, 2021. "Memristor-based biomimetic compound eye for real-time collision detection," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    8. Sergi Bermúdez i Badia & Ulysses Bernardet & Paul F M J Verschure, 2010. "Non-Linear Neuronal Responses as an Emergent Property of Afferent Networks: A Case Study of the Locust Lobula Giant Movement Detector," PLOS Computational Biology, Public Library of Science, vol. 6(3), pages 1-15, March.
    9. Yoram S Bonneh & Tobias H Donner & Alexander Cooperman & David J Heeger & Dov Sagi, 2014. "Motion-Induced Blindness and Troxler Fading: Common and Different Mechanisms," PLOS ONE, Public Library of Science, vol. 9(3), pages 1-8, March.
    10. Li Zhaoping & Li Jingling, 2008. "Filling-In and Suppression of Visual Perception from Context: A Bayesian Account of Perceptual Biases by Contextual Influences," PLOS Computational Biology, Public Library of Science, vol. 4(2), pages 1-13, February.
    11. Udo A Ernst & Sunita Mandon & Nadja Schinkel–Bielefeld & Simon D Neitzel & Andreas K Kreiter & Klaus R Pawelzik, 2012. "Optimality of Human Contour Integration," PLOS Computational Biology, Public Library of Science, vol. 8(5), pages 1-17, May.
    12. Vladislav Kozyrev & Mohammad Reza Daliri & Philipp Schwedhelm & Stefan Treue, 2019. "Strategic deployment of feature-based attentional gain in primate visual cortex," PLOS Biology, Public Library of Science, vol. 17(8), pages 1-28, August.
    13. Eric G. Wu & Nora Brackbill & Colleen Rhoades & Alexandra Kling & Alex R. Gogliettino & Nishal P. Shah & Alexander Sher & Alan M. Litke & Eero P. Simoncelli & E. J. Chichilnisky, 2024. "Fixational eye movements enhance the precision of visual information transmitted by the primate retina," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    14. Robert G. Alexander & Stephen L. Macknik & Susana Martinez-Conde, 2022. "What the Neuroscience and Psychology of Magic Reveal about Misinformation," Publications, MDPI, vol. 10(4), pages 1-19, September.
    15. Jules Tagne Fossi & Vandi Deli & Hélène Carole Edima & Zeric Tabekoueng Njitacke & Florent Feudjio Kemwoue & Jacques Atangana, 2022. "Phase synchronization between two thermo-photoelectric neurons coupled through a Josephson Junction," The European Physical Journal B: Condensed Matter and Complex Systems, Springer;EDP Sciences, vol. 95(4), pages 1-17, April.
    16. Rong J. B. Zhu & Xue-Xin Wei, 2023. "Unsupervised approach to decomposing neural tuning variability," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    17. Malte Persike & Günter Meinhardt, 2015. "Effects of Spatial Frequency Similarity and Dissimilarity on Contour Integration," PLOS ONE, Public Library of Science, vol. 10(6), pages 1-19, June.
    18. Jeroen Brus & Joseph A. Heng & Valeriia Beliaeva & Fabian Gonzalez Pinto & Antonino Mario Cassarà & Esra Neufeld & Marcus Grueschow & Lukas Imbach & Rafael Polanía, 2024. "Causal phase-dependent control of non-spatial attention in human prefrontal cortex," Nature Human Behaviour, Nature, vol. 8(4), pages 743-757, April.
    19. Matthias S Keil & Joan López-Moliner, 2012. "Unifying Time to Contact Estimation and Collision Avoidance across Species," PLOS Computational Biology, Public Library of Science, vol. 8(8), pages 1-1, August.
    20. Sonali Bhatt Marwaha & Edwin C. May, 2015. "Rethinking Extrasensory Perception," SAGE Open, , vol. 5(1), pages 21582440155, March.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:plo:pbio00:0050331. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: plosbiology (email available below). General contact details of provider: https://journals.plos.org/plosbiology/ .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.