Cortical Control of Spatial Resolution by VIP+Interneurons
Open accessAbstract
Neuronal tuning, defined by the degree of selectivity to a specific stimulus, is a hallmark of cortical computation. Understanding the role of GABAergic interneurons in shaping cortical tuning is now possible with the ability to manipulate interneuron classes selectively. Here, we show that interneurons expressing vasoactive intestinal polypeptide (VIP+) regulate the spatial frequency (SF) tuning of pyramidal neurons in mouse visual cortex. Using two-photon calcium imaging and optogenetic manipulations of VIP+cell activity, we found that activating VIP+cells elicited a stronger network response to stimuli of higher SFs, whereas suppressing VIP+cells resulted in a network response shift toward lower SFs. These results establish that cortical inhibition modulates the spatial resolution of visual processing and add further evidence demonstrating that feature selectivity depends, not only on the feedforward excitatory projections into the cortex, but also on dynamic intracortical modulations by specific forms of inhibition. SIGNIFICANCE STATEMENT We demonstrate that interneurons expressing vasoactive intestinal polypeptide (VIP+) play a causal role in regulating the spatial frequency (SF) tuning of neurons in mouse visual cortex. We show that optogenetic activation of VIP+cells results in a shift in network preference toward higher SFs, whereas suppressing them shifts the network toward lower SFs. Several studies have shown that VIP+cells are sensitive to neuromodulation and increase their firing during locomotion, whisking, and pupil dilation and are involved in spatially specific top-down modulation, reminiscent of the effects of top-down attention, and also that attention enhances spatial resolution. Our findings provide a bridge between these studies by establishing the inhibitory circuitry that regulates these fundamental modulations of SF in the cortex.
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Different interneuron populations may also differentially influence heterogeneity of gain modulation.
“and different interneuron populations may also differentially influence this heterogeneity114.”
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Cites
Brainard, D. H. (1997) · Spatial Vision · doi:10.1163/156856897x00357 · Cited by 19,308 · see citing works
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
Neural Mechanisms of Selective Visual Attention
Desimone, R., & Duncan, J. (1995) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.18.030195.001205 · Cited by 8,388 · see citing works
Kleiner, M., Brainard, D., & Pelli, D. G. (2007) · MPG.PuRe (Max Planck Society) · Cited by 3,751 · see citing works
A pyramid approach to subpixel registration based on intensity
Thévenaz, P., Ruttimann, U. E., & Unser, M. A. (1998) · IEEE Transactions on Image Processing · doi:10.1109/83.650848 · Cited by 3,097 · see citing works
Neocortical excitation/inhibition balance in information processing and social dysfunction
Yizhar, O., Fenno, L. E., Prigge, M., Schneider, F., Davidson, T. J., O’Shea, D. J., Sohal, V. S., Goshen, I., Finkelstein, J., Paz, J. T., et al. (2011) · Nature · doi:10.1038/nature10360 · Cited by 2,454 · see citing works
Selective Attention Gates Visual Processing in the Extrastriate Cortex
Moran, J., & Desimone, R. (1985) · Science · doi:10.1126/science.4023713 · Cited by 2,433 · see citing works
Selective Attention Gates Visual Processing in the Extrastriate Cortex
Moran, J., & Desimone, R. (2003) · The MIT Press eBooks · doi:10.7551/mitpress/2834.003.0024 · Cited by 2,164 · see citing works
Pfeffer, C. K., Xue, M., He, M., Huang, Z. J., & Scanziani, M. (2013) · Nature Neuroscience · doi:10.1038/nn.3446 · Cited by 1,353 · see citing works
In vivo two-photon calcium imaging of neuronal networks
Stosiek, C., Garaschuk, O., Holthoff, K., & Konnerth, A. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1232232100 · Cited by 1,313 · see citing works
Functional imaging with cellular resolution reveals precise micro-architecture in visual cortex
Ohki, K., Chung, S., Ch'ng, Y. H., Kara, P., & Reid, R. C. (2005) · Nature · doi:10.1038/nature03274 · Cited by 1,191 · see citing works
Cortical interneurons that specialize in disinhibitory control
Pi, H.-J., Hangya, B., Kvitsiani, D., Sanders, J. I., Huang, Z. J., & Kepecs, A. (2013) · Nature · doi:10.1038/nature12676 · Cited by 1,136 · see citing works
Highly selective receptive fields in mouse visual cortex
Niell, C. M., & Stryker, M. P. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.0623-08.2008 · Cited by 1,081 · see citing works
A Cortical Circuit for Gain Control by Behavioral State
Fu, Y., Tucciarone, J. M., Espinosa, J. S., Sheng, N., Darcy, D. P., Nicoll, R. A., Huang, Z. J., & Stryker, M. P. (2014) · Cell · doi:10.1016/j.cell.2014.01.050 · Cited by 937 · cited 1× · see citing works
“1H) with a median of 0.034 0.004 cpd (n 5 mice; mean SEM), similar to what was found in previous studies (Niell and Stryker, 2008; Gao et al., 2010; Kerlin et al., 2010; Marshel et al., 2011).”
