The Emergence of Contrast-Invariant Orientation Tuning in Simple Cells of Cat Visual Cortex
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Simple cells in primary visual cortex exhibit contrast-invariant orientation tuning, in seeming contradiction to feed-forward models that rely on lateral geniculate nucleus (LGN) input alone. Contrast invariance has therefore been thought to depend on the presence of intracortical lateral inhibition. In vivo intracellular recordings instead suggest that contrast invariance can be explained by three properties of the excitatory pathway. (1) Depolarizations evoked by orthogonal stimuli are determined by the amount of excitation a cell receives from the LGN, relative to the excitation it receives from other cortical cells. (2) Depolarizations evoked by preferred stimuli saturate at lower contrasts than the spike output of LGN relay cells. (3) Visual stimuli evoke contrast-dependent changes in trial-to-trial variability, which lead to contrast-dependent changes in the relationship between membrane potential and spike rate. Thus, high-contrast, orthogonally oriented stimuli that evoke significant depolarizations evoke few spikes. Together these mechanisms, without lateral inhibition, can account for contrast-invariant stimulus selectivity.
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Contrast-invariant orientation tuning of cortical neurons for visual stimuli is a well-characterized example of stable encoding of orientation regardless of changes in contrast.
“Contrast-invariant orientation tuning of cortical neurons for visual stimuli is a well-characterized example of stable encoding of one feature (in this case, orientation), regardless of changes in stimulus context (in this case, contrast)10–12.”
From Mechanisms underlying gain modulation in the cortex (2020) · cites this paper as [10]
Vm fluctuations may contribute to contrast-invariant tuning in neurons of the visual cortex of cats and rodents.
“These fluctuations may contribute to contrast-invariant tuning in neurons of the visual cortex of cats and rodents10,13,63,64.”
From Mechanisms underlying gain modulation in the cortex (2020) · cites this paper as [10]
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
The VideoToolbox software for visual psychophysics: transforming numbers into movies
Pelli, D. G. (1997) · Spatial Vision · doi:10.1163/156856897x00366 · Cited by 11,110 · see citing works
Normalization of cell responses in cat striate cortex
Heeger, D. J. (1992) · Visual Neuroscience · doi:10.1017/s0952523800009640 · Cited by 1,835 · see citing works
Synaptic depression and cortical gain control
Abbott, L. F., Varela, J. A., Sen, K., & Nelson, S. B. (1997) · Science · doi:10.1126/science.275.5297.221 · Cited by 1,690 · see citing works
Tsodyks, M. V., & Markram, H. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.2.719 · Cited by 1,607 · see citing works
Turning on and off recurrent balanced cortical activity
Shu, Y., Hasenstaub, A., & McCormick, D. A. (2003) · Nature · doi:10.1038/nature01616 · Cited by 1,054 · see citing works
Gain Modulation from Background Synaptic Input
Chance, F. S., Abbott, L. F., & Reyes, A. D. (2002) · Neuron · doi:10.1016/s0896-6273(02)00820-6 · Cited by 1,012 · see citing works
Spatial summation in the receptive fields of simple cells in the cat's striate cortex.
