Learning the invariance properties of complex cells from their responses to natural stimuli
Abstract
Neurons in primary visual cortex are typically classified as either simple or complex. Whereas simple cells respond strongly to grating and bar stimuli displayed at a certain phase and visual field location, complex cell responses are insensitive to small translations of the stimulus within the receptive field [Hubel & Wiesel (1962) J. Physiol. (Lond.), 160, 106-154; Kjaer et al. (1997) J. Neurophysiol., 78, 3187-3197]. This constancy in the response to variations of the stimuli is commonly called invariance. Hubel and Wiesel's classical model of the primary visual cortex proposes a connectivity scheme which successfully describes simple and complex cell response properties. However, the question as to how this connectivity arises during normal development is left open. Based on their work and inspired by recent physiological findings we suggest a network model capable of learning from natural stimuli and developing receptive field properties which match those of cortical simple and complex cells. Stimuli are drawn from videos obtained by a camera mounted to a cat's head, so they should approximate the natural input to the cat's visual system. The network uses a competitive scheme to learn simple and complex cell response properties. Employing delayed signals to learn connections between simple and complex cells enables the model to utilize temporal properties of the input. We show that the temporal structure of the input gives rise to the emergence and refinement of complex cell receptive fields, whereas removing temporal continuity prevents this processes. This model lends a physiologically based explanation of the development of complex cell invariance response properties.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
IT neurons have vast receptive fields and respond selectively to certain objects or parts of objects across large changes in size, position and illumination.
“IT neurons have vast receptive fields and respond selectively to certain objects or parts of objects across large changes in size, position and illumination [39,40].”
From The visual word form area: expertise for reading in the fusiform gyrus (2003) · cites this paper as [40]
IT cortex is well known for its role in invariant object recognition.
“For example, inferotemporal (IT) cortex is well known for its role in invariant object recognition.”
From The visual word form area: expertise for reading in the fusiform gyrus (2003) · cites this paper as [40]
Cites
Receptive fields, binocular interaction and functional architecture in the cat’s visual cortex
Hubel, D. H., & Wiesel, T. N. (1962) · The Journal of Physiology · doi:10.1113/jphysiol.1962.sp006837 · Cited by 13,680 · see citing works
Introduction to the theory of neural computation
Hertz, J., Krogh, A., & Palmer, R. G. (1994) · Neural Networks · doi:10.1016/0893-6080(94)90014-0 · Cited by 6,431 · see citing works
Fukushima, K. (1980) · Biological Cybernetics · doi:10.1007/bf00344251 · Cited by 5,759 · see citing works
Emergence of simple-cell receptive field properties by learning a sparse code for natural images
Olshausen, B. A., & Field, D. J. (1996) · Nature · doi:10.1038/381607a0 · Cited by 5,694 · see citing works
Bi, G.-Q., & Poo, M.-M. (1998) · The Journal of Neuroscience · doi:10.1523/jneurosci.18-24-10464.1998 · Cited by 4,744 · see citing works
Regulation of Synaptic Efficacy by Coincidence of Postsynaptic APs and EPSPs
Markram, H., Lübke, J., Frotscher, M., & Sakmann, B. (1997) · Science · doi:10.1126/science.275.5297.213 · Cited by 3,832 · see citing works
Sparse coding with an overcomplete basis set: A strategy employed by V1?