ResultInfluentialFunctional specificity of local synaptic connections in neocortical networks
Ko, H., Hofer, S. B., Pichler, B., Buchanan, K. A., Sjöström, P. J., & Mrsic‐Flogel, T. D. (2011) · Nature · doi:10.1038/nature09880 · Cited by 861 · see citing works
Long-range and local circuits for top-down modulation of visual cortex processing
Zhang, S., Xu, M., Kamigaki, T., Hoang Do, J. P., Chang, W.-C., Jenvay, S., Miyamichi, K., Luo, L., & Dan, Y. (2014) · Science · doi:10.1126/science.1254126 · Cited by 804 · see citing works
Sulforhodamine 101 as a specific marker of astroglia in the neocortex in vivo
Nimmerjahn, A., Kirchhoff, F., Kerr, J. N. D., & Helmchen, F. (2004) · Nature Methods · doi:10.1038/nmeth706 · Cited by 784 · see citing works
Attention improves or impairs visual performance by enhancing spatial resolution
Yeshurun, Y., & Carrasco, M. (1998) · Nature · doi:10.1038/23936 · Cited by 767 · see citing works
A disinhibitory circuit mediates motor integration in the somatosensory cortex
Lee, S., Kruglikov, I., Huang, Z. J., Fishell, G., & Rudy, B. (2013) · Nature Neuroscience · doi:10.1038/nn.3544 · Cited by 758 · see citing works
Pupil fluctuations track fast switching of cortical states during quiet wakefulness
Reimer, J., Froudarakis, E., Cadwell, C. R., Yatsenko, D., Denfield, G. H., & Tolias, A. S. (2014) · Neuron · doi:10.1016/j.neuron.2014.09.033 · Cited by 717 · cited 1× · see citing works
“VIP cells increase their firing during locomotion (Fu et al., 2014), whisking (Lee et al., 2013), or pupil dilation (Reimer et al., 2014) and have a disinhibitory influence on pyramidal cells, primarily by inhibition of SOM cells (Lee et al., 2013; Pi et al., 2013; Jackson et al., 2016; Karnani et…”
BackgroundA neural circuit for spatial summation in visual cortex
Adesnik, H., Bruns, W., Taniguchi, H., Huang, Z. J., & Scanziani, M. (2012) · Nature · doi:10.1038/nature11526 · Cited by 702 · see citing works
Broadly tuned response properties of diverse inhibitory neuron subtypes in mouse visual cortex
Kerlin, A. M., Andermann, M. L., Berezovskii, V. K., & Reid, R. C. (2010) · Neuron · doi:10.1016/j.neuron.2010.08.002 · Cited by 613 · see citing works
Parvalbumin-expressing interneurons linearly transform cortical responses to visual stimuli
Atallah, B. V., Bruns, W., Carandini, M., & Scanziani, M. (2012) · Neuron · doi:10.1016/j.neuron.2011.12.013 · Cited by 612 · see citing works
Rapid innate defensive responses of mice to looming visual stimuli
Yilmaz, M., & Meister, M. (2013) · Current Biology · doi:10.1016/j.cub.2013.08.015 · Cited by 611 · see citing works
Activation of specific interneurons improves V1 feature selectivity and visual perception
Lee, S.-H., Kwan, A. C., Zhang, S., Phoumthipphavong, V., Flannery, J. G., Masmanidis, S. C., Taniguchi, H., Huang, Z. J., Zhang, F., Boyden, E. S., et al. (2012) · Nature · doi:10.1038/nature11312 · Cited by 593 · see citing works
