Orientation selectivity and noise correlation in awake monkey area V1 are modulated by the gamma cycle
Open accessAbstract
Gamma-band synchronization adjusts the timing of excitatory and inhibitory inputs to a neuron. Neurons in the visual cortex are selective for stimulus orientation because of dynamic interactions between excitatory and inhibitory inputs. We hypothesized that these interactions and hence also orientation selectivity vary during the gamma cycle. We determined for each spike its phase relative to the gamma cycle. As a function of gamma phase, we then determined spike rates and their orientation selectivity. Orientation selectivity was modulated by gamma phase. The firing rate of spiking activity that occurred close to a neuron's mean gamma phase of firing was most orientation selective. This stimulus-selective signal could best be conveyed to postsynaptic neurons if it were not corrupted by noise correlations. Noise correlations between firing rates were modulated by gamma phase such that they were not statistically detectable for the spiking activity occurring close to a neuron's mean gamma phase of firing. Thus, gamma-band synchronization produces spiking activity that carries maximal stimulus selectivity and minimal noise correlation in its firing rate, and at the same time synchronizes this spiking activity for maximal impact on postsynaptic targets.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
Gamma-band (30-80 Hz) synchronization is beneficial for information coding, inter-areal transmission, and behavioral performance.
“Several theoretical and empirical studies have suggested that one important temporal feature of cortical sensory processing is gamma-band (30–80 Hz) synchronization, which is beneficial for information coding (Vinck et al., 2010; Womelsdorf et al., 2012), inter-areal transmission (Bosman et al., 2012; Womelsdorf et al., 2007) and behavioral performance”
From Waking state: rapid variations modulate neural and behavioral responses (2015) · cites this paper as Womelsdorf et al., 2012
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Gray, C. M., König, P., Engel, A. K., & Singer, W. (1989) · Nature · doi:10.1038/338334a0 · Cited by 4,183 · see citing works
Self-citationRegulation 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
Modulation of Oscillatory Neuronal Synchronization by Selective Visual Attention
Fries, P., Reynolds, J. H., Rorie, A. E., & Desimone, R. (2001) · Science · doi:10.1126/science.1055465 · Cited by 2,786 · see citing works
Self-citationDriving fast-spiking cells induces gamma rhythm and controls sensory responses
Cardin, J. A., Carlén, M., Meletis, K., Knoblich, U., Zhang, F., Deisseroth, K., Tsai, L.-H., & Moore, C. I. (2009) · Nature · doi:10.1038/nature08002 · Cited by 2,603 · see citing works
Shadlen, M. N., & Newsome, W. T. (1998) · The Journal of Neuroscience · doi:10.1523/jneurosci.18-10-03870.1998 · Cited by 2,178 · see citing works
Place units in the hippocampus of the freely moving rat
O'Keefe, J. (1976) · Experimental Neurology · doi:10.1016/0014-4886(76)90055-8 · Cited by 1,836 · see citing works
Neuronal gamma-band synchronization as a fundamental process in cortical computation
Fries, P. (2009) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.051508.135603 · Cited by 1,713 · see citing works
Self-citationModulation of Neuronal Interactions Through Neuronal Synchronization
Womelsdorf, T., Schoffelen, J.-M., Oostenveld, R., Singer, W., Desimone, R., Engel, A. K., & Fries, P. (2007) · Science · doi:10.1126/science.1139597 · Cited by 1,367 · see citing works
Self-citationCorrelated neuronal activity and the flow of neural information
Salinas, E., & Sejnowski, T. J. (2001) · Nature Reviews Neuroscience · doi:10.1038/35086012 · Cited by 1,333 · see citing works
High-frequency, long-range coupling between prefrontal and visual cortex during attention
Gregoriou, G. G., Gotts, S. J., Zhou, H., & Desimone, R. (2009) · Science · doi:10.1126/science.1171402 · Cited by 1,194 · see citing works
Attention improves performance primarily by reducing interneuronal correlations
Cohen, M. R., & Maunsell, J. H. R. (2009) · Nature Neuroscience · doi:10.1038/nn.2439 · Cited by 1,126 · see citing works
The Asynchronous State in Cortical Circuits
Renart, A., de la Rocha, J., Bartho, P., Hollender, L., Parga, N., Reyes, A., & Harris, K. D. (2010) · Science · doi:10.1126/science.1179850 · Cited by 1,106 · see citing works
Fries, P., Nikolić, D., & Singer, W. (2007) · Trends in Neurosciences · doi:10.1016/j.tins.2007.05.005 · Cited by 1,044 · see citing works
