Inhibitory Actions Unified by Network Integration
Open accessAbstract
Cortical function is regulated by a strikingly diverse array of local-circuit inhibitory neurons. We evaluated how optogenetically activating somatostatin- and parvalbumin-positive interneurons subtractively or divisively suppressed auditory cortical cells' responses to tones. In both awake and anesthetized animals, we found that activating either family of interneurons produced mixtures of divisive and subtractive effects and that simultaneously recorded neurons were often suppressed in qualitatively different ways. A simple network model shows that threshold nonlinearities can interact with network activity to transform subtractive inhibition of neurons into divisive inhibition of networks, or vice versa. Varying threshold and the strength of suppression of a model neuron could determine whether the effect of inhibition appeared divisive, subtractive, or both. We conclude that the characteristics of response inhibition specific to a single interneuron type can be "masked" by the network configuration and cellular properties of the network in which they are embedded.
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?
Optogenetic manipulations of interneurons provide evidence of cell type-specific effects of inhibitory interneurons on gain regulation.
“Optogenetic manipulations of interneurons provide evidence of cell type-specific effects of inhibitory interneurons on gain regulation2,68,104,105,107.”
From Mechanisms underlying gain modulation in the cortex (2020) · cites this paper as [107]
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
Biometry: The Principles and Practice of Statistics in Biological Research
Sokal, R. R., & Rohlf, F. J. (1969) · Cited by 20,963 · see citing works
Biometry. The Principles and Practice of Statistics in Biological Research
Fienberg, S. E., Sokal, R. R., Rohlf, F. J., Rohlf, F. J., & Sokal, R. R. (1970) · Biometrics · doi:10.2307/2529087 · Cited by 9,363 · see citing works
Interneurons of the neocortical inhibitory system
Markram, H., Toledo-Rodriguez, M., Wang, Y., Gupta, A., Silberberg, G., & Wu, C. (2004) · Nature Reviews Neuroscience · doi:10.1038/nrn1519 · Cited by 2,954 · see citing works
Parvalbumin neurons and gamma rhythms enhance cortical circuit performance
Sohal, V. S., Zhang, F., Yizhar, O., & Deisseroth, K. (2009) · Nature · doi:10.1038/nature07991 · Cited by 2,606 · see citing works
Driving 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
A resource of Cre driver lines for genetic targeting of GABAergic neurons in cerebral cortex
Taniguchi, H., He, M., Wu, P., Kim, S., Paik, R., Sugino, K., Kvitsani, D., Fu, Y., Lu, J., Lin, Y., et al. (2011) · Neuron · doi:10.1016/j.neuron.2011.07.026 · Cited by 1,828 · see citing works
Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex
The Petilla Interneuron Nomenclature Group (PING) (2008) · Nature Reviews Neuroscience · doi:10.1038/nrn2402 · Cited by 1,491 · see citing works
Modulation of visual responses by behavioral state in mouse visual cortex
Niell, C. M., & Stryker, M. P. (2010) · Neuron · doi:10.1016/j.neuron.2010.01.033 · Cited by 1,483 · cited 1× · see citing works
“After 1–3 hr of recovery, animals were placed in a head holder on a free-spinning spherical treadmill (modified from Niell and Stryker, 2010) and the silicone plug was removed.”
GABAergic cell subtypes and their synaptic connections in rat frontal cortex
Kawaguchi, Y. (1997) · Cerebral Cortex · doi:10.1093/cercor/7.6.476 · Cited by 1,416 · see citing works
A toolbox of Cre-dependent optogenetic transgenic mice for light-induced activation and silencing
Madisen, L., Mao, T., Koch, H., Zhuo, J.-M., Berenyi, A., Fujisawa, S., Hsu, Y.-W. A., Garcia, A. J., Gu, X., Zanella, S., et al. (2012) · Nature Neuroscience · doi:10.1038/nn.3078 · Cited by 1,398 · see citing works
Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex
Wehr, M., & Zador, A. M. (2003) · Nature · doi:10.1038/nature02116 · Cited by 1,363 · 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
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
Differences between somatic and dendritic inhibition in the hippocampus
Miles, R., Tóth, K., Gulyás, A. I., Hájos, N., & Freund, T. F. (1996) · Neuron · doi:10.1016/s0896-6273(00)80101-4 · Cited by 942 · 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
“In addition, many types of cortical interneurons selectively inhibit one another; activation of one type may thus reduce the inhibition originating from others, producing complex changes in activity and tuning (Jiang et al., 2013; Lee et al., 2013; Pi et al., 2013; Xu et al., 2013; Fu et al., 2014).”