Division and subtraction by distinct cortical inhibitory networks in vivo
Wilson, N. R., Runyan, C. A., Wang, F. L., & Sur, M. (2012) · Nature · doi:10.1038/nature11347 · Cited by 568 · see citing works
Han, X., Chow, B. Y., Zhou, H., Klapoetke, N. C., Chuong, A. S., Rajimehr, R., Yang, A., Baratta, M. V., Winkle, J. A., Desimone, R., et al. (2011) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2011.00018 · Cited by 490 · see citing works
Three distinct families of GABAergic neurons in rat visual cortex
Gonchar, Y. (1997) · Cerebral Cortex · doi:10.1093/cercor/7.4.347 · Cited by 481 · see citing works
Functional Specialization of Seven Mouse Visual Cortical Areas
Marshel, J. H., Garrett, M., Nauhaus, I., & Callaway, E. M. (2011) · Neuron · doi:10.1016/j.neuron.2011.12.004 · Cited by 467 · see citing works
Xu, X., Roby, K. D., & Callaway, E. M. (2010) · Journal of Comparative Neurology · doi:10.1002/cne.22229 · Cited by 429 · see citing works
Functional specialization of mouse higher visual cortical areas
Andermann, M. L., Kerlin, A. M., Roumis, D. K., Glickfeld, L. L., & Reid, R. C. (2011) · Neuron · doi:10.1016/j.neuron.2011.11.013 · Cited by 406 · see citing works
Kawaguchi, Y., & Kubota, Y. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-08-02701.1996 · Cited by 380 · see citing works
Diverse Visual Features Encoded in Mouse Lateral Geniculate Nucleus
Piscopo, D. M., El-Danaf, R. N., Huberman, A. D., & Niell, C. M. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.5187-12.2013 · Cited by 346 · see citing works
Dynamic shifts of visual receptive fields in cortical area MT by spatial attention
Womelsdorf, T., Anton-Erxleben, K., Pieper, F., & Treue, S. (2006) · Nature Neuroscience · doi:10.1038/nn1748 · Cited by 317 · see citing works
Sillito, A. M. (1979) · The Journal of Physiology · doi:10.1113/jphysiol.1979.sp012723 · Cited by 309 · see citing works
Attentional enhancement of spatial resolution: linking behavioural and neurophysiological evidence
Anton-Erxleben, K., & Carrasco, M. (2013) · Nature reviews. Neuroscience · doi:10.1038/nrn3443 · Cited by 289 · see citing works
Visual stimuli recruit intrinsically generated cortical ensembles
Miller, J.-E. K., Ayzenshtat, I., Carrillo-Reid, L., & Yuste, R. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1406077111 · Cited by 288 · see citing works
Self-citationShapley, R. M., Hawken, M. J., & Ringach, D. L. (2003) · Neuron · doi:10.1016/s0896-6273(03)00332-5 · Cited by 263 · see citing works
Task difficulty modulates the activity of specific neuronal populations in primary visual cortex
Chen, Y., Martínez‐Conde, S., Macknik, S. L., Bereshpolova, Y., Swadlow, H. A., & Alonso, J. (2008) · Nature Neuroscience · doi:10.1038/nn.2147 · Cited by 251 · see citing works
Opening Holes in the Blanket of Inhibition: Localized Lateral Disinhibition by VIP Interneurons