Self-citationMeasuring and interpreting neuronal correlations
Cohen, M. R., & Kohn, A. (2011) · Nature Neuroscience · doi:10.1038/nn.2842 · Cited by 1,016 · see citing works
Gamma-band synchronization in visual cortex predicts speed of change detection
Womelsdorf, T., Fries, P., Mitra, P. P., & Desimone, R. (2005) · Nature · doi:10.1038/nature04258 · Cited by 741 · see citing works
Self-citationSpatial attention decorrelates intrinsic activity fluctuations in macaque area V4
Mitchell, J. F., Sundberg, K. A., & Reynolds, J. H. (2009) · Neuron · doi:10.1016/j.neuron.2009.09.013 · Cited by 710 · see citing works
Integrator or coincidence detector? The role of the cortical neuron revisited
Peter König, B., Engel, A. K., & Singer, W. (1996) · Trends in Neurosciences · doi:10.1016/s0166-2236(96)80019-1 · Cited by 674 · see citing works
Self-citationHasenstaub, A. R., Shu, Y., Haider, B., Kraushaar, U., Duque, A., & McCormick, D. A. (2005) · Neuron · doi:10.1016/j.neuron.2005.06.016 · Cited by 654 · see citing works
Orientation Selectivity in Macaque V1: Diversity and Laminar Dependence
Ringach, D. L., Shapley, R. M., & Hawken, M. J. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-13-05639.2002 · Cited by 653 · see citing works
Parallel and Serial Neural Mechanisms for Visual Search in Macaque Area V4
Bichot, N. P., Rossi, A. F., & Desimone, R. (2005) · Science · doi:10.1126/science.1109676 · Cited by 651 · see citing works
Decorrelated neuronal firing in cortical microcircuits
Ecker, A. S., Berens, P., Keliris, G. A., Bethge, M., Logothetis, N. K., & Tolias, A. S. (2010) · Science · doi:10.1126/science.1179867 · Cited by 640 · see citing works
Laminar differences in gamma and alpha coherence in the ventral stream
Buffalo, E. A., Fries, P., Landman, R., Buschman, T. J., & Desimone, R. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1011284108 · Cited by 606 · see citing works
Self-citationPhase-dependent neuronal coding of objects in short-term memory
Siegel, M., Warden, M. R., & Miller, E. K. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0908193106 · Cited by 573 · see citing works
Muthukumaraswamy, S. D., Edden, R. A. E., Jones, D. K., Swettenham, J. B., & Singh, K. D. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0900728106 · Cited by 562 · see citing works
Azouz, R., & Gray, C. M. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.130200797 · Cited by 526 · see citing works
Stimulus Dependence of Neuronal Correlation in Primary Visual Cortex of the Macaque
Kohn, A., & Smith, M. A. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.5106-04.2005 · Cited by 521 · see citing works
Neuronal Coherence as a Mechanism of Effective Corticospinal Interaction
Schoffelen, J., Oostenveld, R., & Fries, P. (2005) · Science · doi:10.1126/science.1107027 · Cited by 519 · see citing works
Self-citationCorrelated Firing in Macaque Visual Area MT: Time Scales and Relationship to Behavior
Bair, W., Zohary, E., & Newsome, W. T. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-05-01676.2001 · Cited by 515 · see citing works
Adaptation-Induced Plasticity of Orientation Tuning in Adult Visual Cortex
Dragoi, V., Sharma, J., & Sur, M. (2000) · Neuron · doi:10.1016/s0896-6273(00)00103-3 · Cited by 495 · see citing works
The pairwise phase consistency: A bias-free measure of rhythmic neuronal synchronization
Vinck, M. A., van Wingerden, M., Womelsdorf, T., Fries, P., & Pennartz, C. M. A. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.01.073 · Cited by 483 · see citing works
Self-citationImpact of Correlated Synaptic Input on Output Firing Rate and Variability in Simple Neuronal Models
Salinas, E., & Sejnowski, T. J. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-16-06193.2000 · Cited by 472 · see citing works
Localizing human visual gamma-band activity in frequency, time and space
Hoogenboom, N., Schoffelen, J., Oostenveld, R., Parkes, L. M., & Fries, P. (2005) · NeuroImage · doi:10.1016/j.neuroimage.2005.08.043 · Cited by 464 · see citing works
Self-citationFries, P., Womelsdorf, T., Oostenveld, R., & Desimone, R. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.4499-07.2008 · Cited by 458 · see citing works
Self-citationRapid Neocortical Dynamics: Cellular and Network Mechanisms
Haider, B., & McCormick, D. A. (2009) · Neuron · doi:10.1016/j.neuron.2009.04.008 · Cited by 441 · see citing works
Cortical Enlightenment: Are Attentional Gamma Oscillations Driven by ING or PING?
