Balanced Excitation and Inhibition Determine Spike Timing during Frequency Adaptation
Open accessAbstract
In layer 4 (L4) of the rat barrel cortex, a single whisker deflection evokes a stereotyped sequence of excitation followed by inhibition, hypothesized to result in a narrow temporal window for spike output. However, awake rats sweep their whiskers across objects, activating the cortex at frequencies known to induce short-term depression at both excitatory and inhibitory synapses within L4. Although periodic whisker deflection causes a frequency-dependent reduction of the cortical response magnitude, whether this adaptation involves changes in the relative balance of excitation and inhibition and how these changes might impact the proposed narrow window of spike timing in L4 is unknown. Here, we demonstrate for the first time that spike output in L4 is determined precisely by the dynamic interaction of excitatory and inhibitory conductances. Furthermore, we show that periodic whisker deflection results in balanced adaptation of the magnitude and timing of excitatory and inhibitory input to L4 neurons. This balanced adaptation mediates a reduction in spike output while preserving the narrow time window of spike generation, suggesting that L4 circuits are calibrated to maintain relative levels of excitation and inhibition across varying magnitudes of input.
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PV+ FS interneurons receive strong thalamic inputs while SOM+ non-FS interneurons receive weaker thalamic inputs.
“For example, PV+ FS interneurons receive strong thalamic inputs16–20 while SOM+ non-FS interneurons receive weaker thalamic inputs21,22.”
From Layer 4 of mouse neocortex differs in cell types and circuit organization between sensory areas (2019) · cites this paper as [18]
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The NEURON Simulation Environment
Hines, M. L., & Carnevale, N. T. (1997) · Neural Computation · doi:10.1162/neco.1997.9.6.1179 · Cited by 2,630 · see citing works
Koch, C. (1998) · Oxford University Press eBooks · doi:10.1093/oso/9780195104912.001.0001 · Cited by 2,306 · see citing works
Reliability of spike timing in neocortical neurons
Mainen, Z. F., & Sejnowski, T. J. (1995) · Science · doi:10.1126/science.7770778 · Cited by 1,950 · see citing works
Synaptic depression and cortical gain control
Abbott, L. F., Varela, J. A., Sen, K., & Nelson, S. B. (1997) · Science · doi:10.1126/science.275.5297.221 · Cited by 1,690 · see citing works
Two networks of electrically coupled inhibitory neurons in neocortex
Gibson, J. R., Beierlein, M., & Connors, B. W. (1999) · Nature · doi:10.1038/47035 · Cited by 1,404 · 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
Enforcement of Temporal Fidelity in Pyramidal Cells by Somatic Feed-Forward Inhibition
Pouille, F., & Scanziani, M. (2001) · Science · doi:10.1126/science.1060342 · Cited by 1,097 · see citing works
Turning on and off recurrent balanced cortical activity
Shu, Y., Hasenstaub, A., & McCormick, D. A. (2003) · Nature · doi:10.1038/nature01616 · Cited by 1,054 · see citing works
Biometric analyses of vibrissal tactile discrimination in the rat
Carvell, G. E., & Simons, D. (1990) · Journal of Neuroscience · doi:10.1523/jneurosci.10-08-02638.1990 · Cited by 870 · see citing works
Analysis of Sniffing of the Albino Rat 1)
Welker, W. (1964) · Behaviour · doi:10.1163/156853964x00030 · Cited by 845 · see citing works
Response properties of vibrissa units in rat SI somatosensory neocortex
Simons, D. J. (1978) · Journal of Neurophysiology · doi:10.1152/jn.1978.41.3.798 · Cited by 771 · see citing works
Thalamocortical responses of mouse somatosensory (barrel) cortexin vitro
Agmon, A., & Connors, B. W. (1991) · Neuroscience · doi:10.1016/0306-4522(91)90333-j · Cited by 673 · see citing works
Fluctuating synaptic conductances recreate in vivo-like activity in neocortical neurons
Destexhe, A., Rudolph, M., Fellous, J.-M., & Sejnowski, T. J. (2001) · Neuroscience · doi:10.1016/s0306-4522(01)00344-x · Cited by 642 · see citing works
Two dynamically distinct inhibitory networks in layer 4 of the neocortex
Beierlein, M., Gibson, J. R., & Connors, B. W. (2003) · Journal of Neurophysiology · doi:10.1152/jn.00283.2003 · Cited by 591 · see citing works
Differential regulation of neocortical synapses by neuromodulators and activity
Gil, Z., Connors, B. W., & Amitai, Y. (1997) · Neuron · doi:10.1016/s0896-6273(00)80380-3 · Cited by 553 · see citing works
Chung, S., Li, X., & Nelson, S. B. (2002) · Neuron · doi:10.1016/s0896-6273(02)00659-1 · Cited by 530 · cited 6× · see citing works
“…suprathreshold responses exhibit frequency-dependent adaptation (Fanselow and Nicolelis, 1999; Ahissar et al., 2000, 2001; Garabedian et al., 2003; Castro-Alamancos, 2004; Khatri et al., 2004) that is at least partially dependent on thalamocortical synaptic depression (Chung et al., 2002).”