Karnani, M. M., Jackson, J., Ayzenshtat, I., Hamzehei Sichani, A., Manoocheri, K., Kim, S., & Yuste, R. (2016) · The Journal of Neuroscience · doi:10.1523/jneurosci.3646-15.2016 · Cited by 236 · see citing works
Self-citationSingle-cell–initiated monosynaptic tracing reveals layer-specific cortical network modules
Wertz, A., Trenholm, S., Yonehara, K., Hillier, D., Raics, Z., Leinweber, M., Szalay, G., Ghanem, A., Keller, G. B., Rózsa, B. J., et al. (2015) · Science · doi:10.1126/science.aab1687 · Cited by 227 · see citing works
Relationship between spatial-frequency and orientation tuning of striate-cortex cells
Webster, M. A., & Valois, R. L. D. (1985) · Journal of the Optical Society of America A · doi:10.1364/josaa.2.001124 · Cited by 223 · see citing works
Ma, W., Liu, B., Li, Y.-T., Huang, Z. J., Zhang, L. I., & Tao, H. W. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.3248-10.2010 · Cited by 212 · see citing works
Parallel processing of visual space by neighboring neurons in mouse visual cortex
Smith, S. L., & Häusser, M. (2010) · Nature Neuroscience · doi:10.1038/nn.2620 · Cited by 205 · see citing works
Prönneke, A., Scheuer, B., Wagener, R. J., Möck, M., Witte, M., & Staiger, J. F. (2015) · Cerebral Cortex · doi:10.1093/cercor/bhv202 · Cited by 204 · see citing works
GABA<sub>A</sub>Inhibition Controls Response Gain in Visual Cortex
Katzner, S., Busse, L., & Carandini, M. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.5753-10.2011 · Cited by 201 · see citing works
Spatial properties of neurons in the monkey striate cortex
Hawken, M. J., & Parker, A. J. (1987) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1987.0044 · Cited by 197 · see citing works
Cooperative subnetworks of molecularly similar interneurons in mouse neocortex
Karnani, M. M., Jackson, J., Ayzenshtat, I., Tucciarone, J., Manoocheri, K., Snider, W. G., & Yuste, R. (2016) · Neuron · doi:10.1016/j.neuron.2016.02.037 · Cited by 196 · see citing works
Sensory experience regulates cortical inhibition by inducing IGF1 in VIP neurons
Mardinly, A. R., Spiegel, I., Patrizi, A., Centofante, E., Bazinet, J. E., Tzeng, C. P., Mandel-Brehm, C., Harmin, D. A., Adesnik, H., Fagiolini, M., et al. (2016) · Nature · doi:10.1038/nature17187 · Cited by 176 · see citing works
Sillito, A. M. (1975) · The Journal of Physiology · doi:10.1113/jphysiol.1975.sp011055 · Cited by 173 · see citing works
Spatial Attention Modulates Center-Surround Interactions in Macaque Visual Area V4
Sundberg, K. A., Mitchell, J. F., & Reynolds, J. H. (2009) · Neuron · doi:10.1016/j.neuron.2009.02.023 · Cited by 162 · see citing works
Kyriazi, H. T., Carvell, G. E., Brumberg, J. C., & Simons, D. (1996) · Journal of Neurophysiology · doi:10.1152/jn.1996.75.2.547 · Cited by 153 · see citing works
Relationship between spatial frequency selectivity and receptive field profile of simple cells.
