 |
|||||
|
|||||
|
|||||
|
|||||
|
|||||
The Journal of Neuroscience, January 25, 2006, 26(4):1219-1230; doi:10.1523/JNEUROSCI.4727-04.2006
Previous Article | Next Article
Behavioral/Systems/Cognitive
Barrel Cortex Microcircuits: Thalamocortical Feedforward Inhibition in Spiny Stellate Cells Is Mediated by a Small Number of Fast-Spiking Interneurons
Qian-Quan Sun, John R. Huguenard, andDavid A. Prince Department of Neurology and Neurological Sciences, Stanford School of Medicine, Stanford, California 94305
Correspondence should be addressed to Dr. David A. Prince, Department of Neurology and Neurological Sciences, Stanford University School of Medicine, Stanford, CA 94305. Email: daprince{at}stanford.edu
Inhibitory and excitatory neurons located in rodent barrel cortex are known to form functional circuits mediating vibrissal sensation. Excitatory neurons located in a single barrel greatly outnumber interneurons, and form extensive reciprocal excitatory synaptic contacts. Inhibitory and excitatory networks must interact to shape information ascending to cortex. The details of these interactions, however, have not been completely explored. Using paired intracellular recordings, we studied the properties of synaptic connections between spiny neurons (i.e., spiny stellate and pyramidal cells) and interneurons, as well as integration of thalamocortical (TC) input, in layer IV barrels of rat thalamocortical slices. Results show the following: (1) the strength of unitary excitatory connections of spiny neurons is similar among different targets; (2) although inhibition from regular-spiking nonpyramidal interneurons to spiny neurons is comparable in strength to excitatory connections, inhibition mediated by fast-spiking (FS) interneurons is 10 times more powerful; (3) TC EPSPs elicit reliable and precisely timed action potentials in FS neurons; and (4) a small number of FS neurons mediate thalamocortical feedforward inhibition in each spiny neuron and can powerfully shunt TC-mediated excitation. The ready activation of FS cells by TC inputs, coupled with powerful feedforward inhibition from these neurons, would profoundly influence sensory processing and constrain runaway excitation in vivo.
Key words: somatosensory cortex; fast-spiking interneuron; IPSPs; spiny stellate neuron; thalamocortical; feedforward inhibition
Received Feb. 27, 2004; revised Nov. 21, 2005; accepted Nov. 22, 2005.
Correspondence should be addressed to Dr. David A. Prince, Department of Neurology and Neurological Sciences, Stanford University School of Medicine, Stanford, CA 94305. Email: daprince{at}stanford.edu
This article has been cited by other articles:
Q.-Q. Sun
Experience-Dependent Intrinsic Plasticity in Interneurons of Barrel Cortex Layer IV
J Neurophysiol, November 1, 2009; 102(5): 2955 - 2973.
[Abstract] [Full Text] [PDF]
F.-W. Zhou, H.-X. Chen, and S. N. Roper
Balance of Inhibitory and Excitatory Synaptic Activity Is Altered in Fast-Spiking Interneurons in Experimental Cortical Dysplasia
J Neurophysiol, October 1, 2009; 102(4): 2514 - 2525.
[Abstract] [Full Text] [PDF]
A.-M. M. Oswald, B. Doiron, J. Rinzel, and A. D. Reyes
Spatial Profile and Differential Recruitment of GABAB Modulate Oscillatory Activity in Auditory Cortex
J. Neurosci., August 19, 2009; 29(33): 10321 - 10334.
[Abstract] [Full Text] [PDF]
C. Hull, J. S. Isaacson, and M. Scanziani
Postsynaptic Mechanisms Govern the Differential Excitation of Cortical Neurons by Thalamic Inputs
J. Neurosci., July 15, 2009; 29(28): 9127 - 9136.
[Abstract] [Full Text] [PDF]
Q.-Q. Sun, Z. Zhang, Y. Jiao, C. Zhang, G. Szabo, and F. Erdelyi
Differential Metabotropic Glutamate Receptor Expression and Modulation in Two Neocortical Inhibitory Networks
J Neurophysiol, May 1, 2009; 101(5): 2679 - 2692.
[Abstract] [Full Text] [PDF]
J. E. Heiss, Y. Katz, E. Ganmor, and I. Lampl
Shift in the Balance between Excitation and Inhibition during Sensory Adaptation of S1 Neurons
J. Neurosci., December 3, 2008; 28(49): 13320 - 13330.
[Abstract] [Full Text] [PDF]
J. R. Gibson, A. F. Bartley, S. A. Hays, and K. M. Huber
Imbalance of Neocortical Excitation and Inhibition and Altered UP States Reflect Network Hyperexcitability in the Mouse Model of Fragile X Syndrome
J Neurophysiol, November 1, 2008; 100(5): 2615 - 2626.
