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The Journal of Neuroscience, April 15, 2001, 21(8):2699-2710
Diverse Types of Interneurons Generate Thalamus-Evoked
Feedforward Inhibition in the Mouse Barrel Cortex
James T.
Porter1,
Cary
K.
Johnson1, and
Ariel
Agmon1, 2
Department of 1 Neurobiology and Anatomy and
2 the Sensory Neuroscience Research Center, West Virginia
University, Morgantown, West Virginia 26506-9128
Sensory information, relayed through the thalamus, arrives in the
neocortex as excitatory input, but rapidly induces strong disynaptic
inhibition that constrains the cortical flow of excitation both
spatially and temporally. This feedforward inhibition is generated by
intracortical interneurons whose precise identity and properties were
not known. To characterize interneurons generating feedforward
inhibition, neurons in layers IV and V of mouse somatosensory ("barrel") cortex in vitro were tested in the
cell-attached configuration for thalamocortically induced firing and in
the whole-cell mode for synaptic responses. Identification as
inhibitory or excitatory neurons was based on intrinsic firing patterns
and on morphology revealed by intracellular staining. Thalamocortical
stimulation evoked action potentials in ~60% of inhibitory
interneurons but in <5% of excitatory neurons. The inhibitory
interneurons that fired received fivefold larger thalamocortical inputs
compared with nonfiring inhibitory or excitatory neurons.
Thalamocortically evoked spikes in inhibitory interneurons followed at
short latency the onset of excitatory monosynaptic responses in the
same cells and slightly preceded the onset of inhibitory responses in
nearby neurons, indicating their involvement in disynaptic inhibition. Both nonadapting (fast-spiking) and adapting (regular-spiking) inhibitory interneurons fired on thalamocortical stimulation, as did
interneurons expressing parvalbumin, calbindin, or neither calcium-binding protein. Morphological analysis revealed that some
interneurons might generate feedforward inhibition within their own
layer IV barrel, whereas others may convey inhibition to upper layers,
within their own or in adjacent columns. We conclude that feedforward
inhibition is generated by diverse classes of interneurons, possibly
serving different roles in the processing of incoming sensory information.
Key words:
feedforward inhibition; thalamocortical; somatosensory
cortex; barrel cortex; mice; parvalbumin; calbindin; FS cells; RSNP
cells; spiny stellate cells; GABAergic interneurons
Copyright © 2001 Society for Neuroscience 0270-6474/01/2182699-12$05.00/0
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|
|
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|
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|
|
|
|
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|
|
|
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|
|
|
|
|
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|
|
|
|
|
|
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|
|
|
|
|
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|
|
|
|
|
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|
|
|
|
|
|
|
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94(3):
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[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
V. C. Kotak, S. Fujisawa, F. A. Lee, O. Karthikeyan, C. Aoki, and D. H. Sanes
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[Full Text]
[PDF]
|
|
|
|
|
|
|
R. D. Traub, D. Contreras, M. O. Cunningham, H. Murray, F. E. N. LeBeau, A. Roopun, A. Bibbig, W. B. Wilent, M. J. Higley, and M. A. Whittington
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93(4):
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[Full Text]
[PDF]
|
|
|
|
|
|
|
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3423 - 3431.
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[Full Text]
[PDF]
|
|
|
|
|
|
|
J. Watts and A. M. Thomson
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562(1):
89 - 97.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
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92(6):
3511 - 3521.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. T. Porter and D. Nieves
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92(5):
2762 - 2770.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
E. E. Kwegyir-Afful and A. Keller
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J Neurophysiol,
October 1, 2004;
92(4):
2083 - 2092.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Zhang and K. D. Alloway
Stimulus-Induced Intercolumnar Synchronization of Neuronal Activity in Rat Barrel Cortex: A Laminar Analysis
J Neurophysiol,
September 1, 2004;
92(3):
1464 - 1478.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Y. Zhu, R. L. Stornetta, and J. J. Zhu
Chandelier Cells Control Excessive Cortical Excitation: Characteristics of Whisker-Evoked Synaptic Responses of Layer 2/3 Nonpyramidal and Pyramidal Neurons
J. Neurosci.,
June 2, 2004;
24(22):
5101 - 5108.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. Wirth and H.-R. Luscher
Spatiotemporal Evolution of Excitation and Inhibition in the Rat Barrel Cortex Investigated With Multielectrode Arrays
J Neurophysiol,
April 1, 2004;
91(4):
1635 - 1647.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. F. Casanova, D. Buxhoeveden, and J. Gomez
Disruption in the Inhibitory Architecture of the Cell Minicolumn: Implications for Autisim
Neuroscientist,
December 1, 2003;
9(6):
496 - 507.
[Abstract]
[PDF]
|
|
|
|
|
|
|
M. Beierlein, J. R. Gibson, and B. W. Connors
Two Dynamically Distinct Inhibitory Networks in Layer 4 of the Neocortex
J Neurophysiol,
November 1, 2003;
90(5):
2987 - 3000.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Butovas and C. Schwarz
Spatiotemporal Effects of Microstimulation in Rat Neocortex: A Parametric Study Using Multielectrode Recordings
J Neurophysiol,
November 1, 2003;
90(5):
3024 - 3039.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. M. Bruno, V. Khatri, P. W. Land, and D. J. Simons
Thalamocortical Angular Tuning Domains within Individual Barrels of Rat Somatosensory Cortex
J. Neurosci.,
October 22, 2003;
23(29):
9565 - 9574.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Nomura, T. Fukai, and T. Aoyagi
Synchrony of Fast-Spiking Interneurons Interconnected by GABAergic and Electrical Synapses
Neural Comput.,
September 1, 2003;
15(9):
2179 - 2198.
[Abstract]
[Full Text]
|
|
|
|
|
|
|
D. Schubert, R. Kotter, K. Zilles, H. J. Luhmann, and J. F. Staiger
Cell Type-Specific Circuits of Cortical Layer IV Spiny Neurons
J. Neurosci.,
April 1, 2003;
23(7):
2961 - 2970.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. A. Swadlow
Fast-spike Interneurons and Feedforward Inhibition in Awake Sensory Neocortex
Cereb Cortex,
January 1, 2003;
13(1):
25 - 32.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
K. D. Miller
Understanding Layer 4 of the Cortical Circuit: A Model Based on Cat V1
Cereb Cortex,
January 1, 2003;
13(1):
73 - 82.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. M. Bruno and D. J. Simons
Feedforward Mechanisms of Excitatory and Inhibitory Cortical Receptive Fields
J. Neurosci.,
December 15, 2002;
22(24):
10966 - 10975.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Beierlein, C. P. Fall, J. Rinzel, and R. Yuste
Thalamocortical Bursts Trigger Recurrent Activity in Neocortical Networks: Layer 4 as a Frequency-Dependent Gate
J. Neurosci.,
November 15, 2002;
22(22):
9885 - 9894.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Beierlein and B. W. Connors
Short-Term Dynamics of Thalamocortical and Intracortical Synapses Onto Layer 6 Neurons in Neocortex
J Neurophysiol,
October 1, 2002;
88(4):
1924 - 1932.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. F. Casanova, D. P. Buxhoeveden, and C. Brown
Clinical and Macroscopic Correlates of Minicolumnar Pathology in Autism
J Child Neurol,
September 1, 2002;
17(9):
692 - 695.
[Abstract]
[PDF]
|
|
|
|
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