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Postsynaptic Mechanisms Govern the Differential Excitation of Cortical Neurons by Thalamic Inputs
Open accessAbstract
Thalamocortical (TC) afferents relay sensory input to the cortex by making synapses onto both excitatory regular-spiking principal cells (RS cells) and inhibitory fast-spiking interneurons (FS cells). This divergence plays a crucial role in coordinating excitation with inhibition during the earliest steps of somatosensory processing in the cortex. Although the same TC afferents contact both FS and RS cells, FS cells receive larger and faster excitatory inputs from individual TC afferents. Here, we show that this larger thalamic excitation of FS cells occurs via GluR2-lacking AMPA receptors (AMPARs), and results from a fourfold larger quantal amplitude compared with the thalamic inputs onto RS cells. Thalamic afferents also activate NMDA receptors (NMDARs) at synapses onto both cells types, yet RS cell NMDAR currents are slower and pass more current at physiological membrane potentials. Because of these synaptic specializations, GluR2-lacking AMPARs selectively maintain feedforward inhibition of RS cells, whereas NMDARs contribute to the spiking of RS cells and hence to cortical recurrent excitation. Thus, thalamic afferent activity diverges into two routes that rely on unique complements of postsynaptic AMPARs and NMDARs to orchestrate the dynamic balance of excitation and inhibition as sensory input enters the cortex.
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“provided by high quantal amplitude with calcium permeable AMPA receptors (Hull et al., 2009) and multiple synaptic contacts forming clusters of neurotransmitter release sites (Bagnall et al., 2011).”
From GABAergic Interneurons in the Neocortex: From Cellular Properties to Circuits (2016) · cites this paper as Hull et al., 2009
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Citations
Cites
Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex
McCormick, D. A., Connors, B. W., Lighthall, J. W., & Prince, D. A. (1985) · Journal of Neurophysiology · doi:10.1152/jn.1985.54.4.782 · Cited by 1,935
Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex
Wehr, M., & Zador, A. M. (2003) · Nature · doi:10.1038/nature02116 · Cited by 1,405
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
Geiger, J. R. P., Melcher, T., Koh, D.-S., Sakmann, B., Seeburg, P. H., Jonas, P., & Monyer, H. (1995) · Neuron · doi:10.1016/0896-6273(95)90076-4 · Cited by 1,260
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
Functional organization of thalamocortical relays
Sherman, S. M., & Guillery, R. W. (1996) · Journal of Neurophysiology · doi:10.1152/jn.1996.76.3.1367 · Cited by 762
Cortex is driven by weak but synchronously active thalamocortical synapses
Bruno, R. M., & Sakmann, B. (2006) · Science · doi:10.1126/science.1124593 · Cited by 714
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
Somatosensory integration controlled by dynamic thalamocortical feed-forward inhibition
Gabernet, L., Jadhav, S. P., Feldman, D. E., Carandini, M., & Scanziani, M. (2005) · Neuron · doi:10.1016/j.neuron.2005.09.022 · Cited by 599
Self-citationTwo 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
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
Two components of transmitter release at a central synapse.
Goda, Y., & Stevens, C. F. (1994) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.91.26.12942 · Cited by 529
Swanson, G. T., Kamboj, S. K., & Cull-Candy, S. G. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-01-00058.1997 · Cited by 489
