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Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex
Open accessAbstract
The development of stimulus selectivity in the primary sensory cortex of higher vertebrates is considered in a general mathematical framework. A synaptic evolution scheme of a new kind is proposed in which incoming patterns rather than converging afferents compete. The change in the efficacy of a given synapse depends not only on instantaneous pre- and postsynaptic activities but also on a slowly varying time-averaged value of the postsynaptic activity. Assuming an appropriate nonlinear form for this dependence, development of selectivity is obtained under quite general conditions on the sensory environment. One does not require nonlinearity of the neuron's integrative power nor does one need to assume any particular form for intracortical circuitry. This is first illustrated in simple cases, e.g., when the environment consists of only two different stimuli presented alternately in a random manner. The following formal statement then holds: the state of the system converges with probability 1 to points of maximum selectivity in the state space. We next consider the problem of early development of orientation selectivity and binocular interaction in primary visual cortex. Giving the environment an appropriate form, we obtain orientation tuning curves and ocular dominance comparable to what is observed in normally reared adult cats or monkeys. Simulations with binocular input and various types of normal or altered environments show good agreement with the relevant experimental data. Experiments are suggested that could test our theory further.
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“Consistent with original ideas (Bienenstock et al. 1982), modest depolarization can elicit LTD, whereas stronger depolarization leads to LTP.”
From NMDA receptor-dependent long-term potentiation and long-term depression (LTP/LTD). (2012) · cites this paper as Bienenstock et al. 1982
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“If this were the case, it has been argued that the system would be unstable and quickly saturate (366–371).”
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“The existence of LTD avoids the problem of saturation, which could be essential for a mnemonic device (366–371).”
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Yeung, L. C., Shouval, H. Z., Blais, B. S., & Cooper, L. N. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0405555101 · Cited by 106
Self-citationMechanisms of heterosynaptic metaplasticity
Hulme, S. R., Jones, O. D., Raymond, C. R., Sah, P., & Abraham, W. C. (2013) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2013.0148 · Cited by 107
Receptive-field plasticity in the adult auditory cortex induced by Hebbian covariance
Cruikshank, S., & Weinberger, N. M. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-02-00861.1996 · Cited by 98
Artola, A., Kamal, A., Ramakers, G. M. J., Biessels, G. J., & Gispen, W. H. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.04205.x · Cited by 99
Nitric oxide and hippocampal synaptic plasticity.
Zorumski, C., & Izumi, Y. (1993) · Biochemical Pharmacology · doi:10.1016/0006-2952(93)90484-e · Cited by 102
Metadata
- Authors
- Bienenstock, E., Cooper, L., & Munro, P.
- Affiliations
- Université Paris-Sud (FR)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 1982-01-01
- Volume
- 2
- Issue
- 1
- Pages
- 32-48
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6564292
- OpenAlex
- W1733248925
- Cited by
- 2,896
- References
- 19
- Citations by year
- 2026: 71 · 2025: 91 · 2024: 98 · 2023: 108 · 2022: 102 · 2021: 104 · 2020: 112 · 2019: 93 · 2018: 112 · 2017: 108 · 2016: 87 · 2015: 117 · 2014: 118 · 2013: 119 · 2012: 112
- FWCI
- 4.02
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Ittleson Foundation
- Brown University
- Fondation de France
- Office of Naval Research
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- orientation selectivity, binocular interaction, primary visual cortex, ocular dominance, synaptic plasticity, orientation tuning curves, synaptic efficacy, cortical development
- MeSH terms
- Animals, Cats, Dominance, Cerebral, Mathematics, Models, Neurological, Neurons, Orientation, Retina, Sensory Deprivation, Synapses, Visual Cortex, Visual Pathways, Visual Perception
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.
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