Andrews, B. W., & Pollen, D. A. (1979) · The Journal of Physiology · doi:10.1113/jphysiol.1979.sp012652 · Cited by 151 · see citing works
GABA-A antagonist causes dramatic expansion of tuning in primary auditory cortex
Wang, J., Caspary, D., & Salvi, R. J. (2000) · NeuroReport · doi:10.1097/00001756-200004070-00045 · Cited by 145 · see citing works
Liu, B., Li, P., Li, Y.-T., Sun, Y. J., Yanagawa, Y., Obata, K., Zhang, L. I., & Tao, H. W. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.1915-09.2009 · Cited by 145 · see citing works
Attention Reshapes Center-Surround Receptive Field Structure in Macaque Cortical Area MT
Anton-Erxleben, K., Stephan, V., & Treue, S. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhp002 · Cited by 130 · see citing works
Interneuron subtypes and orientation tuning
Lee, S., Kwan, A. C., & Dan, Y. (2014) · Nature · doi:10.1038/nature13128 · Cited by 125 · see citing works
Parallel Input Channels to Mouse Primary Visual Cortex
Gao, E., DeAngelis, G. C., & Burkhalter, A. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.6456-09.2010 · Cited by 124 · see citing works
Target-Specific Effects of Somatostatin-Expressing Interneurons on Neocortical Visual Processing
Cottam, J. C. H., Smith, S. L., & Häusser, M. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.2624-13.2013 · Cited by 122 · see citing works
VIP+ interneurons control neocortical activity across brain states
Jackson, J., Ayzenshtat, I., Karnani, M., & Yuste, R. (2016) · Journal of Neurophysiology · doi:10.1152/jn.01124.2015 · Cited by 93 · see citing works
Self-citationKreile, A. K., Bonhoeffer, T., & Hübener, M. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.2143-11.2011 · Cited by 82 · see citing works
Tahvildari, B., Wölfel, M., Duque, A., & McCormick, D. A. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.1181-12.2012 · Cited by 77 · see citing works
Voluntary attention increases perceived spatial frequency
Abrams, J., Barbot, A., & Carrasco, A. (2010) · Attention Perception & Psychophysics · doi:10.3758/app.72.6.1510 · Cited by 73 · see citing works
Mesik, L., Ma, W., Li, L., Ibrahim, L. A., Huang, Z. J., Zhang, L. I., & Tao, H. W. (2015) · Frontiers in Neural Circuits · doi:10.3389/fncir.2015.00022 · Cited by 69 · see citing works
Function of inhibition in visual cortical processing
Alitto, H. J., & Dan, Y. (2010) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2010.02.012 · Cited by 57 · see citing works
Relationship between orientation tuning and spatial frequency in neurones of cat area 17
Vidyasagar, T. R., & Sig�enza, J. A. (1985) · Experimental Brain Research · doi:10.1007/bf00237851 · Cited by 41 · see citing works
Dynamics of spatial frequency tuning in mouse visual cortex
Vreysen, S., Zhang, B., Chino, Y. M., Arckens, L., & den Bergh, G. V. (2012) · Journal of Neurophysiology · doi:10.1152/jn.00022.2012 · Cited by 22 · see citing works
Zhu, W., Xing, D., Shelley, M., & Shapley, R. M. (2010) · Vision Research · doi:10.1016/j.visres.2010.01.007 · Cited by 21 · see citing works
Bayraktar (2000) · doi:10.1002/(sici)1096-9861(20000508)420:3
Flagged first, then by citations
Cited by
Sorted by citations
Mechanisms underlying gain modulation in the cortex
Ferguson, K. A., & Cardin, J. A. (2020) · Nature Reviews Neuroscience · doi:10.1038/s41583-019-0253-y · Cited by 327 · see citing works
Reliable and Elastic Propagation of Cortical Seizures In Vivo
Wenzel, M., Hamm, J. P., Peterka, D. S., & Yuste, R. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.05.090 · Cited by 141 · see citing works
Self-citationCortical inhibitory interneurons control sensory processing
Wood, K. C., Blackwell, J. M., & Geffen, M. N. (2017) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2017.08.018 · Cited by 128 · see citing works