New insights into the classification and nomenclature of cortical GABAergic interneurons
DeFelipe, J., López-Cruz, P. L., Benavides-Piccione, R., Bielza, C., Larrañaga, P., Anderson, S., Burkhalter, A., Cauli, B., Fairén, A., Feldmeyer, D., et al. (2013) · Nature Reviews Neuroscience · doi:10.1038/nrn3444 · Cited by 833 · see citing works
Disynaptic Inhibition between Neocortical Pyramidal Cells Mediated by Martinotti Cells
Silberberg, G., & Markram, H. (2007) · Neuron · doi:10.1016/j.neuron.2007.02.012 · Cited by 768 · 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
Equalizing excitation-inhibition ratios across visual cortical neurons
Xue, M., Atallah, B. V., & Scanziani, M. (2014) · Nature · doi:10.1038/nature13321 · Cited by 722 · see citing works
A 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
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
Freund, T. F., & Katona, I. (2007) · Neuron · doi:10.1016/j.neuron.2007.09.012 · Cited by 656 · 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
Shunting Inhibition Modulates Neuronal Gain during Synaptic Excitation
Mitchell, S. J., & Silver, R. A. (2003) · Neuron · doi:10.1016/s0896-6273(03)00200-9 · Cited by 602 · 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
Pyramidal cell communication within local networks in layer 2/3 of rat neocortex.
Holmgren, C., Harkany, T., Svennenfors, B., & Zilberter, Y. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2003.044784 · Cited by 573 · 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
Kawaguchi, Y., & Kubota, Y. (1993) · Journal of Neurophysiology · doi:10.1152/jn.1993.70.1.387 · Cited by 558 · see citing works
Cardin, J. A., Carlén, M., Meletis, K., Knoblich, U., Zhang, F., Deisseroth, K. A., Tsai, L., & Moore, C. I. (2010) · Nature Protocols · doi:10.1038/nprot.2009.228 · Cited by 542 · see citing works
Distinct behavioural and network correlates of two interneuron types in prefrontal cortex
Kvitsiani, D., Ranade, S., Hangya, B., Taniguchi, H., Huang, J. Z., & Kepecs, A. (2013) · Nature · doi:10.1038/nature12176 · Cited by 516 · see citing works
Hendry, S. H. C., Jones, E. G., Emson, P. C., Lawson, D. E. M., Heizmann, C. W., & Streit, P. (1989) · Experimental Brain Research · doi:10.1007/bf00247904 · Cited by 512 · see citing works
Wang, Y., Toledo‐Rodriguez, M., Gupta, A., Wu, C., Silberberg, G., Luo, J., & Markram, H. (2004) · The Journal of Physiology · doi:10.1113/jphysiol.2004.073353 · Cited by 491 · see citing works
Inhibitory Stabilization of the Cortical Network Underlies Visual Surround Suppression
Ozeki, H., Finn, I. M., Schaffer, E., Miller, K. D., & Ferster, D. (2009) · Neuron · doi:10.1016/j.neuron.2009.03.028 · Cited by 470 · see citing works
Corticonics: Neural Circuits of the Cerebral Cortex
Braitenberg, V. (1992) · Trends in Neurosciences · doi:10.1016/0166-2236(92)90361-b · Cited by 425 · see citing works
Thomson, A. M. (2002) · Cerebral Cortex · doi:10.1093/cercor/12.9.936 · Cited by 420 · see citing works
Fine-scale specificity of cortical networks depends on inhibitory cell type and connectivity
Yoshimura, Y., & Callaway, E. M. (2005) · Nature Neuroscience · doi:10.1038/nn1565 · Cited by 390 · see citing works
Neocortical Somatostatin-Expressing GABAergic Interneurons Disinhibit the Thalamorecipient Layer 4
Xu, H., Jeong, H.-Y., Tremblay, R., & Rudy, B. (2013) · Neuron · doi:10.1016/j.neuron.2012.11.004 · Cited by 366 · see citing works
Paradoxical Effects of External Modulation of Inhibitory Interneurons
Tsodyks, M. V., Skaggs, W. E., B, T. J. S. A., & McNaughton, B. L. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-11-04382.1997 · Cited by 364 · see citing works
The organization of two new cortical interneuronal circuits
Jiang, X., Wang, G., Lee, A. J., Stornetta, R. L., & Zhu, J. J. (2013) · Nature Neuroscience · doi:10.1038/nn.3305 · Cited by 338 · see citing works
Visualization of chandelier cell axons by parvalbumin immunoreactivity in monkey cerebral cortex.