BackgroundResultInfluentialSynaptic Mechanisms of Forward Suppression in Rat Auditory Cortex
Wehr, M., & Zador, A. M. (2005) · Neuron · doi:10.1016/j.neuron.2005.06.009 · Cited by 398 · see citing works
Transformation from temporal to rate coding in a somatosensory thalamocortical pathway
Ahissar, E., Sosnik, R., & Haidarliu, S. (2000) · Nature · doi:10.1038/35018568 · Cited by 393 · see citing works
Topography and synaptic shaping of direction selectivity in primary auditory cortex
Zhang, L. I., Tan, A. Y. Y., Schreiner, C. E., & Merzenich, M. M. (2003) · Nature · doi:10.1038/nature01796 · Cited by 377 · see citing works
Feedforward Mechanisms of Excitatory and Inhibitory Cortical Receptive Fields
Bruno, R. M., & Simons, D. J. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-24-10966.2002 · Cited by 354 · see citing works
Fast-spike Interneurons and Feedforward Inhibition in Awake Sensory Neocortex
Swadlow, H. A. (2002) · Cerebral Cortex · doi:10.1093/cercor/13.1.25 · Cited by 354 · see citing works
Contrast gain control in the cat visual cortex
Ohzawa, I., Sclar, G., & Freeman, R. D. (1982) · Nature · doi:10.1038/298266a0 · Cited by 348 · see citing works
Behavioral Modulation of Tactile Responses in the Rat Somatosensory System
Fanselow, E. E., & Nicolelis, M. A. L. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-17-07603.1999 · Cited by 345 · see citing works
Porter, J. T., Johnson, C. K., & Agmon, A. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-08-02699.2001 · Cited by 344 · see citing works
Brecht, M., & Sakmann, B. J. (2002) · The Journal of Physiology · doi:10.1113/jphysiol.2002.018465 · Cited by 341 · see citing works
Temporal and spatial integration in the rat SI vibrissa cortex
Simons, D. J. (1985) · Journal of Neurophysiology · doi:10.1152/jn.1985.54.3.615 · Cited by 325 · see citing works
Feed‐forward inhibition shapes the spike output of cerebellar Purkinje cells
Mittmann, W., Koch, U., & Häusser, M. (2004) · The Journal of Physiology · doi:10.1113/jphysiol.2004.075028 · Cited by 317 · see citing works
Invariant computations in local cortical networks with balanced excitation and inhibition
Mariño, J., Schummers, J., Lyon, D. C., Schwabe, L., Beck, O., Wiesing, P., Obermayer, K., & Sur, M. (2005) · Nature Neuroscience · doi:10.1038/nn1391 · Cited by 308 · see citing works
Direction Selectivity of Excitation and Inhibition in Simple Cells of the Cat Primary Visual Cortex
Priebe, N. J., & Ferster, D. (2005) · Neuron · doi:10.1016/j.neuron.2004.12.024 · Cited by 250 · see citing works
Circuit dynamics and coding strategies in rodent somatosensory cortex
Pinto, D. J., Brumberg, J. C., & Simons, D. J. (2000) · Journal of Neurophysiology · doi:10.1152/jn.2000.83.3.1158 · Cited by 239 · see citing works
Fee, M. S., Mitra, P. P., & Kleinfeld, D. (1997) · Journal of Neurophysiology · doi:10.1152/jn.1997.78.2.1144 · Cited by 230 · see citing works
Absence of Rapid Sensory Adaptation in Neocortex during Information Processing States
Castro‐Alamancos, M. A. (2004) · Neuron · doi:10.1016/s0896-6273(03)00853-5 · Cited by 228 · see citing works
Ahissar, E., & Arieli, A. (2001) · Neuron · doi:10.1016/s0896-6273(01)00466-4 · Cited by 226 · see citing works
Staiger, J. F. (2004) · Cerebral Cortex · doi:10.1093/cercor/bhh029 · Cited by 226 · see citing works
A Synaptic Explanation of Suppression in Visual Cortex
Carandini, M., Heeger, D. J., & Senn, W. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-22-10053.2002 · Cited by 219 · see citing works
Cell Type-Specific Circuits of Cortical Layer IV Spiny Neurons
Schubert, D., Kötter, R., Zilles, K., Luhmann, H. J., & Staiger, J. F. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-07-02961.2003 · Cited by 207 · see citing works
Castro‐Alamancos, M. A., & Oldford, E. (2002) · The Journal of Physiology · doi:10.1113/jphysiol.2002.016857 · Cited by 185 · see citing works
Armstrong‐James, M., Welker, E., & Callahan, C. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-05-02149.1993 · Cited by 171 · see citing works
Multi-whisker stimulation and its effects on vibrissa units in rat Sml barrel cortex
Simons, D. J. (1983) · Brain Research · doi:10.1016/0006-8993(83)90561-9 · Cited by 162 · see citing works
Nathan, T., Jensen, M. S., & Lambert, J. D. C. (1990) · Neuroscience Letters · doi:10.1016/0304-3940(90)90865-7 · Cited by 158 · see citing works
Temporal Frequency of Whisker Movement. I. Representations in Brain Stem and Thalamus
Sosnik, R., Haidarliu, S., & Ahissar, E. (2001) · Journal of Neurophysiology · doi:10.1152/jn.2001.86.1.339 · Cited by 157 · see citing works