Lee, A. T., Cunniff, M. M., See, J. Z., Wilke, S. A., Luongo, F. J., Ellwood, I. T., Ponnavolu, S., & Sohal, V. S. (2019) · Neuron · doi:10.1016/j.neuron.2019.04.001 · Cited by 97 · see citing works
How Cortical Circuits Implement Cortical Computations: Mouse Visual Cortex as a Model
Niell, C. M., & Scanziani, M. (2021) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-102320-085825 · Cited by 109 · see citing works
Francavilla, R., Villette, V., Luo, X. M., Chamberland, S., Muñoz-Pino, E., Camiré, O., Wagner, K., Kis, V., Somogyi, P., & Topolnik, L. (2018) · Nature Communications · doi:10.1038/s41467-018-07162-5 · Cited by 93 · see citing works
Malina, K. C.-K., Tsivourakis, E., Kushinsky, D., Apelblat, D., Shtiglitz, S., Zohar, E., Sokoletsky, M., Tasaka, G., Mizrahi, A., Lampl, I., et al. (2021) · Neuron · doi:10.1016/j.neuron.2021.05.001 · Cited by 99 · see citing works
Cortical disinhibitory circuits: cell types, connectivity and function
Kullander, K., & Topolnik, L. (2021) · Trends in Neurosciences · doi:10.1016/j.tins.2021.04.009 · Cited by 83 · see citing works
Locomotion modulates specific functional cell types in the mouse visual thalamus
Aydın, Ç., Couto, J., Giugliano, M., Farrow, K., & Bonin, V. (2018) · Nature Communications · doi:10.1038/s41467-018-06780-3 · Cited by 73 · see citing works
Action and learning shape the activity of neuronal circuits in the visual cortex
Pakan, J. M. P., Francioni, V., & Rochefort, N. L. (2018) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2018.04.020 · Cited by 75 · see citing works
Guet-McCreight, A., Skinner, F. K., & Topolnik, L. (2020) · Frontiers in Neural Circuits · doi:10.3389/fncir.2020.00032 · Cited by 64 · see citing works
COALIA: A Computational Model of Human EEG for Consciousness Research
Bensaid, S., Modolo, J., Merlet, I., Wendling, F., & Benquet, P. (2019) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2019.00059 · Cited by 58 · see citing works
VIP interneurons regulate cortical size tuning and visual perception
Ferguson, K., Salameh, J., Alba, C., Selwyn, H., Barnes, C., Lohani, S., & Cardin, J. A. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.113088 · Cited by 42 · see citing works
Ramos-Prats, A., Paradiso, E., Castaldi, F., Sadeghi, M., Mir, M. Y., Hörtnagl, H., Göbel, G., & Ferraguti, F. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.110893 · Cited by 37 · see citing works
Luo, X. M., Muñoz-Pino, E., Francavilla, R., Vallée, M., Droit, A., & Topolnik, L. (2019) · Brain Structure and Function · doi:10.1007/s00429-019-01883-z · Cited by 37 · see citing works
Spatial Clustering of Inhibition in Mouse Primary Visual Cortex
D’Souza, R. D., Bista, P., Meier, A. M., Ji, W., & Burkhalter, A. (2019) · Neuron · doi:10.1016/j.neuron.2019.09.020 · Cited by 34 · see citing works
Myers-Joseph, D., Wilmes, K. A., Fernández-Otero, M., Claudia Clopath, A., & Khan, A. G. (2023) · Neuron · doi:10.1016/j.neuron.2023.11.006 · Cited by 31 · see citing works
VIP interneurons in sensory cortex encode sensory and action signals but not direct reward signals
Ramamurthy, D. L., Chen, A., Zhou, J., Park, C., Huang, P. C., Bharghavan, P., Krishna, G., Liu, J., Casale, K., & Feldman, D. E. (2023) · Current Biology · doi:10.1016/j.cub.2023.06.086 · Cited by 27 · see citing works
Motaharinia, M., Gerrow, K., Boghozian, R., White, E. R., Choi, S.-E., Delaney, K. R., & Brown, C. E. (2021) · Nature Communications · doi:10.1038/s41467-021-26405-6 · Cited by 24 · see citing works
Havenith, M. N., Zijderveld, P. M., van Heukelum, S., Abghari, S., Glennon, J. C., & Tiesinga, P. H. E. (2018) · Scientific Reports · doi:10.1038/s41598-018-34966-8 · Cited by 20 · see citing works
