Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.

Site Tools

  • AAAS
  • Subscribe
  • Feedback

Site Search

Search Advanced

Science 27 May 1994:
Vol. 264. no. 5163, pp. 1333 - 1336
DOI: 10.1126/science.8191289
Prev | Table of Contents | Next

Articles

Science, Vol 264, Issue 5163, 1333-1336
Copyright © 1994 by American Association for the Advancement of Science

articles

Summation and division by neurons in primate visual cortex

M Carandini and DJ Heeger

Center for Neural Science, New York University, New York 10003.

Recordings from monkey primary visual cortex (V1) were used to test a model for the visually driven responses of simple cells. According to the model, simple cells compute a linear sum of the responses of lateral geniculate nucleus (LGN) neurons. In addition, each simple cell's linear response is divided by the pooled activity of a large number of other simple cells. The cell membrane performs both operations; synaptic currents are summed and then divided by the total membrane conductance. Current and conductance are decoupled (by a complementary arrangement of excitation and inhibition) so that current depends only on the LGN inputs and conductance depends only on the cortical inputs. Closed form expressions were derived for fitting and interpreting physiological data. The model accurately predicted responses to drifting grating stimuli of various contrasts, orientations, and spatiotemporal frequencies.


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Time Course of Cross-Orientation Suppression in the Early Visual Cortex.
R. Kimura and I. Ohzawa (2009)
J Neurophysiol 101, 1463-1479
   Abstract »    Full Text »    PDF »
Gain Modulation of Neuronal Responses by Subtractive and Divisive Mechanisms of Inhibition.
A. Ayaz and F. S. Chance (2009)
J Neurophysiol 101, 958-968
   Abstract »    Full Text »    PDF »
The Initial Disparity Vergence Elicited With Single and Dual Grating Stimuli in Monkeys: Evidence for Disparity Energy Sensing and Nonlinear Interactions.
K. Miura, Y. Sugita, K. Matsuura, N. Inaba, K. Kawano, and F. A. Miles (2008)
J Neurophysiol 100, 2907-2918
   Abstract »    Full Text »    PDF »
Dynamic contrast change produces rapid gain control in visual cortex.
N. A. Crowder, M. A. Hietanen, N. S. C. Price, C. W. G. Clifford, and M. R. Ibbotson (2008)
J. Physiol. 586, 4107-4119
   Abstract »    Full Text »    PDF »
Possible Role of Dendritic Compartmentalization in the Spatial Working Memory Circuit.
K. Morita (2008)
J. Neurosci. 28, 7699-7724
   Abstract »    Full Text »    PDF »
Contrast Sensitivity Is Enhanced by Expansive Nonlinear Processing in the Lateral Geniculate Nucleus.
T. Duong and R. D. Freeman (2008)
J Neurophysiol 99, 367-372
   Abstract »    Full Text »    PDF »
Dendrite-to-Soma Input/Output Function of Continuous Time-Varying Signals in Hippocampal CA1 Pyramidal Neurons.
E. P. Cook, J. A. Guest, Y. Liang, N. Y. Masse, and C. M. Colbert (2007)
J Neurophysiol 98, 2943-2955
   Abstract »    Full Text »    PDF »
A Biologically Realistic Model of Contrast Invariant Orientation Tuning by Thalamocortical Synaptic Depression.
Y. Banitt, K. A. C. Martin, and I. Segev (2007)
J. Neurosci. 27, 10230-10239
   Abstract »    Full Text »    PDF »
Suppressed Neuronal Activity and Concurrent Arteriolar Vasoconstriction May Explain Negative Blood Oxygenation Level-Dependent Signal.