DeFelipe, J., Hendry, S. H. C., & Jones, E. G. (1989) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.86.6.2093 · Cited by 338 · see citing works
Kawaguchi, Y., & Kubota, Y. (1998) · Neuroscience · doi:10.1016/s0306-4522(97)00685-4 · Cited by 294 · see citing works
Tamás, G., Buhl, E. H., & Somogyi, P. (1997) · The Journal of Physiology · doi:10.1113/jphysiol.1997.sp022054 · Cited by 278 · see citing works
Shunting Inhibition Does Not Have a Divisive Effect on Firing Rates
Holt, G. R., & Koch, C. (1997) · Neural Computation · doi:10.1162/neco.1997.9.5.1001 · Cited by 250 · see citing works
Gain control of firing rate by shunting inhibition: Roles of synaptic noise and dendritic saturation
Prescott, S. A., & De Koninck, Y. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0337591100 · Cited by 226 · see citing works
Parvalbumin-Expressing Inhibitory Interneurons in Auditory Cortex Are Well-Tuned for Frequency
Moore, A. K., & Wehr, M. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.0663-13.2013 · Cited by 225 · see citing works
Kaur, S., Lazar, R., & Metherate, R. (2004) · Journal of Neurophysiology · doi:10.1152/jn.01121.2003 · Cited by 197 · see citing works
State changes rapidly modulate cortical neuronal responsiveness
Hasenstaub, A., Sachdev, R. N. S., & McCormick, D. A. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.2184-07.2007 · Cited by 196 · see citing works
Self-citationGABA-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
An arithmetic rule for spatial summation of excitatory and inhibitory inputs in pyramidal neurons
Jiang, H., Wang, X.-D., Dan, Y., Poo, M., & Zhang, X.-H. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0912022106 · Cited by 145 · see citing works
Gamma-aminobutyric acid circuits shape response properties of auditory cortex neurons
Wang, J., McFadden, S. L., Caspary, D. M., & Salvi, R. (2002) · Brain Research · doi:10.1016/s0006-8993(02)02926-8 · Cited by 144 · see citing works
Stokes, C. C. A., & Isaacson, J. S. (2010) · Neuron · doi:10.1016/j.neuron.2010.06.029 · Cited by 144 · see citing works
Arithmetical operations performed by nerve cells
Blomfield, S. (1974) · Brain Research · doi:10.1016/0006-8993(74)90375-8 · Cited by 143 · see citing works
Benshalom, G., & White, E. L. (1986) · The Journal of Comparative Neurology · doi:10.1002/cne.902530303 · Cited by 131 · 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
Location-Dependent Effects of Inhibition on Local Spiking in Pyramidal Neuron Dendrites
Jadi, M. P., Poleg-Polsky, A., Schiller, J., & Mel, B. W. (2012) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1002550 · Cited by 121 · see citing works
Volkov, I. O., & Galazyuk, A. V. (1991) · Neuroscience · doi:10.1016/0306-4522(91)90295-y · Cited by 115 · see citing works
Intracellular study of the cat's primary auditory cortex
de Ribaupierre, F., Goldstein, M. H., & Yeni–Komshian, G. H. (1972) · Brain Research · doi:10.1016/0006-8993(72)90178-3 · Cited by 114 · see citing works
Evidence for a Computational Distinction Between Proximal and Distal Neuronal Inhibition
Vu, E. T., & Krasne, F. B. (1992) · Science · doi:10.1126/science.1553559 · Cited by 112 · see citing works
Subtractive and Divisive Inhibition: Effect of Voltage-Dependent Inhibitory Conductances and Noise
Doiron, B., Longtin, A., Berman, N. J., & Maler, L. (2001) · Neural Computation · doi:10.1162/089976601300014691 · Cited by 110 · see citing works
Laminar Analysis of Inhibition in the Gerbil Primary Auditory Cortex
Foeller, E., Vater, M., & Kössl, M. (2001) · Journal of the Association for Research in Otolaryngology · doi:10.1007/s101620010069 · Cited by 71 · see citing works
Response-dependent dynamics of cell-specific inhibition in cortical networks in vivo
El-Boustani, S., & Sur, M. (2014) · Nature Communications · doi:10.1038/ncomms6689 · Cited by 61 · see citing works
Somatostatin cells regulate sensory response fidelity via subtractive inhibition in olfactory cortex
Sturgill, J. F., & Isaacson, J. S. (2015) · Nature Neuroscience · doi:10.1038/nn.3971 · Cited by 49 · see citing works
Divisive inhibition in recurrent networks
Chance, F. S., & Abbott, L. F. (2000) · Network Computation in Neural Systems · doi:10.1088/0954-898x_11_2_301 · Cited by 49 · see citing works
Atallah, B. V., Scanziani, M., & Carandini, M. (2014) · Nature · doi:10.1038/nature13129 · Cited by 34 · see citing works