Tiesinga, P. H. E., & B, T. J. S. A. (2009) · Neuron · doi:10.1016/j.neuron.2009.09.009 · Cited by 421 · see citing works
Neural dissociation between visual awareness and spatial attention
Wyart, V., & Tallon-Baudry, C. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.4748-07.2008 · Cited by 391 · see citing works
Jensen, O. B., & Lisman, J. E. (2000) · Journal of Neurophysiology · doi:10.1152/jn.2000.83.5.2602 · Cited by 312 · see citing works
Background gamma rhythmicity and attention in cortical local circuits: A computational study
Börgers, C., Epstein, S., & Kopell, N. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0502366102 · Cited by 300 · see citing works
Attention Reduces Stimulus-Driven Gamma Frequency Oscillations and Spike Field Coherence in V1
Chalk, M., Herrero, J. L., Gieselmann, M. A., Delicato, L. S., Gotthardt, S., & Thiele, A. (2010) · Neuron · doi:10.1016/j.neuron.2010.03.013 · Cited by 287 · see citing works
Adaptive Coincidence Detection and Dynamic Gain Control in Visual Cortical Neurons In Vivo
Azouz, R., & Gray, C. M. (2003) · Neuron · doi:10.1016/s0896-6273(02)01186-8 · Cited by 278 · see citing works
Shapley, R. M., Hawken, M. J., & Ringach, D. L. (2003) · Neuron · doi:10.1016/s0896-6273(03)00332-5 · Cited by 263 · see citing works
Coherent Oscillatory Activity in Monkey Area V4 Predicts Successful Allocation of Attention
Taylor, K., Mandon, S., Freiwald, W. A., & Kreiter, A. K. (2005) · Cerebral Cortex · doi:10.1093/cercor/bhi023 · Cited by 209 · see citing works
Theta phase–specific codes for two-dimensional position, trajectory and heading in the hippocampus
Huxter, J. R., Senior, T. J., Allen, K. L., & Csicsvari, J. (2008) · Nature Neuroscience · doi:10.1038/nn.2106 · Cited by 206 · see citing works
Friedman‐Hill, S. R. (2000) · Cerebral Cortex · doi:10.1093/cercor/10.11.1105 · Cited by 201 · see citing works
Gamma-phase shifting in awake monkey visual cortex
Vinck, M., Lima, B., Womelsdorf, T., Oostenveld, R., Singer, W., Neuenschwander, S., & Fries, P. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.1623-09.2010 · Cited by 189 · see citing works
Self-citationDynamics of Striate Cortical Activity in the Alert Macaque: II. Fast Time Scale Synchronization
Maldonado, P. (2000) · Cerebral Cortex · doi:10.1093/cercor/10.11.1117 · Cited by 149 · see citing works
Frien, A., Eckhorn, R., Bauer, R., Woelbern, T., & Gabriel, A. (2000) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2000.00025.x · Cited by 141 · see citing works
Fries, P., Scheeringa, R., & Oostenveld, R. (2008) · Neuron · doi:10.1016/j.neuron.2008.04.020 · Cited by 122 · see citing works
Self-citationvan Pelt, S., Boomsma, D. I., & Fries, P. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.5592-11.2012 · Cited by 118 · see citing works
Self-citationSynchronization Dynamics in Response to Plaid Stimuli in Monkey V1
Lima, B., Singer, W., Chen, N.-H., & Neuenschwander, S. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhp218 · Cited by 106 · see citing works
Self-citationPhase Resetting as a Mechanism for Supramodal Attentional Control
Kayser, C. (2009) · Neuron · doi:10.1016/j.neuron.2009.10.022 · Cited by 33 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Rhythms for cognition: communication through coherence
Fries, P. (2015) · Neuron · doi:10.1016/j.neuron.2015.09.034 · Cited by 2,725 · see citing works
Self-citationLisman, J. E., & Jensen, O. (2013) · Neuron · doi:10.1016/j.neuron.2013.03.007 · Cited by 1,609 · see citing works
Arousal and Locomotion Make Distinct Contributions to Cortical Activity Patterns and Visual Encoding
Vinck, M., Batista-Brito, R., Knoblich, U., & Cardin, J. A. (2015) · Neuron · doi:10.1016/j.neuron.2015.03.028 · Cited by 819 · see citing works