Movshon, J. A., Thompson, I. D., & Tolhurst, D. J. (1978) · The Journal of Physiology · doi:10.1113/jphysiol.1978.sp012488 · Cited by 890 · see citing works
An emergent model of orientation selectivity in cat visual cortical simple cells
Somers, D., Nelson, S., & Sur, M. (1995) · The Journal of Neuroscience · doi:10.1523/jneurosci.15-08-05448.1995 · Cited by 860 · see citing works
Specificity of monosynaptic connections from thalamus to visual cortex
Reid, R. C., & Alonso, J. (1995) · Nature · doi:10.1038/378281a0 · Cited by 732 · see citing works
The two-dimensional spatial structure of simple receptive fields in cat striate cortex
Jones, J. P., & Palmer, L. A. (1987) · Journal of Neurophysiology · doi:10.1152/jn.1987.58.6.1187 · Cited by 676 · see citing works
Visual input evokes transient and strong shunting inhibition in visual cortical neurons
Graham, L. J., Monier, C., & Frégnac, Y. (1998) · Nature · doi:10.1038/30735 · Cited by 669 · see citing works
Neural Mechanisms of Orientation Selectivity in the Visual Cortex
Ferster, D., & Miller, K. D. (2000) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.23.1.441 · Cited by 665 · see citing works
Self-citationOrientation selectivity of thalamic input to simple cells of cat visual cortex
Ferster, D., Chung, S., & Wheat, H. S. (1996) · Nature · doi:10.1038/380249a0 · Cited by 541 · see citing works
Self-citationAzouz, R., & Gray, C. M. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.130200797 · Cited by 526 · see citing works
Orientation Tuning of Input Conductance, Excitation, and Inhibition in Cat Primary Visual Cortex
Anderson, J. S., Carandini, M., & Ferster, D. (2000) · Journal of Neurophysiology · doi:10.1152/jn.2000.84.2.909 · Cited by 499 · see citing works
Self-citationTroyer, T. W., Krukowski, A. E., Priebe, N. J., & Miller, K. D. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-15-05908.1998 · Cited by 429 · see citing works
Self-citationExcitatory synaptic inputs to spiny stellate cells in cat visual cortex
Stratford, K. J., Tarczy‐Hornoch, K., Martin, K. A. C., Bannister, N. J., & Jack, J. (1996) · Nature · doi:10.1038/382258a0 · Cited by 427 · see citing works
DeAngelis, G. C., Ohzawa, I., & Freeman, R. D. (1993) · Journal of Neurophysiology · doi:10.1152/jn.1993.69.4.1091 · Cited by 427 · see citing works
The Contribution of Noise to Contrast Invariance of Orientation Tuning in Cat Visual Cortex
Anderson, J. S., Lampl, I., Gillespie, D. C., & Ferster, D. (2000) · Science · doi:10.1126/science.290.5498.1968 · Cited by 422 · see citing works
Self-citationMembrane Potential and Firing Rate in Cat Primary Visual Cortex
Carandini, M., & Ferster, D. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-01-00470.2000 · Cited by 413 · see citing works
Self-citationLow Response Variability in Simultaneously Recorded Retinal, Thalamic, and Cortical Neurons
Kara, P., Reinagel, P., & Reid, R. C. (2000) · Neuron · doi:10.1016/s0896-6273(00)00072-6 · Cited by 404 · see citing works
Internal Dynamics Determine the Cortical Response to Thalamic Stimulation
MacLean, J. N., Watson, B. O., Aaron, G. B., & Yuste, R. (2005) · Neuron · doi:10.1016/j.neuron.2005.09.035 · Cited by 373 · see citing works
A Tonic Hyperpolarization Underlying Contrast Adaptation in Cat Visual Cortex
Carandini, M., & Ferster, D. (1997) · Science · doi:10.1126/science.276.5314.949 · Cited by 372 · see citing works
Self-citationDeAngelis, G. C., Ohzawa, I., & Freeman, R. D. (1993) · Journal of Neurophysiology · doi:10.1152/jn.1993.69.4.1118 · Cited by 361 · see citing works
Orientation and Direction Selectivity of Synaptic Inputs in Visual Cortical Neurons
Monier, C., Chavane, F., Baudot, P., Graham, L. J., & Frégnac, Y. (2003) · Neuron · doi:10.1016/s0896-6273(03)00064-3 · Cited by 356 · see citing works
Miller, K. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-01-00409.1994 · Cited by 349 · see citing works
Orientation selectivity of synaptic potentials in neurons of cat primary visual cortex
Ferster, D. (1986) · Journal of Neuroscience · doi:10.1523/jneurosci.06-05-01284.1986 · Cited by 329 · see citing works
Self-citationSynaptic Integration in Striate Cortical Simple Cells
Hirsch, J. A., Alonso, J., Reid, R. C., & Martı́nez, L. M. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-22-09517.1998 · Cited by 326 · see citing works
Cellular Mechanisms of Long-Lasting Adaptation in Visual Cortical Neurons In Vitro
Sanchez-Vives, M. V., Nowak, L. G., & McCormick, D. A. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-11-04286.2000 · Cited by 320 · see citing works
Skottun, B. C., Bradley, A., Sclar, G., Ohzawa, I., & Freeman, R. D. (1987) · Journal of Neurophysiology · doi:10.1152/jn.1987.57.3.773 · Cited by 298 · cited 6× · see citing works
“And yet, most simple cells respond with few or no spikes at the orthogonal orientation, and orientation tuning is largely contrast invariant (Alitto and Usrey, 2004; Anderson et al., 2000c; Ferster and Miller, 2000; Skottun et al., 1987).”