Synaptic activity at calcium-permeable AMPA receptors induces a switch in receptor subtype
Liu, S. J., & Cull-Candy, S. G. (2000) · Nature · doi:10.1038/35013064 · Cited by 452
Feldmeyer, D., Egger, V., Lübke, J., & Sakmann, B. (1999) · The Journal of Physiology · doi:10.1111/j.1469-7793.1999.00169.x · Cited by 441
Submillisecond AMPA receptor-mediated signaling at a principal neuron-interneuron synapse
Geiger, J. R. P., Lübke, J., Roth, A., Frotscher, M., & Jonas, P. (1997) · Neuron · doi:10.1016/s0896-6273(00)80339-6 · Cited by 407
Wang, Y. (2002) · Cerebral Cortex · doi:10.1093/cercor/12.4.395 · Cited by 382
Efficacy of Thalamocortical and Intracortical Synaptic Connections
Gil, Z., Connors, B. W., & Amitai, Y. (1999) · Neuron · doi:10.1016/s0896-6273(00)80788-6 · Cited by 357
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
Bochet, P., Audinat, É., Lambolez, B., Crépel, F., Rossier, J., Iino, M., Tsuzuki, K., & Ozawa, S. (1994) · Neuron · doi:10.1016/0896-6273(94)90279-8 · Cited by 353
Porter, J. T., Johnson, C. K., & Agmon, A. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-08-02699.2001 · Cited by 344
Polyneuronal innervation of spiny stellate neurons in cat visual cortex
Ahmed, B., Anderson, J. C., Douglas, R. J., Martin, K. A. C., & Nelson, J. C. (1994) · The Journal of Comparative Neurology · doi:10.1002/cne.903410105 · Cited by 338
Dynamics of excitation and inhibition underlying stimulus selectivity in rat somatosensory cortex
Wilent, W. B., & Contreras, D. (2005) · Nature Neuroscience · doi:10.1038/nn1545 · Cited by 288 · cited 2×
“The divergence of TC fibers onto interneurons and principal cells forms the basis of a disynaptic feedforward inhibitory circuit that is critical in coordinating excitation with inhibition during the initial phases of cortical sensory processing (Agmon and Connors, 1991; Swadlow and Gusev, 2000; Wehr and Zador, 2003;…”
BackgroundSilver, R., Momiyama, A., & Cull-Candy, S. (1998) · Journal of Physiology · doi:10.1111/j.1469-7793.1998.881bj.x · Cited by 279
Balanced Excitation and Inhibition Determine Spike Timing during Frequency Adaptation
Higley, M. J., & Contreras, D. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.3506-05.2006 · Cited by 270
Anti-Hebbian Long-Term Potentiation in the Hippocampal Feedback Inhibitory Circuit
Lamsa, K. P., Heeroma, J. H., Somogyi, P., Rusakov, D. A., & Kullmann, D. M. (2007) · Science · doi:10.1126/science.1137450 · Cited by 261
Population Coding of Stimulus Location in Rat Somatosensory Cortex
Petersen, R. S., Panzeri, S., & Diamond, M. E. (2001) · Neuron · doi:10.1016/s0896-6273(01)00481-0 · Cited by 253
Sun, Q., Huguenard, J. R., & Prince, D. A. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.4727-04.2006 · Cited by 242
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
Multiple Structural Elements Determine Subunit Specificity of Mg2+Block in NMDA Receptor Channels
Kuner, T., & Schoepfer, R. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-11-03549.1996 · Cited by 235
Ca(2+)‐permeable AMPA and NMDA receptor channels in basket cells of rat hippocampal dentate gyrus.
Koh, D., Geiger, J. R. P., Jónás, P., & Sakmann, B. J. (1995) · The Journal of Physiology · doi:10.1113/jphysiol.1995.sp020737 · Cited by 227
Unveiling synaptic plasticity: a new graphical and analytical approach
Clements, J. D., & Silver, R. A. (2000) · Trends in Neurosciences · doi:10.1016/s0166-2236(99)01520-9 · Cited by 224
McBain, C. J., & Dingledine, R. (1993) · The Journal of Physiology · doi:10.1113/jphysiol.1993.sp019560 · Cited by 221
Visual responses in adult cat visual cortex depend on N-methyl-D-aspartate receptors.