Thomson, A. M., & West, D. C. (1993) · Neuroscience · doi:10.1016/0306-4522(93)90256-f · Cited by 155 · 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
Temporal Frequency of Whisker Movement. II. Laminar Organization of Cortical Representations
Ahissar, E., Sosnik, R., Bagdasarian, K., & Haidarliu, S. (2001) · Journal of Neurophysiology · doi:10.1152/jn.2001.86.1.354 · Cited by 139 · see citing works
Wilent, W. B., & Contreras, D. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.5782-03.2004 · Cited by 138 · see citing works
Self-citationCortical damping: analysis of thalamocortical response transformations in rodent barrel cortex
Pinto, D. J. (2003) · Cerebral Cortex · doi:10.1093/cercor/13.1.33 · Cited by 137 · see citing works
Timing and Specificity of Feed-Forward Inhibition within the LGN
Blitz, D. M., & Regehr, W. G. (2005) · Neuron · doi:10.1016/j.neuron.2005.01.033 · Cited by 132 · see citing works
Khatri, V., Hartings, J. A., & Simons, D. J. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00257.2004 · Cited by 124 · see citing works
Perkins, K. L., & Wong, R. K. S. (1995) · Journal of Neurophysiology · doi:10.1152/jn.1995.73.2.911 · Cited by 115 · see citing works
Hellweg, F.-C., Schultz, W., & Creutzfeldt, O. D. (1977) · Journal of Neurophysiology · doi:10.1152/jn.1977.40.3.463 · Cited by 112 · see citing works
Beierlein, M., Fall, C. P., Rinzel, J., & Yuste, R. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-22-09885.2002 · Cited by 104 · see citing works
Intracellular QX-314 inhibits calcium currents in hippocampal CA1 pyramidal neurons
Talbot, M., & Sayer, R. J. (1996) · Journal of Neurophysiology · doi:10.1152/jn.1996.76.3.2120 · Cited by 99 · see citing works
Thalamocortical response transformations in simulated whisker barrels
Kyriazi, H. T., & Simons, D. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-04-01601.1993 · Cited by 96 · see citing works
Band-Pass Response Properties of Rat SI Neurons
Garabedian, C. E., Jones, S. R., Merzenich, M. M., Dale, A. M., & Moore, C. I. (2003) · Journal of Neurophysiology · doi:10.1152/jn.01158.2002 · Cited by 95 · see citing works
The Origin of Cortical Surround Receptive Fields Studied in the Barrel Cortex
Fox, K. D., Wright, N. F., Wallace, H., & Glazewski, S. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-23-08380.2003 · Cited by 88 · see citing works
The Influence of Single VB Thalamocortical Impulses on Barrel Columns of Rabbit Somatosensory Cortex
Swadlow, H. A., & Gusev, A. G. (2000) · Journal of Neurophysiology · doi:10.1152/jn.2000.83.5.2802 · Cited by 84 · see citing works
White, E. L., & Rock, M. P. (1981) · Journal of Comparative Neurology · doi:10.1002/cne.901950207 · Cited by 80 · see citing works
Spectral motion produces an auditory after-effect
Shu, Z., Swindale, N. V., & Cynader, M. (1993) · Nature · doi:10.1038/364721a0 · Cited by 72 · see citing works
Nonlinear Integration of Sensory Responses in the Rat Barrel Cortex: An Intracellular StudyIn Vivo
Higley, M. J., & Contreras, D. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-32-10190.2003 · Cited by 70 · see citing works
Self-citationPetersen, C. C. H. (2002) · Journal of Neurophysiology · doi:10.1152/jn.2002.87.6.2904 · Cited by 51 · see citing works
Axmacher, N., & Miles, R. (2004) · The Journal of Physiology · doi:10.1113/jphysiol.2003.052225 · Cited by 47 · see citing works
Thalamic Relay of Afferent Responses to 1- to 12-Hz Whisker Stimulation in the Rat
Hartings, J. A., & Simons, D. J. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.80.2.1016 · Cited by 46 · see citing works
Functional Connectivity in Layer IV Local Excitatory Circuits of Rat Somatosensory Cortex
Cowan, A. I., & Stricker, C. (2004) · Journal of Neurophysiology · doi:10.1152/jn.01262.2003 · Cited by 43 · see citing works
Integration of Synaptic Responses to Neighboring Whiskers in Rat Barrel Cortex In Vivo
Higley, M. J., & Contreras, D. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00917.2004 · Cited by 43 · see citing works
Self-citationGardner, E. P., Palmėr, C., Hämäläinen, H., & Warren, S. (1992) · Journal of Neurophysiology · doi:10.1152/jn.1992.67.1.37 · Cited by 27 · see citing works
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Tremblay, R., Lee, S., & Rudy, B. (2016) · Neuron · doi:10.1016/j.neuron.2016.06.033 · Cited by 2,033 · see citing works
“, 2003; Wilent and Contreras, 2005) and producing cortical responses that more precisely represent the timing of sensory input (Gabernet et al., 2005; Higley and Contreras, 2006).”