Tuckwell, H. C. (1986) · Biological Cybernetics · doi:10.1007/bf00341923 · Cited by 11 · see citing works
Flagged first, then by citations
2 of the 68 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Waking 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
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
Circuits and Mechanisms for Surround Modulation in Visual Cortex
Angelucci, A., Bijanzadeh, M., Nurminen, L., Federer, F., Merlin, S., & Bressloff, P. C. (2017) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-072116-031418 · Cited by 268 · see citing works
Spatiotemporal constraints on optogenetic inactivation in cortical circuits
Li, N., Chen, S., Guo, Z. V., Chen, H., Huo, Y., Inagaki, H., Chen, G., Davis, C., Hansel, D., Guo, C., et al. (2019) · eLife · doi:10.7554/elife.48622 · Cited by 215 · see citing works
Somatostatin-Expressing Inhibitory Interneurons in Cortical Circuits
Yavorska, I., & Wehr, M. (2016) · Frontiers in Neural Circuits · doi:10.3389/fncir.2016.00076 · Cited by 185 · see citing works
A Corticothalamic Circuit for Dynamic Switching between Feature Detection and Discrimination
Guo, W., Clause, A. R., Barth‐Maron, A., & Polley, D. B. (2017) · Neuron · doi:10.1016/j.neuron.2017.05.019 · Cited by 179 · see citing works
Inhibitory stabilization and visual coding in cortical circuits with multiple interneuron subtypes
Litwin-Kumar, A., Rosenbaum, R., & Doiron, B. (2016) · Journal of Neurophysiology · doi:10.1152/jn.00732.2015 · Cited by 138 · see citing works
Inhibitory Circuits in Cortical Layer 5
Naka, A., & Adesnik, H. (2016) · Frontiers in Neural Circuits · doi:10.3389/fncir.2016.00035 · Cited by 130 · see citing works
Asymmetric effects of activating and inactivating cortical interneurons
Phillips, E. A. K., & Hasenstaub, A. R. (2016) · eLife · doi:10.7554/elife.18383 · Cited by 127 · 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
Cortical Interneurons Differentially Shape Frequency Tuning following Adaptation
Natan, R. G., Rao, W., & Geffen, M. N. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.10.012 · Cited by 125 · see citing works
Inhibitory control of correlated intrinsic variability in cortical networks
Stringer, C., Pachitariu, M., Steinmetz, N. A., Okun, M., Barthó, P., Harris, K. D., Sahani, M., & Lesica, N. A. (2016) · eLife · doi:10.7554/elife.19695 · Cited by 100 · see citing works
Rapid Rebalancing of Excitation and Inhibition by Cortical Circuitry
Moore, A. K., Weible, A. P., Balmer, T. S., Trussell, L. O., & Wehr, M. (2018) · Neuron · doi:10.1016/j.neuron.2018.01.045 · Cited by 94 · see citing works
Jang, H. J., Chung, H., Rowland, J. M., Richards, B. A., Kohl, M. M., & Kwag, J. (2020) · Science Advances · doi:10.1126/sciadv.aay5333 · Cited by 71 · see citing works
Cortical Interneurons Differentially Regulate the Effects of Acoustic Context
Phillips, E. A. K., Schreiner, C. E., & Hasenstaub, A. R. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.07.001 · Cited by 67 · see citing works
Self-citationdel Molino, L. C. G., Yang, G. R., Mejías, J. F., & Wang, X. (2017) · eLife · doi:10.7554/elife.29742 · Cited by 70 · see citing works
Auditory cortex shapes sound responses in the inferior colliculus
Blackwell, J. M., Lesicko, A. M., Rao, W., De Biasi, M., & Geffen, M. N. (2020) · eLife · doi:10.7554/elife.51890 · Cited by 68 · see citing works
Movement and VIP Interneuron Activation Differentially Modulate Encoding in Mouse Auditory Cortex
Bigelow, J., Morrill, R. J., DeKloe, J., & Hasenstaub, A. R. (2019) · eNeuro · doi:10.1523/eneuro.0164-19.2019 · Cited by 66 · see citing works
Self-citationCortical Microcircuit Mechanisms of Mismatch Negativity and Its Underlying Subcomponents
Ross, J. M., & Hamm, J. P. (2020) · Frontiers in Neural Circuits · doi:10.3389/fncir.2020.00013 · Cited by 60 · see citing works
Heeger, D. J., & Mackey, W. E. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1911633116 · Cited by 54 · see citing works
White Noise Background Improves Tone Discrimination by Suppressing Cortical Tuning Curves
Christensen, R. K., Lindén, H., Nakamura, M., & Barkat, T. R. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.10.049 · Cited by 55 · see citing works
Separable gain control of ongoing and evoked activity in the visual cortex by serotonergic input
Azimi, Z., Barzan, R., Spoida, K., Surdin, T., Wollenweber, P., Mark, M. D., Herlitze, S., & Jancke, D. (2020) · eLife · doi:10.7554/elife.53552 · Cited by 58 · see citing works