Olshausen, B. A., & Field, D. J. (1997) · Vision Research · doi:10.1016/s0042-6989(97)00169-7 · Cited by 3,642 · see citing works
Hierarchical models of object recognition in cortex
Riesenhuber, M., & Poggio, T. (1999) · Nature Neuroscience · doi:10.1038/14819 · Cited by 3,309 · see citing works
Advances in Neural Information Processing Systems 5
Zemel, R. S., Williams, C. K. I., & Mozer, M. C. (1993) · Cited by 1,896 · see citing works
The “independent components” of natural scenes are edge filters
Bell, A. J., & Sejnowski, T. J. (1997) · Vision Research · doi:10.1016/s0042-6989(97)00121-1 · Cited by 1,592 · see citing works
Spatial frequency selectivity of cells in macaque visual cortex
De Valois, R. L., Albrecht, D. G., & Thorell, L. G. (1982) · Vision Research · doi:10.1016/0042-6989(82)90113-4 · Cited by 1,489 · see citing works
Synaptic plasticity: LTP and LTD
Bear, M. F., & Malenka, R. C. (1994) · Current Opinion in Neurobiology · doi:10.1016/0959-4388(94)90101-5 · Cited by 1,355 · see citing works
Slow Feature Analysis: Unsupervised Learning of Invariances
Wiskott, L., & B, T. J. S. A. (2002) · Neural Computation · doi:10.1162/089976602317318938 · Cited by 1,351 · see citing works
Sparse Coding and Decorrelation in Primary Visual Cortex During Natural Vision
Vinje, W. E., & Gallant, J. L. (2000) · Science · doi:10.1126/science.287.5456.1273 · Cited by 1,288 · see citing works
A new cellular mechanism for coupling inputs arriving at different cortical layers
Larkum, M. E., Zhu, J. J., & Sakmann, B. (1999) · Nature · doi:10.1038/18686 · Cited by 1,180 · see citing works
A mechanism for the Hebb and the anti-Hebb processes underlying learning and memory.
Lisman, J. (1989) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.86.23.9574 · Cited by 1,127 · see citing works
SURVEY OF INDEPENDENT COMPONENT ANALYSIS
Hyvärinen, A. (1999) · Cited by 1,120 · see citing works
Independent component filters of natural images compared with simple cells in primary visual cortex
van Hateren, J. H., & van der Schaaf, A. (1998) · Proceedings of the Royal Society of London. Series B: Biological Sciences · doi:10.1098/rspb.1998.0303 · Cited by 1,106 · see citing works
<i>Introduction to the Theory of Neural Computation</i>
Hertz, J., Krogh, A., Palmer, R. G., & Horner, H. (1991) · Physics Today · doi:10.1063/1.2810360 · Cited by 1,079 · see citing works
Artola, A., Bröcher, S., & Singer, W. (1990) · Nature · doi:10.1038/347069a0 · Cited by 880 · see citing works
Natural signal statistics and sensory gain control
Schwartz, O., & Simoncelli, E. P. (2001) · Nature Neuroscience · doi:10.1038/90526 · Cited by 835 · see citing works
A functional microcircuit for cat visual cortex
Douglas, R. J., & Martin, K. A. (1991) · The Journal of Physiology · doi:10.1113/jphysiol.1991.sp018733 · Cited by 736 · see citing works
Learning invariance from transformation sequences
Földiák, P. (1991) · Neural Computation · doi:10.1162/neco.1991.3.2.194 · Cited by 661 · see citing works
Classifying simple and complex cells on the basis of response modulation
SKOTTUN, B. C., Valois, R. L. D., Grosof, D. H., Movshon, J. A., Albrecht, D. G., & Bonds, A. B. (1991) · Vision Research · doi:10.1016/0042-6989(91)90033-2 · Cited by 608 · see citing works
INVARIANT FACE AND OBJECT RECOGNITION IN THE VISUAL SYSTEM
Wallis, G. M., & Rolls, E. T. (1997) · Progress in Neurobiology · doi:10.1016/s0301-0082(96)00054-8 · Cited by 539 · see citing works
Hyvärinen, A., & Hoyer, P. O. (2000) · Neural Computation · doi:10.1162/089976600300015312 · Cited by 533 · see citing works
Sparseness of the neuronal representation of stimuli in the primate temporal visual cortex
Rolls, E. T., & Tovée, M. J. (1995) · Journal of Neurophysiology · doi:10.1152/jn.1995.73.2.713 · Cited by 500 · see citing works
The CaM kinase II hypothesis for the storage of synaptic memory
Lisman, J. E. (1994) · Trends in Neurosciences · doi:10.1016/0166-2236(94)90014-0 · Cited by 499 · see citing works
Digital Image Processing: Concepts, Algorithms, and Scientific Applications
Jähne, B. (1991) · Cited by 380 · see citing works
Larkum, M. E., Kaiser, K. M. M., & Sakmann, B. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.25.14600 · Cited by 342 · see citing works
Mel, B. W. (1997) · Neural Computation · doi:10.1162/neco.1997.9.4.777 · Cited by 341 · see citing works
An intracellular analysis of geniculo‐cortical connectivity in area 17 of the cat.