How Inhibition Shapes Cortical Activity
Isaacson, J. S., & Scanziani, M. (2011) · Neuron · doi:10.1016/j.neuron.2011.09.027 · Cited by 1,678 · see citing works
Acetylcholine as a Neuromodulator: Cholinergic Signaling Shapes Nervous System Function and Behavior
Picciotto, M. R., Higley, M. J., & Mineur, Y. S. (2012) · Neuron · doi:10.1016/j.neuron.2012.08.036 · Cited by 1,404 · see citing works
Self-citationIntegrated Brain Circuits: Astrocytic Networks Modulate Neuronal Activity and Behavior
Halassa, M. M., & Haydon, P. G. (2010) · Annual Review of Physiology · doi:10.1146/annurev-physiol-021909-135843 · Cited by 835 · see citing works
Synaptic basis for intense thalamocortical activation of feedforward inhibitory cells in neocortex
Cruikshank, S. J., Lewis, T. J., & Connors, B. W. (2007) · Nature Neuroscience · doi:10.1038/nn1861 · Cited by 558 · see citing works
Plasticity of Cortical Excitatory-Inhibitory Balance
Froemke, R. C. (2015) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-071714-034002 · Cited by 458 · 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
Rapid 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
Differences in Gamma Frequencies across Visual Cortex Restrict Their Possible Use in Computation
Ray, S., & Maunsell, J. H. R. (2010) · Neuron · doi:10.1016/j.neuron.2010.08.004 · Cited by 424 · 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
Regulation of spike timing in visual cortical circuits
Tiesinga, P. H. E., Fellous, J., & B, T. J. S. A. (2008) · Nature reviews. Neuroscience · doi:10.1038/nrn2315 · Cited by 352 · see citing works
Inhibition, Spike Threshold, and Stimulus Selectivity in Primary Visual Cortex
Priebe, N. J., & Ferster, D. (2008) · Neuron · doi:10.1016/j.neuron.2008.02.005 · Cited by 359 · see citing works
Balanced Amplification: A New Mechanism of Selective Amplification of Neural Activity Patterns
Murphy, B. K., & Miller, K. D. (2009) · Neuron · doi:10.1016/j.neuron.2009.02.005 · Cited by 338 · see citing works
Lateral Sharpening of Cortical Frequency Tuning by Approximately Balanced Inhibition
Wu, G. K., Arbuckle, R., Liu, B., Tao, H. W., & Zhang, L. I. (2008) · Neuron · doi:10.1016/j.neuron.2008.01.035 · Cited by 276 · see citing works
Haider, B., Krause, M. R., Duque, A., Yu, Y., Touryan, J., Mazer, J. A., & McCormick, D. A. (2010) · Neuron · doi:10.1016/j.neuron.2009.12.005 · Cited by 263 · see citing works
Inhibitory Interneurons Regulate Temporal Precision and Correlations in Cortical Circuits
Cardin, J. A. (2018) · Trends in Neurosciences · doi:10.1016/j.tins.2018.07.015 · Cited by 254 · see citing works
Synaptic Mechanisms Underlying Sparse Coding of Active Touch
Crochet, S., Poulet, J. F. A., Kremer, Y., & Petersen, C. C. H. (2011) · Neuron · doi:10.1016/j.neuron.2011.02.022 · Cited by 241 · see citing works
Moving Sensory Adaptation beyond Suppressive Effects in Single Neurons
Solomon, S. G., & Kohn, A. (2014) · Current Biology · doi:10.1016/j.cub.2014.09.001 · Cited by 239 · see citing works
Layer 4 of mouse neocortex differs in cell types and circuit organization between sensory areas
Scala, F., Kobak, D., Shan, S., Bernaerts, Y., Laturnus, S., Cadwell, C. R., Hartmanis, L., Froudarakis, E., Castro, J. R., Tan, Z. H., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-12058-z · Cited by 193 · see citing works
Inhibitory and Excitatory Spike-Timing-Dependent Plasticity in the Auditory Cortex
D’amour, J. A., & Froemke, R. C. (2015) · Neuron · doi:10.1016/j.neuron.2015.03.014 · Cited by 201 · 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
Rapid Neural Adaptation to Sound Level Statistics
Dean, I., Robinson, B. L., Harper, N. S., & McAlpine, D. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.0470-08.2008 · Cited by 205 · see citing works