Barrel cortex VIP/ChAT interneurons suppress sensory responses in vivo
Dudai, A., Yayon, N., Lerner, V., Tasaka, G., Deitcher, Y., Gorfine, K., Niederhoffer, N., Mizrahi, A., Soreq, H., & London, M. (2020) · PLoS Biology · doi:10.1371/journal.pbio.3000613 · Cited by 23 · see citing works
Visual Processing by Calretinin Expressing Inhibitory Neurons in Mouse Primary Visual Cortex
Camillo, D., Ahmadlou, M., Saiepour, M. H., Yasaminshirazi, M., Levelt, C. N., & Heimel, J. A. (2018) · Scientific Reports · doi:10.1038/s41598-018-30958-w · Cited by 21 · see citing works
Baruchin, L. J., Ghezzi, F., Kohl, M. M., & Butt, S. J. B. (2021) · Cerebral Cortex · doi:10.1093/cercor/bhab363 · Cited by 20 · see citing works
Coarse-to-fine processing drives the efficient coding of natural scenes in mouse visual cortex
Skyberg, R. J., Tanabe, S., Chen, H., & Cang, J. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.110606 · Cited by 19 · see citing works
Serotonergic regulation of bipolar cell survival in the developing cerebral cortex
Wong, F. K., Selten, M. M., Rosés-Novella, C., Sreenivasan, V., Pallas‐Bazarra, N., Serafeimidou‐Pouliou, E., Hanusz-Godoy, A., Oozeer, F., Edwards, R. H., & Marín, Ó. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111037 · Cited by 19 · see citing works
Roethler, O., Zohar, E., Malina, K. C.-K., Bitan, L., Gabel, H. W., & Spiegel, I. (2023) · Neuron · doi:10.1016/j.neuron.2023.05.026 · Cited by 20 · see citing works
Malwade, S., Gasthaus, J., Bellardita, C., Andelic, M., Moric, B., Korshunova, I., Kiehn, O., Vasistha, N. A., & Khodosevich, K. (2021) · Biological Psychiatry · doi:10.1016/j.biopsych.2021.09.012 · Cited by 17 · see citing works
Antagonistic inhibitory subnetworks control cooperation and competition across cortical spacePreprint
Mossing, D. P., Veit, J., Palmigiano, A., Miller, K. D., & Adesnik, H. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.03.31.437953 · Cited by 16 · see citing works
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Dudai, A., Yayon, N., Soreq, H., & London, M. (2020) · Journal of Neurochemistry · doi:10.1111/jnc.15263 · Cited by 14 · see citing works
Jiang, S.-N., Cao, J.-W., Liu, L.-Y., Zhou, Y., Shan, G.-Y., Fu, Y.-H., Shao, Y.-C., & Yu, Y.-C. (2023) · Cerebral Cortex · doi:10.1093/cercor/bhac343 · Cited by 10 · see citing works
Spiegel, I. (2020) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2020.11.013 · Cited by 11 · see citing works
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Newton, D. F., Fee, C., Nikolova, Y. S., & Sibille, E. L. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-813333-0.00028-7 · Cited by 11 · see citing works
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Williams, L. E., Küffer, L., Bawa, T., Husi, E., Pagès, S., & Holtmaat, A. J. D. G. (2024) · Journal of Neuroscience · doi:10.1523/jneurosci.2189-23.2024 · Cited by 10 · see citing works
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Zhang, Y., & Zhang, X. (2020) · Cognitive Neurodynamics · doi:10.1007/s11571-020-09623-4 · Cited by 7 · see citing works
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Kondziella, D., Amiri, M., Othman, M., Jakobsen, E. W., Jansen, T., & Møller, K. (2022) · Acta Neurochirurgica · doi:10.1007/s00701-022-05378-5 · Cited by 9 · see citing works
Ingram, T. G. J., King, J. L., & Crowder, N. A. (2019) · Frontiers in Neural Circuits · doi:10.3389/fncir.2019.00040 · Cited by 8 · see citing works
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Karnani, M., & Jackson, J. (2017) · The Neuroscientist · doi:10.1177/1073858417733719 · Cited by 7 · see citing works
