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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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“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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Cites
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
Koch, C. (1998) · Oxford University Press eBooks · doi:10.1093/oso/9780195104912.001.0001 · Cited by 2,306
Reliability of spike timing in neocortical neurons
Mainen, Z. F., & Sejnowski, T. J. (1995) · Science · doi:10.1126/science.7770778 · Cited by 1,950
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
Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex
Wehr, M., & Zador, A. M. (2003) · Nature · doi:10.1038/nature02116 · Cited by 1,413
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
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
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
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
Analysis of Sniffing of the Albino Rat 1)
Welker, W. (1964) · Behaviour · doi:10.1163/156853964x00030 · Cited by 845
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 780
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
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
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
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
Chung, S., Li, X., & Nelson, S. B. (2002) · Neuron · doi:10.1016/s0896-6273(02)00659-1 · Cited by 530 · cited 6×
“…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
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
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
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
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
Contrast gain control in the cat visual cortex
Ohzawa, I., Sclar, G., & Freeman, R. D. (1982) · Nature · doi:10.1038/298266a0 · Cited by 348
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
Porter, J. T., Johnson, C. K., & Agmon, A. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-08-02699.2001 · Cited by 344
Brecht, M., & Sakmann, B. J. (2002) · The Journal of Physiology · doi:10.1113/jphysiol.2002.018465 · Cited by 341
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
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
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
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
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
Fee, M. S., Mitra, P. P., & Kleinfeld, D. (1997) · Journal of Neurophysiology · doi:10.1152/jn.1997.78.2.1144 · Cited by 230
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
Ahissar, E., & Arieli, A. (2001) · Neuron · doi:10.1016/s0896-6273(01)00466-4 · Cited by 226
Staiger, J. F. (2004) · Cerebral Cortex · doi:10.1093/cercor/bhh029 · Cited by 226
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
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
Castro‐Alamancos, M. A., & Oldford, E. (2002) · The Journal of Physiology · doi:10.1113/jphysiol.2002.016857 · Cited by 185
Armstrong‐James, M., Welker, E., & Callahan, C. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-05-02149.1993 · Cited by 171
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
Nathan, T., Jensen, M. S., & Lambert, J. D. C. (1990) · Neuroscience Letters · doi:10.1016/0304-3940(90)90865-7 · Cited by 158
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
Thomson, A. M., & West, D. C. (1993) · Neuroscience · doi:10.1016/0306-4522(93)90256-f · Cited by 155
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
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
Wilent, W. B., & Contreras, D. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.5782-03.2004 · Cited by 138
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
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
Khatri, V., Hartings, J. A., & Simons, D. J. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00257.2004 · Cited by 124
Perkins, K. L., & Wong, R. K. S. (1995) · Journal of Neurophysiology · doi:10.1152/jn.1995.73.2.911 · Cited by 115
Hellweg, F.-C., Schultz, W., & Creutzfeldt, O. D. (1977) · Journal of Neurophysiology · doi:10.1152/jn.1977.40.3.463 · Cited by 112
Beierlein, M., Fall, C. P., Rinzel, J., & Yuste, R. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-22-09885.2002 · Cited by 106
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
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
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
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
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
White, E. L., & Rock, M. P. (1981) · Journal of Comparative Neurology · doi:10.1002/cne.901950207 · Cited by 80
Spectral motion produces an auditory after-effect
Shu, Z., Swindale, N. V., & Cynader, M. (1993) · Nature · doi:10.1038/364721a0 · Cited by 72
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
Self-citationPetersen, C. C. H. (2002) · Journal of Neurophysiology · doi:10.1152/jn.2002.87.6.2904 · Cited by 51
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 49
Axmacher, N., & Miles, R. (2004) · The Journal of Physiology · doi:10.1113/jphysiol.2003.052225 · Cited by 47
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
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
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
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Halassa, M. M., & Haydon, P. G. (2010) · Annual Review of Physiology · doi:10.1146/annurev-physiol-021909-135843 · Cited by 763
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Metadata
- 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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