Inhibitory Synapses Are Repeatedly Assembled and Removed at Persistent Sites In Vivo
Villa, K. L., Berry, K., Subramanian, J., Cha, J. W., Oh, W. C., Kwon, H., Kubota, Y., So, P. T. C., & Nedivi, E. (2016) · Neuron · doi:10.1016/j.neuron.2016.01.010 · Cited by 198 · see citing works
Ji, X.-Y., Zingg, B., Mesik, L., Xiao, Z., Zhang, L. I., & Tao, H. W. (2016) · Cerebral Cortex · doi:10.1093/cercor/bhv099 · Cited by 176 · see citing works
Stimulus feature selectivity in excitatory and inhibitory neurons in primary visual cortex
Cardin, J. A., Palmer, L. A., & Contreras, D. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.1692-07.2007 · Cited by 185 · see citing works
Self-citationThalamic synchrony and the adaptive gating of information flow to cortex
Wang, Q., Webber, R. M., & Stanley, G. B. (2010) · Nature Neuroscience · doi:10.1038/nn.2670 · Cited by 166 · see citing works
Neuromodulation by acetylcholine: examples from schizophrenia and depression
Higley, M. J., & Picciotto, M. R. (2014) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2014.06.004 · Cited by 184 · see citing works
Self-citationIascone, D. M., Li, Y., Sümbül, U., Doron, M., Chen, H., Andreu, V., Goudy, F., Blockus, H., Abbott, L. F., Segev, I., et al. (2020) · Neuron · doi:10.1016/j.neuron.2020.02.015 · Cited by 165 · see citing works
Coding and Transformations in the Olfactory System
Uchida, N., Poo, C., & Haddad, R. (2014) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-071013-013941 · Cited by 158 · see citing works
Refining the roles of GABAergic signaling during neural circuit formation
Akerman, C. J., & Cline, H. T. (2007) · Trends in Neurosciences · doi:10.1016/j.tins.2007.06.002 · Cited by 159 · see citing works
Robust but delayed thalamocortical activation of dendritic-targeting inhibitory interneurons
Tan, Z., Hu, H., Huang, Z. J., & Agmon, A. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0710628105 · Cited by 155 · see citing works
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Chiu, C. Q., Barberis, A., & Higley, M. J. (2019) · Nature reviews. Neuroscience · doi:10.1038/s41583-019-0141-5 · Cited by 145 · see citing works
Self-citationPostsynaptic mechanisms govern the differential excitation of cortical neurons by thalamic inputs
Hull, C., Isaacson, J. S., & Scanziani, M. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.5971-08.2009 · Cited by 147 · see citing works
Nagappan, P. G., Chen, H., & Wang, D. Y. (2020) · Military Medical Research · doi:10.1186/s40779-020-00259-3 · Cited by 148 · see citing works
Monier, C., Fournier, J., & Frégnac, Y. (2007) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2007.11.008 · Cited by 143 · 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
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Paillé, V., Fino, É., Du, K., Morera‐Herreras, T., Siaume‐Perez, S., Kotaleski, J. H., & Venance, L. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.5796-12.2013 · Cited by 136 · see citing works
Locus coeruleus-norepinephrine modulation of sensory processing and perception: A focused review
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Chen, I.-W., Helmchen, F., & Lütcke, H. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.2240-15.2015 · Cited by 142 · see citing works
Inhibitory synaptic plasticity: spike timing-dependence and putative network function
Vogels, T. P., Froemke, R. C., Doyon, N., Gilson, M., Haas, J. S., Liu, R., Maffei, A., Miller, P. C., Wierenga, C. J., Woodin, M. A., et al. (2013) · Frontiers in Neural Circuits · doi:10.3389/fncir.2013.00119 · Cited by 137 · see citing works
Precise excitation-inhibition balance controls gain and timing in the hippocampus
Bhatia, A., Moza, S., & Bhalla, U. S. (2019) · eLife · doi:10.7554/elife.43415 · Cited by 136 · see citing works
What is the dynamical regime of cerebral cortex?
