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The Journal of Neuroscience, January 25, 2006, 26(4):1219-1230; doi:10.1523/JNEUROSCI.4727-04.2006
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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
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