A. Devor, P. Tian, N. Nishimura, I. C. Teng, E. M. C. Hillman, S. N. Narayanan, I. Ulbert, D. A. Boas, D. Kleinfeld, and A. M. Dale (2007)
J. Neurosci. 27, 4452-4459
   Abstract »    Full Text »    PDF »
Implications of Functionally Different Synaptic Inputs for Neuronal Gain and Computational Properties of Fly Visual Interneurons.
J. Grewe, N. Matos, M. Egelhaaf, and A.-K. Warzecha (2006)
J Neurophysiol 96, 1838-1847
   Abstract »    Full Text »    PDF »
Origins of Cross-Orientation Suppression in the Visual Cortex.
B. Li, J. K. Thompson, T. Duong, M. R. Peterson, and R. D. Freeman (2006)
J Neurophysiol 96, 1755-1764
   Abstract »    Full Text »    PDF »
Suppressive surrounds and contrast gain in magnocellular-pathway retinal ganglion cells of macaque..
S. G. Solomon, B. B. Lee, and H. Sun (2006)
J. Neurosci. 26, 8715-8726
   Abstract »    Full Text »    PDF »
Effects of spatial attention on contrast response functions in macaque area v4..
T. Williford and J. H. R. Maunsell (2006)
J Neurophysiol 96, 40-54
   Abstract »    Full Text »    PDF »
Tilt Aftereffect and Adaptation-Induced Changes in Orientation Tuning in Visual Cortex.
D. Z. Jin, V. Dragoi, M. Sur, and H. S. Seung (2005)
J Neurophysiol 94, 4038-4050
   Abstract »    Full Text »    PDF »
Do We Know What the Early Visual System Does?.
M. Carandini, J. B. Demb, V. Mante, D. J. Tolhurst, Y. Dan, B. A. Olshausen, J. L. Gallant, and N. C. Rust (2005)
J. Neurosci. 25, 10577-10597
   Abstract »    Full Text »    PDF »
Low-Frequency Oscillations Arising From Competitive Interactions Between Visual Stimuli in Macaque Inferotemporal Cortex.
J. E. Rollenhagen and C. R. Olson (2005)
J Neurophysiol 94, 3368-3387
   Abstract »    Full Text »    PDF »
Competitive Dynamics in Cortical Responses to Visual Stimuli.
S. Moldakarimov, J. E. Rollenhagen, C. R. Olson, and C. C. Chow (2005)
J Neurophysiol 94, 3388-3396
   Abstract »    Full Text »    PDF »
Deterministic Multiplicative Gain Control with Active Dendrites.
W. H. Mehaffey, B. Doiron, L. Maler, and R. W. Turner (2005)
J. Neurosci. 25, 9968-9977
   Abstract »    Full Text »    PDF »
Cross-Orientation Suppression: Monoptic and Dichoptic Mechanisms Are Different.
B. Li, M. R. Peterson, J. K. Thompson, T. Duong, and R. D. Freeman (2005)
J Neurophysiol 94, 1645-1650
   Abstract »    Full Text »    PDF »
Intracortical Origins of Interocular Suppression in the Visual Cortex.
F. Sengpiel and V. Vorobyov (2005)
J. Neurosci. 25, 6394-6400
   Abstract »    Full Text »    PDF »
Possible Effects of Depolarizing GABAA Conductance on the Neuronal Input-Output Relationship: A Modeling Study.
K. Morita, K. Tsumoto, and K. Aihara (2005)
J Neurophysiol 93, 3504-3523
   Abstract »    Full Text »    PDF »
Chromatic Gain Controls in Visual Cortical Neurons.
S. G. Solomon and P. Lennie (2005)
J. Neurosci. 25, 4779-4792
   Abstract »    Full Text »    PDF »
Distinct Properties of Stimulus-Evoked Bursts in the Lateral Geniculate Nucleus.
H. J. Alitto, T. G. Weyand, and W. M. Usrey (2005)
J. Neurosci. 25, 514-523
   Abstract »    Full Text »    PDF »
Intracellular Measurements of Spatial Integration and the MAX Operation in Complex Cells of the Cat Primary Visual Cortex.
I. Lampl, D. Ferster, T. Poggio, and M. Riesenhuber (2004)
J Neurophysiol 92, 2704-2713
   Abstract »    Full Text »    PDF »
Adaptive Temporal Integration of Motion in Direction-Selective Neurons in Macaque Visual Cortex.