Ahmadian, Y., & Miller, K. D. (2021) · Neuron · doi:10.1016/j.neuron.2021.07.031 · Cited by 140 · see citing works
Shift in the Balance between Excitation and Inhibition during Sensory Adaptation of S1 Neurons
Heiss, J. E., Katz, Y., Ganmor, E., & Lampl, I. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.2646-08.2008 · Cited by 137 · see citing works
Synaptic Mechanisms of Feature Coding in the Visual Cortex of Awake Mice
Adesnik, H. (2017) · Neuron · doi:10.1016/j.neuron.2017.08.014 · Cited by 130 · see citing works
Orientation Selectivity of Synaptic Input to Neurons in Mouse and Cat Primary Visual Cortex
Tan, A. Y. Y., Brown, B. D., Scholl, B., Mohanty, D., & Priebe, N. J. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.2039-11.2011 · Cited by 121 · see citing works
Alloway, K. D. (2007) · Cerebral Cortex · doi:10.1093/cercor/bhm138 · Cited by 125 · see citing works
Laminar processing in the visual cortical column.
Hirsch, J. A., & Martinez, L. M. (2006) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2006.06.014 · Cited by 120 · see citing works
Intervening inhibition underlies simple-cell receptive field structure in visual cortex
Liu, B., Li, P., Sun, Y. J., Li, Y.-T., Zhang, L. I., & Tao, H. W. (2009) · Nature Neuroscience · doi:10.1038/nn.2443 · Cited by 122 · see citing works
Magnusson, A. K., Park, T. J., Pecka, M., Grothe, B., & Koch, U. (2008) · Neuron · doi:10.1016/j.neuron.2008.05.011 · Cited by 116 · see citing works
The Anatomy and Physiology of Claustrum-Cortex Interactions
Jackson, J., Smith, J. B., & Lee, A. K. (2020) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-092519-101637 · Cited by 115 · see citing works
Mittmann, W., & Häusser, M. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.5117-06.2007 · Cited by 111 · see citing works
Regulation of Irregular Neuronal Firing by Autaptic Transmission
Guo, D., Wu, S., Chen, M., Perc, M., Zhang, Y., Ma, J., Cui, Y., Xu, P., Xia, Y., & Yao, D. (2016) · Scientific Reports · doi:10.1038/srep26096 · Cited by 107 · see citing works
Frequency-specific modulation of population-level frequency tuning in human auditory cortex
Okamoto, H., Stracke, H., Zwitserlood, P., Roberts, L. E., & Pantev, C. (2009) · BMC Neuroscience · doi:10.1186/1471-2202-10-1 · Cited by 107 · see citing works
Coding Principles in Adaptation
Weber, A. I., Krishnamurthy, K., & Fairhall, A. L. (2019) · Annual Review of Vision Science · doi:10.1146/annurev-vision-091718-014818 · Cited by 103 · see citing works
Cortical Excitation and Inhibition Following Focal Traumatic Brain Injury
Ding, M., Wang, Q., Lo, E. H., & Stanley, G. B. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.3572-11.2011 · Cited by 103 · see citing works
Carvalho, T. P., & Buonomano, D. V. (2009) · Neuron · doi:10.1016/j.neuron.2009.01.013 · Cited by 100 · see citing works
Serotoninergic Fine-Tuning of the Excitation–Inhibition Balance in Rat Visual Cortical Networks
Moreau, A. W., Amar, M., Roux, N. L., Morel, N., & Fossier, P. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhp114 · Cited by 95 · see citing works
Plasticity during sleep is linked to specific regulation of cortical circuit activity
Niethard, N., Burgalossi, A., & Born, J. (2017) · Frontiers in Neural Circuits · doi:10.3389/fncir.2017.00065 · Cited by 89 · see citing works
Preceding Inhibition Silences Layer 6 Neurons in Auditory Cortex
Zhou, Y., Liu, B., Wu, G. K., Kim, Y.-J., Xiao, Z., Tao, H. W., & Zhang, L. I. (2010) · Neuron · doi:10.1016/j.neuron.2010.02.021 · Cited by 94 · see citing works
Microcircuits Mediating Feedforward and Feedback Synaptic Inhibition in the Piriform Cortex
Suzuki, N., & Bekkers, J. M. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.4112-11.2012 · Cited by 94 · see citing works
Localized GABAergic inhibition of dendritic Ca2+ signalling
Higley, M. J. (2014) · Nature reviews. Neuroscience · doi:10.1038/nrn3803 · Cited by 87 · see citing works
Self-citationThe adaptive trade-off between detection and discrimination in cortical representations and behavior