BackgroundResultInfluentialNew 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
Chung, S., & Ferster, D. (1998) · Neuron · doi:10.1016/s0896-6273(00)80498-5 · Cited by 270 · see citing works
Self-citationDirection Selectivity of Excitation and Inhibition in Simple Cells of the Cat Primary Visual Cortex
Priebe, N. J., & Ferster, D. (2005) · Neuron · doi:10.1016/j.neuron.2004.12.024 · Cited by 250 · see citing works
Self-citationSpatially opponent excitation and inhibition in simple cells of the cat visual cortex
Ferster, D. (1988) · Journal of Neuroscience · doi:10.1523/jneurosci.08-04-01172.1988 · Cited by 240 · see citing works
Self-citationStimulus dependence of two-state fluctuations of membrane potential in cat visual cortex
Anderson, J. S., Lampl, I., Reichova, I., Carandini, M., & Ferster, D. (2000) · Nature Neuroscience · doi:10.1038/75797 · Cited by 219 · see citing works
Self-citationA Synaptic Explanation of Suppression in Visual Cortex
Carandini, M., Heeger, D. J., & Senn, W. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-22-10053.2002 · Cited by 219 · see citing works
The contribution of spike threshold to the dichotomy of cortical simple and complex cells
Priebe, N. J., Mechler, F., Carandini, M., & Ferster, D. (2004) · Nature Neuroscience · doi:10.1038/nn1310 · Cited by 217 · see citing works
Self-citationSuppression without Inhibition in Visual Cortex
Freeman, T., Durand, S., Kiper, D., & Carandini, M. (2002) · Neuron · doi:10.1016/s0896-6273(02)00819-x · Cited by 211 · see citing works
Amplification of Trial-to-Trial Response Variability by Neurons in Visual Cortex
Carandini, M. (2004) · PLoS Biology · doi:10.1371/journal.pbio.0020264 · Cited by 210 · see citing works
Neural Noise Can Explain Expansive, Power-Law Nonlinearities in Neural Response Functions
Miller, K. D., & Troyer, T. W. (2002) · Journal of Neurophysiology · doi:10.1152/jn.00425.2001 · Cited by 207 · see citing works
Receptive field structure varies with layer in the primary visual cortex
Martinez, L. M., Wang, Q., Reid, R. C., Pillai, C., Alonso, J.-M., Sommer, F. T., & Hirsch, J. A. (2005) · Nature Neuroscience · doi:10.1038/nn1404 · Cited by 203 · see citing works
Mechanisms underlying cross-orientation suppression in cat visual cortex
Priebe, N. J., & Ferster, D. (2006) · Nature Neuroscience · doi:10.1038/nn1660 · Cited by 184 · see citing works
Self-citationGlobal processing of visual stimuli in a neural network of coupled oscillators.