W. Bair and J. A. Movshon (2004)
J. Neurosci. 24, 7305-7323
   Abstract »    Full Text »    PDF »
Mapping receptive fields in primary visual cortex.
D. L. Ringach (2004)
J. Physiol. 558, 717-728
   Abstract »    Full Text »    PDF »
Visual Cortex Neurons of Monkeys and Cats: Temporal Dynamics of the Spatial Frequency Response Function.
R. A. Frazor, D. G. Albrecht, W. S. Geisler, and A. M. Crane (2004)
J Neurophysiol 91, 2607-2627
   Abstract »    Full Text »    PDF »
Influence of Contrast on Orientation and Temporal Frequency Tuning in Ferret Primary Visual Cortex.
H. J. Alitto and W. M. Usrey (2004)
J Neurophysiol 91, 2797-2808
   Abstract »    Full Text »    PDF »
Neuronal Integration of Synaptic Input in the Fluctuation-Driven Regime.
A. Kuhn, A. Aertsen, and S. Rotter (2004)
J. Neurosci. 24, 2345-2356
   Abstract »    Full Text »    PDF »
Barrages of Synaptic Activity Control the Gain and Sensitivity of Cortical Neurons.
Y. Shu, A. Hasenstaub, M. Badoual, T. Bal, and D. A. McCormick (2003)
J. Neurosci. 23, 10388-10401
   Abstract »    Full Text »    PDF »
Persistent Cortical Activity: Mechanisms of Generation and Effects on Neuronal Excitability.
D. A. McCormick, Y. Shu, A. Hasenstaub, M. Sanchez-Vives, M. Badoual, and T. Bal (2003)
Cereb Cortex 13, 1219-1231
   Abstract »    Full Text »    PDF »
A Synaptic Explanation of Suppression in Visual Cortex.
M. Carandini, D. J Heeger, and W. Senn (2002)
J. Neurosci. 22, 10053-10065
   Abstract »    Full Text »    PDF »
Spatial Organization of Receptive Fields of V1 Neurons of Alert Monkeys: Comparison With Responses to Gratings.
I. Kagan, M. Gur, and D. M. Snodderly (2002)
J Neurophysiol 88, 2557-2574
   Abstract »    Full Text »    PDF »
Contrast-Dependent Changes in Spatial Frequency Tuning of Macaque V1 Neurons: Effects of a Changing Receptive Field Size.
M. P. Sceniak, M. J. Hawken, and R. Shapley (2002)
J Neurophysiol 88, 1363-1373
   Abstract »    Full Text »    PDF »
Visual Cortex Neurons of Monkeys and Cats: Temporal Dynamics of the Contrast Response Function.
D. G. Albrecht, W. S. Geisler, R. A. Frazor, and A. M. Crane (2002)
J Neurophysiol 88, 888-913
   Abstract »    Full Text »    PDF »
Local Correlation-Based Circuitry Can Account for Responses to Multi-Grating Stimuli in a Model of Cat V1.
T. Z. Lauritzen, A. E. Krukowski, and K. D. Miller (2001)
J Neurophysiol 86, 1803-1815
   Abstract »    Full Text »    PDF »
Visual Spatial Characterization of Macaque V1 Neurons.
M. P. Sceniak, M. J. Hawken, and R. Shapley (2001)
J Neurophysiol 85, 1873-1887
   Abstract »    Full Text »    PDF »
Contrast-Dependent Nonlinearities Arise Locally in a Model of Contrast-Invariant Orientation Tuning.
A. Kayser, N. J. Priebe, and K. D. Miller (2001)
J Neurophysiol 85, 2130-2149
   Abstract »    Full Text »    PDF »
Membrane Potential and Conductance Changes Underlying Length Tuning of Cells in Cat Primary Visual Cortex.
J. S. Anderson, I. Lampl, D. C. Gillespie, and D. Ferster (2001)
J. Neurosci. 21, 2104-2112
   Abstract »    Full Text »    PDF »
Modeling Inhibitory Plasticity in the Electrosensory System of Mormyrid Electric Fish.
P. D. Roberts (2000)
J Neurophysiol 84, 2035-2047
   Abstract »    Full Text »    PDF »
Orientation Tuning of Input Conductance, Excitation, and Inhibition in Cat Primary Visual Cortex.
J. S. Anderson, M. Carandini, and D. Ferster (2000)
J Neurophysiol 84, 909-926
   Abstract »    Full Text »    PDF »