Ollerenshaw, D., Zheng, H. J. V., Millard, D. C., Wang, Q., & Stanley, G. B. (2014) · Neuron · doi:10.1016/j.neuron.2014.01.025 · Cited by 107 · see citing works
Snapshots of the Brain in Action: Local Circuit Operations through the Lens of γ Oscillations
Cardin, J. A. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.1021-16.2016 · Cited by 88 · see citing works
Heterosynaptic Plasticity Determines the Set Point for Cortical Excitatory-Inhibitory Balance
Field, R. E., D’amour, J. A., Tremblay, R., Miehl, C., Rudy, B., Gjorgjieva, J., & Froemke, R. C. (2020) · Neuron · doi:10.1016/j.neuron.2020.03.002 · Cited by 86 · see citing works
Neural Correlation Is Stimulus Modulated by Feedforward Inhibitory Circuitry
Middleton, J. W., Omar, C., Doiron, B., & Simons, D. J. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.3474-11.2012 · Cited by 85 · see citing works
Derdikman, D., Yu, C., Haidarliu, S., Bagdasarian, K., Arieli, A., & Ahissar, E. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.0918-06.2006 · Cited by 84 · see citing works
Sellers, K. K., Bennett, D., Hutt, A., Williams, J. H., & Frӧhlich, F. (2015) · Journal of Neurophysiology · doi:10.1152/jn.00923.2014 · Cited by 79 · see citing works
Poleg-Polsky, A., & Diamond, J. S. (2011) · PLoS ONE · doi:10.1371/journal.pone.0019463 · Cited by 80 · see citing works
Functional consequences of correlated excitatory and inhibitory conductances in cortical networks
Kremkow, J., Perrinet, L., Masson, G. S., & Aertsen, A. (2010) · Journal of Computational Neuroscience · doi:10.1007/s10827-010-0240-9 · Cited by 82 · see citing works
Vonderschen, K., & Chacron, M. J. (2011) · Journal of Neurophysiology · doi:10.1152/jn.00588.2011 · Cited by 81 · see citing works
Spike-timing-dependent plasticity in the human dorso-lateral prefrontal cortex
Casula, E. P., Pellicciari, M. C., Picazio, S., Caltagirone, C., & Koch, G. (2016) · NeuroImage · doi:10.1016/j.neuroimage.2016.08.060 · Cited by 76 · see citing works
Pelled, G., Chuang, K., Dodd, S. J., & Koretsky, A. P. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2007.03.069 · Cited by 76 · see citing works
Development of Inhibitory Timescales in Auditory Cortex
Oswald, A.-M. M., & Reyes, A. D. (2010) · Cerebral Cortex · doi:10.1093/cercor/bhq214 · Cited by 77 · see citing works
Torborg, C. L., Nakashiba, T., Tonegawa, S., & McBain, C. J. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.3099-10.2010 · Cited by 76 · see citing works
Petersen, P. C., & Berg, R. W. (2016) · eLife · doi:10.7554/elife.18805 · Cited by 76 · see citing works
Altered hippocampal interneuron activity precedes ictal onset
Miri, M. L., Vinck, M. A., Pant, R., & Cardin, J. A. (2018) · eLife · doi:10.7554/elife.40750 · Cited by 73 · see citing works
Rapid Suppression of Inhibitory Synaptic Transmission by Retinoic Acid
Sarti, F., Zhang, Z., Schroeder, J., & Chen, L. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.1710-13.2013 · Cited by 72 · see citing works
Coupling between somatosensory evoked potentials and hemodynamic response in the rat
Franceschini, M. A., Nissila, I. T., Wu, W., Diamond, S. G., Bonmassar, G., & Boas, D. A. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2008.02.061 · Cited by 74 · see citing works
Single Neuron Firing Properties Impact Correlation-Based Population Coding
Hong, S., Ratté, S., Prescott, S. A., & De Schutter, E. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.3735-11.2012 · Cited by 72 · see citing works
Widespread Inhibition Proportional to Excitation Controls the Gain of a Leech Behavioral Circuit
Baca, S. M., Marín‐Burgin, A., Wagenaar, D. A., & Kristan, W. B. (2008) · Neuron · doi:10.1016/j.neuron.2007.11.028 · Cited by 72 · see citing works
Cellular mechanisms of temporal sensitivity in visual cortex neurons
Cardin, J. A., Kumbhani, R. D., Contreras, D., & Palmer, L. A. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.5279-09.2010 · Cited by 62 · see citing works
Self-citationDevelopment of auditory cortical synaptic receptive fields
Froemke, R. C., & Marlin, B. J. (2011) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2011.02.006 · Cited by 70 · see citing works
Critical branching neural networks.