Inhibition in the auditory cortex
Studer, F., & Barkat, T. R. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.11.021 · Cited by 52 · see citing works
Maor, I., Shalev, A., & Mizrahi, A. (2016) · Cerebral Cortex · doi:10.1093/cercor/bhw266 · Cited by 53 · see citing works
Cell-specific gain modulation by synaptically released zinc in cortical circuits of audition
Anderson, C. T., Kumar, M., Xiong, S., & Tzounopoulos, T. (2017) · eLife · doi:10.7554/elife.29893 · Cited by 51 · see citing works
Cone, J. J., Scantlen, M. D., Histed, M. H., & Maunsell, J. H. R. (2019) · eNeuro · doi:10.1523/eneuro.0337-18.2019 · Cited by 49 · see citing works
Blackwell, J. M., & Geffen, M. N. (2017) · Nature Communications · doi:10.1038/s41467-017-01755-2 · Cited by 46 · see citing works
Cortical microcircuits as gated-recurrent neural networksPreprint
Costa, R. P., Assael, Y., Shillingford, B., de Freitas, N., & Vogels, T. P. (2017) · arXiv (Cornell University) · doi:10.48550/arxiv.1711.02448 · Cited by 45 · see citing works
Learning to live with Dale’s principle: ANNs with separate excitatory and inhibitory unitsPreprint
Cornford, J. H., Kalajdzievski, D., Leite, M., Lamarquette, A., Kullmann, D. M., & Richards, B. A. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.11.02.364968 · Cited by 43 · see citing works
Capogna, M., Castillo, P. E., & Maffei, A. (2020) · European Journal of Neuroscience · doi:10.1111/ejn.14907 · Cited by 41 · see citing works
Neural Correlates of Learning Pure Tones or Natural Sounds in the Auditory Cortex
Maor, I., Shwartz-Ziv, R., Feigin, L., Elyada, Y. M., Sompolinsky, H., & Mizrahi, A. (2020) · Frontiers in Neural Circuits · doi:10.3389/fncir.2019.00082 · Cited by 42 · see citing works
Inhibition by Somatostatin Interneurons in Olfactory Cortex
Large, A. M., Kunz, N. A., Mielo, S. L., & Oswald, A.-M. M. (2016) · Frontiers in Neural Circuits · doi:10.3389/fncir.2016.00062 · Cited by 38 · see citing works
IGFBP2 Plays an Essential Role in Cognitive Development during Early Life
Khan, S., Lu, X., Huang, Q. D., Tang, J., Weng, J., Yang, Z., Lv, M., Xu, X., Xia, F., Zhang, M., et al. (2019) · Advanced Science · doi:10.1002/advs.201901152 · Cited by 29 · see citing works
Parvalbumin neurons enhance temporal coding and reduce cortical noise in complex auditory scenes
Nocon, J. C., Gritton, H. J., James, N. M., Mount, R. A., Qu, Z., Han, X., & Sen, K. (2023) · Communications Biology · doi:10.1038/s42003-023-05126-0 · Cited by 31 · 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
Rikhye, R. V., Yıldırım, M., Hu, M., Breton‐Provencher, V., & Sur, M. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.3176-20.2021 · Cited by 30 · see citing works
Synaptic Mechanisms for Bandwidth Tuning in Awake Mouse Primary Auditory Cortex
Li, H., Liang, F., Zhong, W., Yan, L., Mesik, L., Xiao, Z., Tao, H. W., & Zhang, L. I. (2018) · Cerebral Cortex · doi:10.1093/cercor/bhy165 · Cited by 30 · see citing works
Kouvaros, S., Kumar, M., & Tzounopoulos, T. (2020) · Cerebral Cortex · doi:10.1093/cercor/bhaa005 · Cited by 24 · see citing works
Amplitude modulation coding in awake mice and squirrel monkeys
Hoglen, N. E. G., Larimer, P., Phillips, E. A. K., Malone, B. J., & Hasenstaub, A. R. (2018) · Journal of Neurophysiology · doi:10.1152/jn.00101.2017 · Cited by 30 · see citing works
Self-citationUntangling stability and gain modulation in cortical circuits with multiple interneuron classesPreprint
Bos, H., Miehl, C., Oswald, A.-M. M., & Doiron, B. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.06.15.148114 · Cited by 29 · see citing works
Translaminar recurrence from layer 5 suppresses superficial cortical layers
Onodera, K., & Kato, H. (2022) · Nature Communications · doi:10.1038/s41467-022-30349-w · Cited by 25 · see citing works
Diverse effects of stimulus history in waking mouse auditory cortex
Phillips, E. A. K., Schreiner, C. E., & Hasenstaub, A. R. (2017) · Journal of Neurophysiology · doi:10.1152/jn.00094.2017 · Cited by 28 · see citing works
Self-citationTask Engagement Improves Neural Discriminability in the Auditory Midbrain of the Marmoset Monkey
Shaheen, L. A., Slee, S. J., & David, S. V. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.1112-20.2020 · Cited by 26 · see citing works
Cell-type-specific responses to associative learning in the primary motor cortex