Ferster, D., & Lindström, S. (1983) · The Journal of Physiology · doi:10.1113/jphysiol.1983.sp014846 · Cited by 324 · see citing works
Guitton, D., Douglas, R. M., & Volle, M. (1984) · Journal of Neurophysiology · doi:10.1152/jn.1984.52.6.1030 · Cited by 310 · see citing works
New perspectives on the mechanisms for orientation selectivity
Sompolinsky, H., & Shapley, R. M. (1997) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(97)80031-1 · Cited by 297 · see citing works
Functional connectivity between simple cells and complex cells in cat striate cortex
Alonso, J.-M., & Martinez, L. M. (1998) · Nature Neuroscience · doi:10.1038/1609 · Cited by 278 · see citing works
Ellias, S. A., & Grossberg, S. (1975) · Biological Cybernetics · doi:10.1007/bf00327046 · Cited by 271 · see citing works
Hoffmann, K. ‐., & Stone, J. (1971) · Brain Research · doi:10.1016/0006-8993(71)90340-4 · Cited by 262 · see citing works
Pike, F. G., Meredith, R. M., Olding, A. W. A., & Paulsen, O. (1999) · The Journal of Physiology · doi:10.1111/j.1469-7793.1999.0571p.x · Cited by 226 · see citing works
Digital image processing—Concepts, algorithms and scientific applications
(1992) · CVGIP Image Understanding · doi:10.1016/1049-9660(92)90091-g · Cited by 208 · see citing works
The velocity tuning of single units in cat striate cortex.
Movshon, J. A. (1975) · The Journal of Physiology · doi:10.1113/jphysiol.1975.sp011025 · Cited by 206 · see citing works
Complex cells as cortically amplified simple cells
Chance, F. S., Nelson, S. B., & Abbott, L. F. (1999) · Nature Neuroscience · doi:10.1038/6381 · Cited by 196 · see citing works
Organization of cat visual cortex as investigated by cross-correlation technique.
Toyama, K., Kimura, M., & Tanaka, K. (1981) · Journal of Neurophysiology · doi:10.1152/jn.1981.46.2.202 · Cited by 194 · see citing works
Wilson, J. R., & Sherman, S. M. (1976) · Journal of Neurophysiology · doi:10.1152/jn.1976.39.3.512 · Cited by 179 · see citing works
Mel, B. W., Ruderman, D., & Archie, K. A. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-11-04325.1998 · Cited by 142 · see citing works
Ngezahayo, A., Schachner, M., & Artola, A. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-07-02451.2000 · Cited by 139 · see citing works
Mutual information maximization: models of cortical self-organization
Becker, S. (1996) · Network Computation in Neural Systems · doi:10.1080/0954898x.1996.11978653 · Cited by 137 · see citing works
Learning with two sites of synaptic integration
Kording, K. P., & Peter König, B. (2000) · Network Computation in Neural Systems · doi:10.1088/0954-898x_11_1_302 · Cited by 105 · see citing works
Debanne, D., Gähwiler, B. H., & Thompson, S. M. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.20.11225 · Cited by 96 · see citing works
The processing and encoding of information in the visual cortex
Reid, R. C., & Alonso, J. (1996) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(96)80052-3 · Cited by 84 · see citing works
Initial synaptic efficacy influences induction and expression of long-term changes in transmission.