Miller, K. D., Chapman, B., & Stryker, M. P. (1989) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.86.13.5183 · Cited by 181
Spatial gradients and inhibitory summation in the rat whisker barrel system
Brumberg, J. C., Pinto, D. J., & Simons, D. J. (1996) · Journal of Neurophysiology · doi:10.1152/jn.1996.76.1.130 · Cited by 176
Morphology of Golgi‐Cox‐impregnated barrel neurons in rat SmI cortex
Simons, D. J., & Woolsey, T. A. (1984) · Journal of Comparative Neurology · doi:10.1002/cne.902300111 · Cited by 175
Armstrong‐James, M., Welker, E., & Callahan, C. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-05-02149.1993 · Cited by 171
Silver, R. A. (2003) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2003.09.030 · Cited by 168
Short-Term Dynamics of Thalamocortical and Intracortical Synapses Onto Layer 6 Neurons in Neocortex
Beierlein, M., & Connors, B. W. (2002) · Journal of Neurophysiology · doi:10.1152/jn.2002.88.4.1924 · Cited by 152
Receptive-field construction in cortical inhibitory interneurons
Swadlow, H. A., & Gusev, A. G. (2002) · Nature Neuroscience · doi:10.1038/nn847 · Cited by 148
Wilent, W. B., & Contreras, D. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.5782-03.2004 · Cited by 138
Angulo, M. C., Rossier, J., & Audinat, É. (1999) · Journal of Neurophysiology · doi:10.1152/jn.1999.82.3.1295 · Cited by 131
White, E. L., & Rock, M. P. (1980) · Journal of Neurocytology · doi:10.1007/bf01205029 · Cited by 127
Fleidervish, I. A., Binshtok, A. M., & Gutnick, M. J. (1998) · Neuron · doi:10.1016/s0896-6273(00)80623-6 · Cited by 121
Zhang, Z.-W., & Deschênes, M. (1998) · Cerebral Cortex · doi:10.1093/cercor/8.5.428 · Cited by 112
Ferster, D., & Lindström, S. (1985) · The Journal of Physiology · doi:10.1113/jphysiol.1985.sp015821 · Cited by 109
NMDA Receptors in Layer 4 Spiny Stellate Cells of the Mouse Barrel Cortex Contain the NR2C Subunit
Binshtok, A. M., Fleidervish, I. A., Sprengel, R., & Gutnick, M. J. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.4409-05.2006 · 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
Computer‐assisted analyses of barrel neuron axons and their putative synaptic contacts
Harris, R. M., & Woolsey, T. A. (1983) · The Journal of Comparative Neurology · doi:10.1002/cne.902200107 · Cited by 78
OFF response transformations in the whisker/barrel system
Kyriazi, H. T., Carvell, G. E., & Simons, D. J. (1994) · Journal of Neurophysiology · doi:10.1152/jn.1994.72.1.392 · Cited by 77
Clements, J. D. (2003) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2003.09.019 · Cited by 72
Inoue, T., & Imoto, K. (2006) · Journal of Neurophysiology · doi:10.1152/jn.00301.2006 · Cited by 67
Adult thalamocortical transmission involves both NMDA and non-NMDA receptors
Gil, Z., & Amitai, Y. (1996) · Journal of Neurophysiology · doi:10.1152/jn.1996.76.4.2547 · Cited by 60
Recruitment of GABAA inhibition in rat neocortex is limited and not NMDA dependent
Ling, D. S. F., & Benardo, L. S. (1995) · Journal of Neurophysiology · doi:10.1152/jn.1995.74.6.2329 · Cited by 54
Kasamatsu, T., Imamura, K., Mataga, N., Hartveit, E., Heggelund, U., & Heggelund, P. (1997) · Neuroscience · doi:10.1016/s0306-4522(97)00222-4 · Cited by 30
Dingledine, R., & McBain, C. J. (2021) · Carolina Digital Repository (University of North Carolina at Chapel Hill) · doi:10.17615/0ctd-e358 · Cited by 7
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Metadata
- Authors
- Hull, C., Isaacson, J. S., & Scanziani, M.
- Affiliations
- University of California San Diego (US)
- Corresponding author
- Scanziani, M.
- Venue
- Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2009-07-15
- Volume
- 29
- Issue
- 28
- Pages
- 9127-9136
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC2753516
- OpenAlex
- W2046924947
- Cited by
- 147
- References
- 56
- Citations by year
- 2026: 1 · 2025: 3 · 2024: 2 · 2023: 3 · 2022: 5 · 2021: 4 · 2020: 6 · 2019: 6 · 2018: 11 · 2017: 16 · 2016: 10 · 2015: 10 · 2014: 13 · 2013: 14 · 2012: 12
- FWCI
- 5.96
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Neuroscience (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (NH70058)
- National Institute of Mental Health (R01MH070058)
- National Institute of Neurological Disorders and Stroke (F32NS060585)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- thalamocortical afferents, postsynaptic mechanisms, fast-spiking interneurons, NMDA receptor, feedforward inhibition, excitation-inhibition balance, somatosensory processing, synaptic specializations
- MeSH terms
- Animals, Animals, Newborn, Biophysics, Calcium, Drug Interactions, Electric Stimulation, Mice, Inbred ICR, Neural Inhibition, Neural Pathways, Neurons, Pyridazines, Somatosensory Cortex, Strontium, Synapses, Thalamus, Time Factors, Receptors, N-Methyl-D-Aspartate, Patch-Clamp Techniques, Excitatory Amino Acid Antagonists, GABA Antagonists, Excitatory Postsynaptic Potentials, Principal Component Analysis, Mice, Inhibitory Postsynaptic Potentials, In Vitro Techniques
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