Sompolinsky, H., Golomb, D., & Kleinfeld, D. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.18.7200 · Cited by 178 · see citing works
Functionally distinct inhibitory neurons at the first stage of visual cortical processing
Hirsch, J. A., Martinez, L. M., Pillai, C., Alonso, J.-M., Wang, Q., & Sommer, F. T. (2003) · Nature Neuroscience · doi:10.1038/nn1152 · Cited by 176 · see citing works
Short-Term Depression in Thalamocortical Synapses of Cat Primary Visual Cortex
Boudreau, C. E., & Ferster, D. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.1445-05.2005 · Cited by 162 · see citing works
Self-citationHow Noise Contributes to Contrast Invariance of Orientation Tuning in Cat Visual Cortex
Hansel, D., & van Vreeswijk, C. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-12-05118.2002 · Cited by 157 · see citing works
Influence of Contrast on Orientation and Temporal Frequency Tuning in Ferret Primary Visual Cortex
Alitto, H. J., & Usrey, W. M. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00943.2003 · Cited by 143 · see citing works
An egalitarian network model for the emergence of simple and complex cells in visual cortex
Tao, L., Shelley, M., McLaughlin, D. W., & Shapley, R. M. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2036460100 · Cited by 142 · see citing works
Direction Selectivity of Synaptic Potentials in Simple Cells of the Cat Visual Cortex
Jagadeesh, B., Wheat, H. S., Kontsevich, L. L., Tyler, C. W., & Ferster, D. (1997) · Journal of Neurophysiology · doi:10.1152/jn.1997.78.5.2772 · Cited by 123 · see citing works
Self-citationLaminar processing of stimulus orientation in cat visual cortex
Martı́nez, L. M., Alonso, J., Reid, R. C., & Hirsch, J. A. (2002) · The Journal of Physiology · doi:10.1113/jphysiol.2001.012776 · Cited by 114 · see citing works
Tsodyks, M. V., & Markram, H. (1997) · Cited by 111 · see citing works
Tolhurst, D. J., & Heeger, D. J. (1997) · Visual Neuroscience · doi:10.1017/s0952523800011433 · Cited by 99 · see citing works
Different Roles for Simple-Cell and Complex-Cell Inhibition in V1
Lauritzen, T. Z., & Miller, K. D. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-32-10201.2003 · Cited by 94 · see citing works
Lampl, I., Anderson, J. S., Gillespie, D. C., & Ferster, D. (2001) · Neuron · doi:10.1016/s0896-6273(01)00278-1 · Cited by 82 · see citing works
Self-citationOrigins of Cross-Orientation Suppression in the Visual Cortex
Li, B., Thompson, J. K., Duong, T., Peterson, M. R., & Freeman, R. D. (2006) · Journal of Neurophysiology · doi:10.1152/jn.00425.2006 · Cited by 73 · see citing works
Contrast-Dependent Nonlinearities Arise Locally in a Model of Contrast-Invariant Orientation Tuning
Kayser, A. S., Priebe, N. J., & Miller, K. D. (2001) · Journal of Neurophysiology · doi:10.1152/jn.2001.85.5.2130 · Cited by 61 · see citing works
Self-citationComparison of the selectivity of postsynaptic potentials and spike responses in cat visual cortex
Volgushev, M., Pernberg, J., & Eysel, U. T. (2000) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2000.00909.x · Cited by 57 · see citing works
Excitatory inputs to spiny cells in layers 4 and 6 of cat striate cortex
Bannister, N. J., Nelson, J. C., & Jack, J. (2002) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2002.1160 · Cited by 44 · see citing works
McLaughlin, D. W., Shapley, R. M., & Shelley, M. (2003) · Journal of Physiology-Paris · doi:10.1016/j.jphysparis.2003.09.019 · Cited by 28 · see citing works
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- Authors
- Finn, I. M., Priebe, N. J., & Ferster, D.
- Affiliations
- Northwestern University (US)
- Corresponding author
- Ferster, David
- ORCID
- Priebe, Nicholas J.
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2007-04
- Volume
- 54
- Issue
- 1
- Pages
- 137-152
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC1993919
- OpenAlex
- W2146353372
- Cited by
- 248
- References
- 60
- Citations by year
- 2026: 3 · 2025: 13 · 2024: 11 · 2023: 7 · 2022: 9 · 2021: 11 · 2020: 10 · 2019: 18 · 2018: 8 · 2017: 10 · 2016: 17 · 2015: 16 · 2014: 9 · 2013: 22 · 2012: 25
- FWCI
- 7.17
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 2335 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Mental Health (P20 MH066239)
- National Eye Institute (R01 EY04726)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- contrast invariance, orientation tuning, simple cells, primary visual cortex, lateral geniculate nucleus, depolarization, spike frequency, trial-to-trial variability, membrane potential, feedforward models, cats
- MeSH terms
- Animals, Cats, Female, Geniculate Bodies, Membrane Potentials, Models, Neurological, Neural Inhibition, Neurons, Orientation, Photic Stimulation, Visual Cortex, Visual Pathways, Contrast Sensitivity, Patch-Clamp Techniques
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