Self-citationWaking state: rapid variations modulate neural and behavioral responses
McGinley, M. J., Vinck, M., Reimer, J., Batista-Brito, R., Zagha, E., Cadwell, C. R., Tolias, A. S., Cardin, J. A., & McCormick, D. A. (2015) · Neuron · doi:10.1016/j.neuron.2015.09.012 · Cited by 801 · see citing works
“…feature of cortical sensory processing is gamma-band (30–80 Hz) synchronization, which is beneficial for information coding (Vinck et al., 2010; Womelsdorf et al., 2012), inter-areal transmission (Bosman et al., 2012; Womelsdorf et al., 2007) and behavioral performance (Siegle et al., 2014;…”
Self-citationDynamic circuit motifs underlying rhythmic gain control, gating and integration
Womelsdorf, T., Valiante, T. A., Sahin, N. T., Miller, K. J., & Tiesinga, P. (2014) · Nature Neuroscience · doi:10.1038/nn.3764 · Cited by 341 · see citing works
Self-citationEthridge, L. E., White, S. P., Mosconi, M. W., Wang, J., Byerly, M. J., & Sweeney, J. A. (2016) · Translational Psychiatry · doi:10.1038/tp.2016.48 · Cited by 188 · see citing works
Developmental Dysfunction of VIP Interneurons Impairs Cortical Circuits
Batista-Brito, R., Vinck, M., Ferguson, K. A., Chang, J. T., Laubender, D., Lur, G., Mossner, J. M., Hernandez, V. G., Ramakrishnan, C., Deisseroth, K., et al. (2017) · Neuron · doi:10.1016/j.neuron.2017.07.034 · Cited by 135 · see citing works
Self-citationStimulus repetition modulates gamma-band synchronization in primate visual cortex
Brunet, N. M., Bosman, C. A., Vinck, M., Roberts, M., Oostenveld, R., Desimone, R., De Weerd, P., & Fries, P. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1309714111 · Cited by 130 · see citing works
Self-citationBurst Firing Synchronizes Prefrontal and Anterior Cingulate Cortex during Attentional Control
Womelsdorf, T., Ardid, S., Everling, S., & Valiante, T. A. (2014) · Current Biology · doi:10.1016/j.cub.2014.09.046 · Cited by 113 · see citing works
Self-citationEriksson, D., Wunderle, T., & Schmidt, K. (2012) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2012.00026 · Cited by 7 · see citing works
- Authors
- Womelsdorf, T., Lima, B., Vinck, M., Oostenveld, R., Singer, W., Neuenschwander, S., & Fries, P.
- Affiliations
- Radboud University Nijmegen (NL)
- Max Planck Institute for Brain Research (DE)
- Max Planck Society (DE)
- Goethe University Frankfurt (DE)
- ORCID
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2012-02-27
- Volume
- 109
- Issue
- 11
- Pages
- 4302-4307
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC3306673
- OpenAlex
- W2121164361
- Cited by
- 119
- References
- 51
- Citations by year
- 2026: 4 · 2025: 8 · 2024: 9 · 2023: 5 · 2022: 4 · 2021: 8 · 2020: 8 · 2019: 9 · 2018: 6 · 2017: 7 · 2016: 17 · 2015: 13 · 2014: 6 · 2013: 10 · 2012: 5
- FWCI
- 5.57
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Americanae (AECID Library) (publishedVersion, other-oa)
- UvA-DARE (University of Amsterdam) (publishedVersion)
- LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) (publishedVersion, other-oa)
- Radboud Repository (Radboud University) (submittedVersion)
- Max Planck Institute for Plasma Physics (submittedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Funders
- European Science Foundation
- Max-Planck-Gesellschaft
- Canadian Institutes of Health Research
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- gamma-band synchronization, orientation selectivity, noise correlation, primary visual cortex, area V1, excitatory-inhibitory interactions, firing rate, neuronal synchronization, monkeys
- MeSH terms
- Action Potentials, Animals, Haplorhini, Cortical Synchronization, Noise, Orientation, Visual Cortex, Wakefulness
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