Membrane Mechanisms Underlying Contrast Adaptation in Cat Area 17 In Vivo.
M. V. Sanchez-Vives, L. G. Nowak, and D. A. McCormick (2000)
J. Neurosci. 20, 4267-4285
   Abstract »    Full Text »    PDF »
Contrast Gain Control in the Visual Cortex: Monocular Versus Binocular Mechanisms.
A. M. Truchard, I. Ohzawa, and R. D. Freeman (2000)
J. Neurosci. 20, 3017-3032
   Abstract »    Full Text »    PDF »
Intrinsic Dynamics in Neuronal Networks. I. Theory.
P. E. Latham, B. J. Richmond, P. G. Nelson, and S. Nirenberg (2000)
J Neurophysiol 83, 808-827
   Abstract »    Full Text »    PDF »
Synaptic Basis of Cortical Persistent Activity: the Importance of NMDA Receptors to Working Memory.
X.-J. Wang (1999)
J. Neurosci. 19, 9587-9603
   Abstract »    Full Text »    PDF »
Shift in Smooth Pursuit Initiation and MT and MST Neuronal Activity Under Different Stimulus Conditions.
G. H. Recanzone and R. H. Wurtz (1999)
J Neurophysiol 82, 1710-1727
   Abstract »    Full Text »    PDF »
Motion Opponency in Visual Cortex.
D. J. Heeger, G. M. Boynton, J. B. Demb, E. Seidemann, and W. T. Newsome (1999)
J. Neurosci. 19, 7162-7174
   Abstract »    Full Text »    PDF »
Functional Selection of Adaptive Auditory Space Map by GABAA-Mediated Inhibition.
W. Zheng and E. I. Knudsen (1999)
Science 284, 962-965
   Abstract »    Full Text »
Effects of Attention on Orientation-Tuning Functions of Single Neurons in Macaque Cortical Area V4.
C. J. McAdams and J. H. R. Maunsell (1999)
J. Neurosci. 19, 431-441
   Abstract »    Full Text »    PDF »
Synaptic Integration in Striate Cortical Simple Cells.
J. A. Hirsch, J.-M. Alonso, R. C. Reid, and L. M. Martinez (1998)
J. Neurosci. 18, 9517-9528
   Abstract »    Full Text »    PDF »
Contrast-Invariant Orientation Tuning in Cat Visual Cortex: Thalamocortical Input Tuning and Correlation-Based Intracortical Connectivity.
T. W. Troyer, A. E. Krukowski, N. J. Priebe, and K. D. Miller (1998)
J. Neurosci. 18, 5908-5927
   Abstract »    Full Text »    PDF »
Synaptic Depression and the Temporal Response Characteristics of V1 Cells.
F. S. Chance, S. B. Nelson, and L. F. Abbott (1998)
J. Neurosci. 18, 4785-4799
   Abstract »    Full Text »    PDF »
Responses of MT and MST Neurons to One and Two Moving Objects in the Receptive Field.
G. H. Recanzone, R. H. Wurtz, and U. Schwarz (1997)
J Neurophysiol 78, 2904-2915
   Abstract »    Full Text »    PDF »
Linearity and Normalization in Simple Cells of the Macaque Primary Visual Cortex.
M. Carandini, D. J. Heeger, and J. A. Movshon (1997)
J. Neurosci. 17, 8621-8644
   Abstract »    Full Text »    PDF »
Encoding of Binocular Disparity by Complex Cells in the Cat's Visual Cortex.
I. Ohzawa, G. C. Deangelis, and R. D. Freeman (1997)
J Neurophysiol 77, 2879-2909
   Abstract »    Full Text »    PDF »
Invariant Visual Responses From Attentional Gain Fields.
E. Salinas and L. F. Abbott (1997)
J Neurophysiol 77, 3267-3272
   Abstract »    Full Text »    PDF »
Linear Systems Analysis of Functional Magnetic Resonance Imaging in Human V1.
G. M. Boynton, S. A. Engel, G. H. Glover, and D. J. Heeger (1996)
J. Neurosci. 16, 4207-4221
   Abstract »    Full Text »    PDF »
Recurrent excitation in neocortical circuits.
R. Douglas, C Koch, M Mahowald, K. Martin, and H. Suarez (1995)
Science 269, 981-985
   Abstract »    PDF »


To Advertise     Find Products

Science. ISSN 0036-8075 (print), 1095-9203 (online)