Yang, X. D., & Faber, D. S. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.10.4299 · Cited by 75 · see citing works
Extracting Slow Subspaces from Natural Videos Leads to Complex Cells
Kayser, C., Wolfgang Einhäuser, A., Dümmer, O., Peter König, B., & Kording, K. P. (2001) · Lecture notes in computer science · doi:10.1007/3-540-44668-0_149 · Cited by 65 · see citing works
Self-citationImplicit Learning in 3D Object Recognition: The Importance of Temporal Context
Becker, S. (1999) · Neural Computation · doi:10.1162/089976699300016683 · Cited by 55 · see citing works
Cat area 17. I. Pattern of thalamic control of cortical layers
Malpeli, J. G., Lee, C., Schwark, H. D., & Weyand, T. G. (1986) · Journal of Neurophysiology · doi:10.1152/jn.1986.56.4.1062 · Cited by 45 · see citing works
Learning Invariance from Transformation Sequences
Földiák, P. (1999) · The MIT Press eBooks · doi:10.7551/mitpress/7011.003.0006 · Cited by 43 · see citing works
A learning rule for dynamic recruitment and decorrelation
Kording, K. P., & König, P. (2000) · Neural Networks · doi:10.1016/s0893-6080(99)00088-x · Cited by 27 · see citing works
Self-citationCompetitive Anti-Hebbian Learning of Invariants
Schraudolph, N. N., & B, T. J. S. A. (1991) · Cited by 26 · see citing works
Insensitivity of V1 Complex Cell Responses to Small Shifts in the Retinal Image of Complex Patterns
Kjær, T. W., Gawne, T. J., Hertz, J., & Richmond, B. J. (1997) · Journal of Neurophysiology · doi:10.1152/jn.1997.78.6.3187 · Cited by 22 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
The visual word form area: expertise for reading in the fusiform gyrus
McCandliss, B. D., Cohen, L., & Dehaene, S. (2003) · Trends in Cognitive Sciences · doi:10.1016/s1364-6613(03)00134-7 · Cited by 1,489 · see citing works
Learning optimized features for hierarchical models of invariant object recognition.
Wersing, H., & Körner, E. (2003) · Neural Computation · doi:10.1162/089976603321891800 · Cited by 169 · see citing works
How are complex cell properties adapted to the statistics of natural stimuli?
Körding, K. P., Kayser, C., Einhäuser, W., & König, P. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00149.2003 · Cited by 121 · see citing works
Self-citationCognitive functions of intracellular mechanisms for contextual amplification
Phillips, W. A. (2017) · Brain and Cognition · doi:10.1016/j.bandc.2015.09.005 · Cited by 62 · see citing works
- Authors
- Einhäuser, W., Kayser, C., König, P., & Körding, K. P.
- Affiliations
- Max Planck Society (DE)
- ORCID
- Kayser, Christoph
- Venue
- European Journal of Neuroscience
- Publisher
- Wiley
- Published
- 2002-02
- Volume
- 15
- Issue
- 3
- Pages
- 475-486
- ISSN
- 0953-816X (ISSN-L)
- 1460-9568
- OpenAlex
- W2134309959
- Cited by
- 91
- References
- 57
- Citations by year
- 2026: 1 · 2025: 4 · 2024: 1 · 2023: 1 · 2022: 1 · 2021: 3 · 2020: 2 · 2019: 3 · 2016: 4 · 2015: 3 · 2014: 6 · 2013: 11 · 2012: 4
- FWCI
- 3.67
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- European Journal of Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- PUB – Publications at Bielefeld University (Bielefeld University) (submittedVersion)
- Publikationen an der Universität Bielefeld (Universität Bielefeld) (submittedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion)
- Funders
- Boehringer Ingelheim Fonds
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Physical Sciences › Computer Science › Artificial Intelligence › Neural Networks and Applications
- Keywords
- complex cells, simple cells, primary visual cortex, invariance, receptive field development, naturalistic stimuli, competitive learning, cat visual system, network models
- MeSH terms
- Animals, Cats, Evoked Potentials, Visual, Learning, Models, Neurological, Nerve Net, Synaptic Transmission, Neurons, Pattern Recognition, Visual, Photic Stimulation, Video Recording, Visual Cortex, Visual Fields, Neural Networks, Computer
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