Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2004 Jun 2;24(22):5101-8.
doi: 10.1523/JNEUROSCI.0544-04.2004.

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, J Julius Zhu
Affiliations

Chandelier cells control excessive cortical excitation: characteristics of whisker-evoked synaptic responses of layer 2/3 nonpyramidal and pyramidal neurons

Yinghua Zhu et al. J Neurosci. .

Abstract

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.

PubMed Disclaimer

Figures

Figure 1.
Figure 1.
Whisker-evoked synaptic responses in chandelier cells and other FS nonpyramidal neurons. A, B, Neurolucida reconstruction of an FS chandelier cell (A) and an FS basket cell (B). Recording traces below show responses of the chandelier cell and basket cell to hyperpolarizing and depolarizing current step injections. Short lines on the left side in A and B indicate cortical layer boundaries. C, D, Primary whisker-evoked responses of the chandelier cell (C) and basket cell (D) at the resting membrane potentials (2 single trials). Note that the primary whiskers of the chandelier cell and basket cell were whiskers C2 and C1, respectively. E, F, Average responses of the chandelier cell and basket cell to a brief deflection of the primary whisker, a first-order surrounding whisker, and a second-order surrounding whisker. G, H, Average responses of the chandelier cell (G) and basket cell (H) to the simultaneous deflection of whiskers C1, C2, and C3. Note the early IPSPs (arrows) in E and G. I, J, Spontaneous events of the chandelier cell (I) and basket cell (J) recorded at slightly depolarized membrane potentials.
Figure 2.
Figure 2.
Receptive fields of whisker-evoked synaptic responses of chandelier cells and other FS nonpyramidal neurons. A, B, Amplitudes and latency of the initial EPSPs evoked by brief deflections of single whiskers from A0 to E5 in the chandelier cell (A) and basket cell (B) reconstructed in Figure 1.C, D, Amplitudes and latencies of the initial IPSPs evoked by brief deflections of single whiskers from A0 to E5 in the same chandelier cell (C) and basket cell (D).
Figure 3.
Figure 3.
Receptive fields of whisker-evoked synaptic responses of chandelier cells and other FS nonpyramidal neurons. A, Histograms of average amplitudes of the primary whisker-evoked initial EPSPs in chandelier cells (black bars) and other FS nonpyramidal neurons (gray bars). B, Histograms of average latencies of the whisker-evoked initial EPSPs of chandelier cells and other FS nonpyramidal neurons. C, Histograms of average latencies of the whisker-evoked initial IPSPs of chandelier cells and other FS nonpyramidal neurons. D, Histograms of average excitatory and inhibitory receptive field sizes (defined as the number of whiskers that evoked an initial EPSP or IPSP) for chandelier cells and other FS nonpyramidal neurons. Note that the excitatory and inhibitory receptive field sizes were the same within cell types, although they differed between cell types. E, Plots of average acuities of excitatory receptive fields of chandelier cells and other FS nonpyramidal neurons. F, Plots of average acuities of inhibitory receptive fields of chandelier cells and other FS nonpyramidal neurons. EPSP and IPSP amplitudes and SEs were normalized to average values from primary whiskers.
Figure 4.
Figure 4.
Whisker-evoked synaptic responses in FS nonpyramidal neurons. A–C, Neurolucida reconstruction of a double bouquet cell (A), a net basket cell (B), and a bitufted cell (C). Note that the cell in A has its dendritic and axonal branches vertically oriented, the cell in B exhibits a local net of dendritic and axonal branches on one side of the soma, and the cell in C gives rise to two primary dendrites emerging on opposite sides of the soma. Recording traces below show responses of the nonpyramidal cells to hyperpolarizing and depolarizing current step injections. Cortical layer boundaries indicated by short lines on the right side of C apply to A–C. D–F, Amplitudes and latencies of the initial EPSPs evoked by brief deflections of single whiskers from A0 to E5 in the double bouquet cell (D), net basket cell (E), and bitufted cell (F).
Figure 6.
Figure 6.
Spontaneous activity-evoked action potentials in simultaneously recorded chandelier cells and other cortical neurons. A, Neurolucida reconstruction of a chandelier cell (left) and a neurogliaform cell (right). Recording traces show the responses of the two neurons to hyperpolarizing and depolarizing current step injections. Short lines on the left side indicate cortical layer boundaries. B, Simultaneous recordings of spontaneous activity in the chandelier cell (left) and neurogliaform cell (right) in normal condition (top traces), with superperfusion of 2 μm bicuculline (middle traces), or after washout of bicuculline (bottom traces). C, Average spontaneous firing frequency in chandelier cells versus other FS nonpyramidal or RS pyramidal neurons before and after superperfusion of bicuculline. Note that •—• indicates chandelier cell and other FS nonpyramidal cell pairs, and ▪—▪ indicates chandelier cell and RS pyramidal cell pairs.
Figure 5.
Figure 5.
Whisker-evoked synaptic responses in RS pyramidal neurons. A, Neurolucida reconstruction of a layer 2/3 RS pyramidal neuron. Recording traces below show responses of the pyramidal cell to hyperpolarizing and depolarizing current step injections. Short lines on the left side indicate cortical layer boundaries. B, Average responses of the pyramidal neuron to a brief deflection of the primary whisker C0, a first-order surrounding whisker C1, and a second-order surrounding whisker C2. C, Amplitudes and latencies of the initial EPSPs evoked by brief deflections of single whiskers from A0 to E5 in the pyramidal neuron. D, Histograms of average amplitudes of the primary whisker-, first-order surrounding whisker-, and second-order surrounding whisker-evoked initial EPSPs in pyramidal neurons. E, Plots of average acuities of excitatory receptive fields of pyramidal neurons versus chandelier cells (left) and pyramidal neurons versus other FS nonpyramidal neurons (right). EPSP amplitudes and SEs were normalized to average values from primary whiskers.
See this image and copyright information in PMC

Similar articles

See all similar articles

Cited by

See all "Cited by" articles

References

    1. Agmon A, Connors BW (1992) Correlation between intrinsic firing patterns and thalamocortical synaptic responses of neurons in mouse barrel cortex. J Neurosci 12: 319–329. - PMC - PubMed
    1. Arellano JI, Munoz A, Ballesteros-Yanez I, Sola RG, DeFelipe J (2004) Histopathology and reorganization of chandelier cells in the human epileptic sclerotic hippocampus. Brain 127: 45–64. - PubMed
    1. Armstrong-James M, Fox K (1987) Spatiotemporal convergence and divergence in the rat S1 “barrel” cortex. J Comp Neurol 263: 265–281. - PubMed
    1. Beierlein M, Gibson JR, Connors BW (2000) A network of electrically coupled interneurons drives synchronized inhibition in neocortex. Nat Neurosci 3: 904–910. - PubMed
    1. Borg-Graham LJ, Monier C, Fregnac Y (1998) Visual input evokes transient and strong shunting inhibition in visual cortical neurons. Nature 393: 369–373. - PubMed

Publication types

MeSH terms

LinkOut - more resources

-