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The Journal of Neuroscience, June 2, 2004, 24(22):5101-5108; doi:10.1523/JNEUROSCI.0544-04.2004

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Behavioral/Systems/Cognitive
Chandelier Cells Control Excessive Cortical Excitation: Characteristics of Whisker-Evoked Synaptic Responses of Layer 2/3 Nonpyramidal and Pyramidal Neurons

Yinghua Zhu,¹ Ruth L. Stornetta,¹ and J. Julius Zhu^1,2,3

¹Department of Pharmacology, University of Virginia School of Medicine, Charlottesville, Virginia 22908, ²Cold Spring Harbor Laboratory, Cold Spring Harbor, New York 11724, and ³Max Planck Institute for Medical Research, Department of Cell Physiology, Heidelberg D-69120, Germany

Chandelier cells form inhibitory axo-axonic synapses on pyramidal neurons with their characteristic candlestick-like axonal terminals. The functional role of chandelier cells is still unclear, although the preferential loss of this cell type at epileptic loci suggests a role in epilepsy. Here we report an examination of whisker- and spontaneous activity-evoked responses in chandelier cells and other fast-spiking nonpyramidal neurons and regular-spiking pyramidal neurons in layer 2/3 of the barrel cortex. Fast-spiking nonpyramidal neurons, including chandelier cells, basket cells, neurogliaform cells, double bouquet cells, net basket cells, bitufted cells, and regular-spiking pyramidal neurons all respond to stimulation of multiple whiskers on the contralateral face. Whisker stimulation, however, evokes small, delayed EPSPs preceded by an earlier IPSP and no action potentials in chandelier cells, different from other nonpyramidal and pyramidal neurons. In addition, chandelier cells display a larger receptive field with lower acuity than other fast-spiking nonpyramidal neurons and pyramidal neurons. Notably, simultaneous dual whole-cell in vivo recordings show that chandelier cells, which rarely fire action potentials spontaneously, fire more robustly than other types of cortical neurons when the overall cortical excitation increases. Thus, chandelier cells may not process fast ascending sensory information but instead may be reserved to prevent excessive excitatory activity in neuronal networks.

Key words: rat; somatosensory; excitation; inhibition; whisker; epilepsy

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Received Feb 16, 2004; revised March 30, 2004; accepted April 21, 2004.

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