Lee, C., Harkin, E. F., Yin, X., Naud, R., & Chen, S. X. (2022) · eLife · doi:10.7554/elife.72549 · Cited by 23 · see citing works
The local and long‐range input landscape of inhibitory neurons in mouse auditory cortex
Tasaka, G., Maggi, C., Taha, E. A., & Mizrahi, A. (2022) · The Journal of Comparative Neurology · doi:10.1002/cne.25437 · Cited by 23 · see citing works
Cortical Neural Activity Predicts Sensory Acuity Under Optogenetic Manipulation
Briguglio, J. J., Aizenberg, M., Balasubramanian, V., & Geffen, M. N. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.2457-17.2017 · Cited by 18 · see citing works
Cooke, J. E., Kahn, M. C., Mann, E. O., King, A. J., Schnupp, J. W. H., & Willmore, B. D. B. (2020) · Journal of Neurophysiology · doi:10.1152/jn.00587.2019 · Cited by 20 · see citing works
Torres‐López, C., Cuartero, M. I., García‐Culebras, A., de la Parra, J., Fernández-Valle, M. E., Benito, M., Vázquez‐Reyes, S., Jareño-Flores, T., Castro-Millán, F. J., Hurtado, O., et al. (2023) · Stroke · doi:10.1161/strokeaha.123.043516 · Cited by 19 · see citing works
Slater, B. J., & Isaacson, J. S. (2020) · eNeuro · doi:10.1523/eneuro.0256-20.2020 · Cited by 20 · see citing works
Dynamics of cortical contrast adaptation predict perception of signals in noise
Angeloni, C. F., Młynarski, W. F., Piasini, E., Williams, A. M., Wood, K. C., Garami, L., Hermundstad, A. M., & Geffen, M. N. (2023) · Nature Communications · doi:10.1038/s41467-023-40477-6 · Cited by 17 · see citing works
The Impact of SST and PV Interneurons on Nonlinear Synaptic Integration in the Neocortex
Dorsett, C. R., Philpot, B. D., Smith, S. L., & Smith, I. T. (2021) · eNeuro · doi:10.1523/eneuro.0235-21.2021 · Cited by 16 · see citing works
Gothner, T., Gonçalves, P. J., Sahani, M., Linden, J. F., & Hildebrandt, K. J. (2020) · Cerebral Cortex · doi:10.1093/cercor/bhaa347 · Cited by 15 · see citing works
Barzan, R., Bozkurt, B., Nejad, M. M., Süß, S. T., Surdin, T., Böke, H., Spoida, K., Azimi, Z., Grömmke, M., Eickelbeck, D., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-51861-1 · Cited by 11 · see citing works
Cre-Dependent Optogenetic Transgenic Mice Without Early Age-Related Hearing Loss
Lyngholm, D., & Sakata, S. (2019) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2019.00029 · Cited by 11 · see citing works
Uncertainty-modulated prediction errors in cortical microcircuits
Wilmes, K. A., Petrovici, M. A., Sachidhanandam, S., & Senn, W. (2025) · eLife · doi:10.1101/2023.05.11.540393 · Cited by 10 · see citing works
PV+ Cells Enhance Temporal Population Codes but not Stimulus-Related Timing in Auditory Cortex
Krause, B. M., Murphy, C. A., Uhlrich, D. J., & Banks, M. I. (2017) · Cerebral Cortex · doi:10.1093/cercor/bhx345 · Cited by 11 · see citing works
Spatiotemporal limits of optogenetic manipulations in cortical circuitsPreprint
Li, N., Chen, S., Guo, Z. V., Chen, H., Huo, Y., Inagaki, H., Davis, C., Hansel, D., Guo, C., & Svoboda, K. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/642215 · Cited by 11 · see citing works
Tobin, M., Sheth, J. K., Wood, K. C., Michel, E. K., & Geffen, M. N. (2024) · Journal of Neuroscience · doi:10.1523/jneurosci.1502-23.2024 · Cited by 10 · see citing works
Plasticity in auditory cortex during parenthood
Haimson, B., & Mizrahi, A. (2023) · Hearing Research · doi:10.1016/j.heares.2023.108738 · Cited by 9 · see citing works
Mehra, M., Mukesh, A., & Bandyopadhyay, S. (2022) · Journal of Neuroscience · doi:10.1523/jneurosci.0333-21.2022 · Cited by 9 · see citing works
Saeedi, A., Wang, K., Nikpourian, G., Bartels, A., Logothetis, N. K., Totah, N. K. B., & Watanabe, M. (2024) · Nature Communications · doi:10.1038/s41467-024-46885-6 · Cited by 9 · see citing works
Pairing with Enriched Sound Exposure Restores Auditory Processing Degraded by an Antidepressant
Cheng, Y., Chen, R., Su, B., Zhang, G., Sun, Y., An, P., Fang, Y., Zhang, Y., Shan, Y., de Villers‐Sidani, E., et al. (2023) · Journal of Neuroscience · doi:10.1523/jneurosci.2027-22.2023 · Cited by 8 · see citing works
Shunting Inhibition as a Neural-Inspired Mechanism for Multiplication in Neuromorphic Architectures
Chance, F. S., & Cardwell, S. (2023) · Neuro Inspired Computational Elements Conference (NICE) · doi:10.1145/3584954.3584965 · Cited by 8 · see citing works
Inhibitory control of correlated intrinsic variability in cortical networksPreprint