Kello, C. T. (2013) · Psychological Review · doi:10.1037/a0030970 · Cited by 63 · see citing works
Khazipov, R., Minlebaev, M., & Valeeva, G. R. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.07.019 · Cited by 65 · see citing works
Voltage Fluctuations in Neurons: Signal or Noise?
Yarom, Y., & Hounsgaard, J. (2011) · Physiological Reviews · doi:10.1152/physrev.00019.2010 · Cited by 65 · see citing works
Surround suppression and sparse coding in visual and barrel cortices
Sachdev, R. N. S., Krause, M. R., & Mazer, J. A. (2012) · Frontiers in Neural Circuits · doi:10.3389/fncir.2012.00043 · Cited by 65 · see citing works
Griffen, T. C. (2014) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00091 · Cited by 62 · see citing works
Ganmor, E., Katz, Y., & Lampl, I. (2010) · Neuron · doi:10.1016/j.neuron.2010.03.032 · Cited by 63 · see citing works
Timing Precision in Population Coding of Natural Scenes in the Early Visual System
Desbordes, G., Jin, J., Weng, C., Lesica, N. A., Stanley, G. B., & Alonso, J. (2008) · PLoS Biology · doi:10.1371/journal.pbio.0060324 · Cited by 58 · 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
Homeostatic control of the excitation–inhibition balance in cortical layer 5 pyramidal neurons
Roux, N. L., Amar, M., Baux, G., & Fossier, P. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.05203.x · Cited by 57 · see citing works
Leitch, B. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25105549 · Cited by 53 · see citing works
The neurogenesis of P1 and N1: A concurrent EEG/LFP study
Bruyns‐Haylett, M., Luo, J., Kennerley, A. J., Harris, S., Boorman, L. W., Milne, E., Vautrelle, N., Hayashi, Y., Whalley, B. J., Jones, M., et al. (2016) · NeuroImage · doi:10.1016/j.neuroimage.2016.09.034 · Cited by 52 · see citing works
Sensory-evoked synaptic integration in cerebellar and cerebral cortical neurons
Chadderton, P. T., Schaefer, A. T., Williams, S. R., & Margrie, T. W. (2014) · Nature reviews. Neuroscience · doi:10.1038/nrn3648 · Cited by 50 · see citing works
Facilitating sensory responses in developing mouse somatosensory barrel cortex.
Borgdorff, A., Poulet, J., & Petersen, C. (2007) · Journal of Neurophysiology · doi:10.1152/jn.00013.2007 · Cited by 55 · see citing works
Zhang, Z., & Sun, Q. (2011) · International review of neurobiology · doi:10.1016/b978-0-12-385198-7.00012-6 · Cited by 45 · see citing works
Wang, Y., Zan, G., Xu, C., Li, X., Shu, X., Yao, S.-Y., Xu, X.-S., Qiu, X., Chen, Y., Jin, K., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-43636-x · Cited by 44 · see citing works
D-Serine and Glycine Differentially Control Neurotransmission during Visual Cortex Critical Period
Meunier, C. N. J., Dallérac, G. M., Roux, N. L., Sacchi, S., Levasseur, G., Amar, M., Pollegioni, L., Mothet, J., & Fossier, P. (2016) · PLoS ONE · doi:10.1371/journal.pone.0151233 · Cited by 42 · see citing works
Impaired GABAergic transmission disrupts normal homeostatic plasticity in rat cortical networks
Roux, N. L., Amar, M., Moreau, A. W., Baux, G., & Fossier, P. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06288.x · Cited by 39 · see citing works
- Authors
- Higley, M. J., & Contreras, D.
- Affiliations
- University of Pennsylvania (US)
- Corresponding author
- Contreras, Diego
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2006-01-11
- Volume
- 26
- Issue
- 2
- Pages
- 448-457
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6674406
- OpenAlex
- W2040663063
- Cited by
- 270
- References
- 65
- Citations by year
- 2026: 4 · 2025: 7 · 2024: 8 · 2023: 4 · 2022: 6 · 2021: 7 · 2020: 15 · 2019: 16 · 2018: 10 · 2017: 16 · 2016: 21 · 2015: 17 · 2014: 19 · 2013: 13 · 2012: 19
- FWCI
- 9.23
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- 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 › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- excitation-inhibition balance, spike timing, frequency adaptation, short-term depression, layer 4, barrel cortex, whisker deflection
- MeSH terms
- Action Potentials, Adaptation, Physiological, Animals, Male, Synaptic Transmission, Neurons, Reaction Time, Somatosensory Cortex, Touch, Vibrissae, Rats, Sprague-Dawley, Patch-Clamp Techniques, Excitatory Postsynaptic Potentials, Rats
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