Cited by 2,896Visual perception and processing mechanismsNeural dynamics and brain functionNeurogenesis and neuroplasticity mechanisms

Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex

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Bienenstock, EL, Cooper, LN, Munro, PW·1982·The Journal of Neuroscience

Abstract

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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Crossref · 10.1523/jneurosci.02-01-00032.1982

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  • Consistent with original ideas, modest depolarization can elicit LTD, whereas stronger depolarization leads to LTP.

    “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

    Section II, “Modification of Cortical Synapses” (page unavailable), proposes that synaptic strength decreases when postsynaptic output is below a modification threshold and increases when it is above it. This supports the claim’s low-versus-high activity pattern, but the paper describes a theoretical rule based on postsynaptic response, not a finding that modest versus stronger depolarization elicits LTD and LTP. (LLM, conf=0.85)

    Experimental — accuracy not yet measured
  • If the contribution of CaMKII to synaptic transmission were a net gain that simply adds onto the preexisting excitatory drive of the cell, the system would be unstable and quickly saturate.

    “If this were the case, it has been argued that the system would be unstable and quickly saturate (366–371).”

    From Synaptic memory and CaMKII (2023) · cites this paper as [367]

    In §II, the paper says that if synapses are allowed only to increase, all will eventually saturate. It also says that its activity-dependent modification threshold is necessary for a bounded state. This supports the general concern about unchecked synaptic gain, but the paper does not address CaMKII or establish that saturation would occur quickly. (LLM, conf=0.84)

    Experimental — accuracy not yet measured
  • The existence of LTD avoids the problem of saturation, which could be essential for a mnemonic device.

    “The existence of LTD avoids the problem of saturation, which could be essential for a mnemonic device (366–371).”

    From Synaptic memory and CaMKII (2023) · cites this paper as [367]

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Research works printed but not linked: 7

  1. Anderson, J. A. (1970) Two models for memory organization Hebb, D. 0. (1949) Organization of Behavior, John Wiley and using interacting traces. Math. Biosci. 8: 137-160.
  2. selectivity. Doctoral thesis, Brown University, Providence, Hirsch, H. V. B., and D. N. Spinelli (1971) Modification of the RI. distribution of receptive field orientation in cats by selective
  3. Hubel, D. H., and T. N. Wiesel (1962) Receptive fields, binoc- Vol. 2, No. 1, Jan. 1982 ular interaction and functional architecture in the cat's visual cortex. J. Physiol. (Lond.) 160: 106-154.
  4. LeventhaI, A. G., and H. V. B. Hirsch (1977) Effects of early experience upon orientation selectivity and binocularity of neurons in visual cortex of cats. Proc. Natl. Acad. Sci. U. S. A. 74: 1272-1276.
  5. Pettigrew, J. D. (1978) The paradox of the critical period for striate cortex. In Neuronal Plasticity, C. W. Cotman, ed., pp. 311-330, Raven Press, New York.
  6. Singer, W. (1979) Central-core control of visual functions. In Neuroscience Fourth Study Program, F. Schmitt and F. Worden, eds., pp. 1093-1109, MIT Press, Cambridge.
  7. Trotter, Y., Y. Fregnac, P. Buisseret (1981) Gating control of developmental plasticity by extraocular proprioception in kitten area 17. In Fourth European Conference on Visual Perception, Gouzieux, France.

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Authors
Bienenstock, E., Cooper, L., & Munro, P.
Affiliations
Université Paris-Sud (FR)
Venue
The Journal of Neuroscience
Published
1982-01-01
Volume
2
Issue
1
Pages
32-48
ISSN
  • 0270-6474 (ISSN-L)
  • 1529-2401
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
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

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