Stringer, C., Pachitariu, M., Okun, M., Barthó, P., Harris, K., Latham, P. E., Sahani, M., & Lesica, N. A. (2016) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/041103 · Cited by 7 · see citing works
Untangling stability and gain modulation in cortical circuits with multiple interneuron classes
Bos, H., Miehl, C., Oswald, A.-M. M., & Doiron, B. (2025) · eLife · doi:10.7554/elife.99808.4 · Cited by 6 · see citing works
Clayton, K. K., Awwad, B., McGill, M., Stecyk, K. S., Kremer, C., Sudana, K., Skerleva, D., Narayanan, D., Zhu, J., Hancock, K. E., et al. (2025) · Neuron · doi:10.1016/j.neuron.2025.10.017 · Cited by 10 · see citing works
Uncertainty estimation with prediction-error circuits
Hertäg, L., Wilmes, K. A., & Clopath, C. (2025) · Nature Communications · doi:10.1038/s41467-025-58311-6 · Cited by 15 · see citing works
Backpropagation through space, time and the brain
Ellenberger, B., Haider, P., Benitez, F., Jordan, J., Max, K., Jaras, I., Kriener, L., & Petrovici, M. A. (2025) · Nature Communications · doi:10.1038/s41467-025-66666-z · Cited by 6 · see citing works
Untangling stability and gain modulation in cortical circuits with multiple interneuron classesPreprint
Bos, H., Miehl, C., Oswald, A.-M. M., & Doiron, B. (2024) · eLife · doi:10.7554/elife.99808 · Cited by 6 · see citing works
Zou, J., Jin, B., Ao, Y., Han, Y., Huang, B., Jia, Y., Yang, L., Jia, Y., Chen, Q.-C., & Fu, Z. (2023) · Conservation Physiology · doi:10.1093/conphys/coad017 · Cited by 5 · see citing works
Subtraction and division of visual cortical population responses by the serotonergic systemPreprint
Azimi, Z., Spoida, K., Barzan, R., Wollenweber, P., Mark, M. D., Herlitze, S., & Jancke, D. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/444943 · Cited by 5 · see citing works
Spatially targeted inhibitory rhythms differentially affect neuronal integrationPreprint
Headley, D. B., Latimer, B., Aberbach, A., & Nair, S. S. (2024) · eLife · doi:10.7554/elife.95562.1 · Cited by 5 · see citing works
Maximov, K., & Kanold, P. O. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.04.02.646797 · Cited by 5 · see citing works
Quantitative models of auditory cortical processing
Sadagopan, S., Kar, M., & Parida, S. (2023) · Hearing Research · doi:10.1016/j.heares.2023.108697 · Cited by 4 · see citing works
Thomas, K., Azimi, H., Maggioni, D., Sanders, M., Sánchez, P. V., Harvey, M., & Rainer, G. (2025) · Communications Biology · doi:10.1038/s42003-024-07318-8 · Cited by 4 · see citing works
Sun, Y., Liu, B.-H., Tao, H., & Zhang, L. I. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.2492-18.2018 · Cited by 4 · see citing works
Neural correlates of learning pure tones versus natural sounds in the auditory cortexPreprint
Maor, I., Shwartz-Ziv, R., Feigin, L., Elyada, Y. M., Sompolinsky, H., & Mizrahi, A. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/273342 · Cited by 4 · see citing works
Cortical determinants of loudness perception and auditory hypersensitivityPreprint
Clayton, K. K., McGill, M., Awwad, B., Stecyk, K. S., Kremer, C., Skerleva, D., Narayanan, D., Zhu, J., Hancock, K. E., Kujawa, S. G., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.05.30.596691 · Cited by 4 · see citing works
Francavilla, R., Chattopadhyaya, B., Kamda, J. L. D., Jadhav, V., Kourrich, S., Michaud, J. L., & Cristo, G. D. (2024) · eLife · doi:10.7554/elife.97100.4 · Cited by 5 · see citing works
Spatially targeted inhibitory rhythms differentially affect neuronal integrationPreprint
Headley, D. B., Latimer, B., Aberbach, A., & Nair, S. S. (2024) · eLife · doi:10.7554/elife.95562.3 · Cited by 4 · see citing works
Timing Is Everything: Corticothalamic Mechanisms for Active Listening
Linden, J. F. (2017) · Neuron · doi:10.1016/j.neuron.2017.06.032 · Cited by 3 · see citing works
Sensing Sound Through Thalamocortical Afferent Architecture and Cortical Microcircuits
Read, H. L., & Reyes, A. D. (2018) · Springer handbook of auditory research · doi:10.1007/978-3-319-71798-2_7 · Cited by 3 · see citing works
Divisive gain modulation enables flexible and rapid entrainment in a neocortical microcircuit model
Papasavvas, C., Trevelyan, A. J., Kaiser, M., & Wang, Y. (2020) · Journal of Neurophysiology · doi:10.1152/jn.00401.2019 · Cited by 3 · see citing works
Primary Auditory Cortex II. Some Functional Considerations
Malone, B. J., Hasenstaub, A. R., & Schreiner, C. E. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-809324-5.24268-5 · Cited by 3 · see citing works