[Abstract] [Full Text] [PDF]
J. de la Rocha, C. Marchetti, M. Schiff, and A. D. Reyes
Linking the Response Properties of Cells in Auditory Cortex with Network Architecture: Cotuning versus Lateral Inhibition
J. Neurosci., September 10, 2008; 28(37): 9151 - 9163.
[Abstract] [Full Text] [PDF]
E. I. Krook-Magnuson, P. Li, S. M. Paluszkiewicz, and M. M. Huntsman
Tonically Active Inhibition Selectively Controls Feedforward Circuits in Mouse Barrel Cortex
J Neurophysiol, August 1, 2008; 100(2): 932 - 944.
[Abstract] [Full Text] [PDF]
A. Hirata and M. A. Castro-Alamancos
Cortical Transformation of Wide-Field (Multiwhisker) Sensory Responses
J Neurophysiol, July 1, 2008; 100(1): 358 - 370.
[Abstract] [Full Text] [PDF]
V. Egger, T. Nevian, and R. M. Bruno
Subcolumnar Dendritic and Axonal Organization of Spiny Stellate and Star Pyramid Neurons within a Barrel in Rat Somatosensory Cortex
Cereb Cortex, April 1, 2008; 18(4): 876 - 889.
[Abstract] [Full Text] [PDF]
Z. Tan, H. Hu, Z. J. Huang, and A. Agmon
Robust but delayed thalamocortical activation of dendritic-targeting inhibitory interneurons
PNAS, February 12, 2008; 105(6): 2187 - 2192.
[Abstract] [Full Text] [PDF]
M. Derchansky, S. S. Jahromi, M. Mamani, D. S. Shin, A. Sik, and P. L. Carlen
Transition to seizures in the isolated immature mouse hippocampus: a switch from dominant phasic inhibition to dominant phasic excitation
J. Physiol., January 15, 2008; 586(2): 477 - 494.
[Abstract] [Full Text] [PDF]
Y. Ben-Ari, J.-L. Gaiarsa, R. Tyzio, and R. Khazipov
GABA: A Pioneer Transmitter That Excites Immature Neurons and Generates Primitive Oscillations
Physiol Rev, October 1, 2007; 87(4): 1215 - 1284.
[Abstract] [Full Text] [PDF]
P. Rigas and M. A. Castro-Alamancos
Thalamocortical Up States: Differential Effects of Intrinsic and Extrinsic Cortical Inputs on Persistent Activity
J. Neurosci., April 18, 2007; 27(16): 4261 - 4272.
[Abstract] [Full Text] [PDF]
C. Quairiaux, M. Armstrong-James, and E. Welker
Modified Sensory Processing in the Barrel Cortex of the Adult Mouse After Chronic Whisker Stimulation
J Neurophysiol, March 1, 2007; 97(3): 2130 - 2147.
[Abstract] [Full Text] [PDF]
M. Minlebaev, Y. Ben-Ari, and R. Khazipov
Network Mechanisms of Spindle-Burst Oscillations in the Neonatal Rat Barrel Cortex In Vivo
J Neurophysiol, January 1, 2007; 97(1): 692 - 700.
[Abstract] [Full Text] [PDF]
P. Y. Chang and M. B. Jackson
Heterogeneous spatial patterns of long-term potentiation in rat hippocampal slices
J. Physiol., October 15, 2006; 576(2): 427 - 443.
[Abstract] [Full Text] [PDF]
K. M. Rodgers, A. M. Benison, and D. S. Barth
Two-Dimensional Coincidence Detection in the Vibrissa/Barrel Field
J Neurophysiol, October 1, 2006; 96(4): 1981 - 1990.
[Abstract] [Full Text] [PDF]
T. Inoue and K. Imoto
Feedforward Inhibitory Connections From Multiple Thalamic Cells to Multiple Regular-Spiking Cells in Layer 4 of the Somatosensory Cortex
J Neurophysiol, October 1, 2006; 96(4): 1746 - 1754.
[Abstract] [Full Text] [PDF]
Y. Jiao, C. Zhang, Y. Yanagawa, and Q.-Q. Sun
Major Effects of Sensory Experiences on the Neocortical Inhibitory Circuits.
J. Neurosci., August 23, 2006; 26(34): 8691 - 8701.
[Abstract] [Full Text] [PDF]
|
|
|
|
 |
|