Self-citationNishio, N., Hayashi, K., Ishikawa, A. W., & Yoshimura, Y. (2021) · The Journal of Physiology · doi:10.1113/jp281463 · Cited by 6 · see citing works
Malwade, S., Sellgren, C. M., Vasistha, N. A., & Khodosevich, K. (2025) · Biological Psychiatry Global Open Science · doi:10.1016/j.bpsgos.2025.100495 · Cited by 6 · see citing works
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Shapiro, J. T., Michaud, N. M., & Crowder, N. A. (2025) · The Journal of Physiology · doi:10.1113/jp287265 · Cited by 3 · see citing works
He, Y., Chou, X.-L., Lavoie, A., Liu, J., Russo, M., & Liu, B. (2024) · Current Biology · doi:10.1016/j.cub.2024.08.037 · Cited by 2 · see citing works
Shi, C., Zhang, C., Chen, J., & Yao, Z. (2024) · Cerebral Cortex · doi:10.1093/cercor/bhae051 · Cited by 1 · see citing works
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Wu, J., Yoneda, T., Robinson, K., Tsuchiya, N., & Yoshimura, Y. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.09.29.679183 · Cited by 1 · see citing works
Anesthesia Lowers Spatial Frequency Preference in the Primary Visual CortexPreprint
Wu, J., Yoneda, T., Robinson, K., Tsuchiya, N., & Yoshimura, Y. (2026) · eLife · doi:10.7554/elife.110295.1 · Cited by 1 · see citing works
Baruchin, L. J., Kohl, M. M., & Butt, S. J. B. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.02.18.431791
Altering sensory learning by chronic inactivation of VIP interneurons
Alba, C., Selwyn, H., Ferguson, K., & Cardin, J. A. (2020)
Coarse-to-Fine Processing Drives the Efficient Coding of Natural Scenes in Mouse Visual CortexPreprint
Skyberg, R. J., Tanabe, S., Chen, H., & Cang, J. (2021) · SSRN Electronic Journal · doi:10.2139/ssrn.3933995
NDNF+ interneurons have a privileged role in regulating cortical excitabilityPreprint
Richardson, A., Mercier, M. S., Shimoda, Y., Graham, R., Leite, M., Garcia, A. J., Muller, M., Bond, S. A., Grodzdanova, M., Wu, Q., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.11.27.690945
Moreno, C., Riquelme, D., Cornejo, C., Leyton, P., & Leiva‐Salcedo, E. (2026) · Biological Research · doi:10.1186/s40659-026-00673-2
Anesthesia Lowers Spatial Frequency Preference in the Primary Visual CortexPreprint
Wu, J., Yoneda, T., Robinson, K., Tsuchiya, N., & Yoshimura, Y. (2026) · eLife · doi:10.7554/elife.110295
- Authors
- Ayzenshtat, I., Karnani, M. M., Jackson, J., & Yuste, R.
- Affiliations
- Columbia University (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2016-11-09
- Volume
- 36
- Issue
- 45
- Pages
- 11498-11509
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6601713
- OpenAlex
- W2553564376
- Cited by
- 50
- References
- 70
- Citations by year
- 2026: 3 · 2025: 4 · 2024: 3 · 2023: 4 · 2022: 5 · 2021: 10 · 2020: 7 · 2019: 6 · 2018: 5 · 2017: 3
- FWCI
- 2.97
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- Defense Advanced Research Projects Agency (N66001-15-C-4032)
- Advanced Research Projects Agency (W911NF-12-1-0594)
- Multidisciplinary University Research Initiative (W911NF1210594)
- National Eye Institute (R01EY011787, DP1EY024503)
- Army Research Office (W911NF-12-1-0594, W911NF)
- Army Research Laboratory (W911NF-12-1-0594, W911NF)
- 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
- vasoactive intestinal peptide, VIP interneurons, GABAergic interneurons, spatial frequency tuning, visual cortex, cortical inhibition, spatial resolution, feature selectivity, top-down attention, optogenetic manipulation, neuromodulation
- MeSH terms
- Animals, Interneurons, Nerve Net, Neural Inhibition, Vasoactive Intestinal Peptide, Visual Cortex, Visual Fields, Visual Perception, Mice
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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.
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