Self-citationRikhye, R. V., Hu, M., Yıldırım, M., & Sur, M. (2017) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/187062 · Cited by 3 · see citing works
Auditory cortex shapes sound responses in the inferior colliculusPreprint
Blackwell, J. M., Lesicko, A. M. H., Rao, W., Biasi, M. D., & Geffen, M. N. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/584334 · Cited by 4 · see citing works
Somatostatin interneurons in auditory cortex contribute to perceptual categorizationPreprint
Chai, R., Zhang, Y., Xin, Y., Deng, L., & Xu, N.-L. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.07.06.498950 · Cited by 4 · 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
Shahidi, N., Rozenblit, F., Khani, M. H., Schreyer, H. M., Mietsch, M., Protti, D. A., & Gollisch, T. (2025) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1013031 · Cited by 2 · see citing works
Distinct Regulation of History-dependent Responses by Two Cortical Interneuron PopulationsPreprint
Phillips, E. A. K., Schreiner, C. E., & Hasenstaub, A. R. (2017) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/129593 · Cited by 2 · see citing works
Self-citationORGaNICs: A Canonical Neural Circuit ComputationPreprint
Heeger, D. J., & Mackey, W. E. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/506337 · Cited by 2 · see citing works
Uncertainty-modulated prediction errors in cortical microcircuitsPreprint
Wilmes, K. A., Petrovici, M. A., Sachidhanandam, S., & Senn, W. (2024) · eLife · doi:10.7554/elife.95127 · Cited by 2 · see citing works
Untangling stability and gain modulation in cortical circuits with multiple interneuron classesPreprint
Bos, H., Miehl, C., Oswald, A.-M. M., & Doiron, B. (2025) · eLife · doi:10.7554/elife.99808.3 · Cited by 2 · see citing works
Computing the effects of excitatory-inhibitory balance on neuronal input-output properties
Reyes, A. D. (2026) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1013958 · Cited by 1 · see citing works
Rolón‐Martínez, S., Mendoza, A. J., Angeloni, C. F., Vogler, N. W., Drotos, A. C., Aizenberg, M., Chen, R., Vu, K., Haas, J. S., & Geffen, M. N. (2026) · PLoS Biology · doi:10.1371/journal.pbio.3003693 · Cited by 1 · see citing works
Differential coupling of parvalbumin and somatostatin interneurons with adult-born granule cells
Yang, S. M., Groisman, A. I., & Schinder, A. F. (2019) · Greater South Information System · doi:10.60692/bp6f4-r9e67 · Cited by 1 · see citing works
Modulation of adult-born neuron excitability by coupling to GABAergic networks
Yang, S. M., Groisman, A. I., & Schinder, A. F. (2019) · Greater South Information System · doi:10.60692/4a93a-ddm52 · Cited by 1 · see citing works
Paez-Segala, M. G., & Looger, L. L. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-816386-3.00092-2 · Cited by 1 · see citing works
Francavilla, R., Chattopadhyaya, B., Kamda, J. L. D., Jadhav, V., Kourrich, S., Michaud, J. L., & Cristo, G. D. (2024) · eLife · doi:10.7554/elife.97100.1 · Cited by 1 · see citing works
Francavilla, R., Chattopadhyaya, B., Kamda, J. L. D., Jadhav, V., Kourrich, S., Michaud, J. L., & Cristo, G. D. (2024) · eLife · doi:10.7554/elife.97100.2 · Cited by 1 · see citing works
- Authors
- Seybold, B. A., Phillips, E. A. K., Schreiner, C. E., & Hasenstaub, A. R.
- Affiliations
- University of California, San Francisco (US)
- Corresponding author
- Hasenstaub, Andrea R.
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2015-09
- Volume
- 87
- Issue
- 6
- Pages
- 1181-1192
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC4635400
- OpenAlex
- W2117897492
- Cited by
- 118
- References
- 68
- Citations by year
- 2026: 6 · 2025: 13 · 2024: 21 · 2023: 9 · 2022: 5 · 2021: 4 · 2020: 16 · 2019: 12 · 2018: 9 · 2017: 14 · 2016: 8 · 2015: 1
- FWCI
- 6.41
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- National Institute on Deafness and Other Communication Disorders (F31DC012719, R01DC002260, R01DC014101)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Sensory Systems › Hearing, Cochlea, Tinnitus, Genetics
- Keywords
- inhibitory interneurons, somatostatin interneurons, parvalbumin interneurons, divisive inhibition, auditory cortex, network integration, threshold nonlinearity, network models, optogenetic stimulation, cortical inhibition
- MeSH terms
- Animals, Auditory Cortex, Interneurons, Mice, Transgenic, Nerve Net, Neural Inhibition, Mice, Optogenetics
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
