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Open Access Research

Columnar distribution of activity dependent gabaergic depolarization in sensorimotor cortical neurons

Jaekwang Lee13, Junsung Woo3, Oleg V Favorov1, Mark Tommerdahl1, C Justin Lee3* and Barry L Whitsel12*

Author Affiliations

1 Departments of Biomedical Engineering, University of North Carolina at Chapel Hill, CB#7575, Chapel Hill, NC, USA

2 Department of Cell and Molecular Physiology, University of North Carolina at Chapel Hill, CB#7575, Chapel Hill, NC, USA

3 WCI Center for Functional Connectomics, Institute of Science and Technology (KIST), Seoul, 136-791, Korea

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Molecular Brain 2012, 5:33  doi:10.1186/1756-6606-5-33

Published: 24 September 2012

Abstract

Background

GABA, the major inhibitory neurotransmitter in CNS, has been demonstrated to paradoxically produce excitation even in mature brain. However activity-dependent form of GABA excitation in cortical neurons has not been observed. Here we report that after an intense electrical stimulation adult cortical neurons displayed a transient GABA excitation that lasted for about 30s.

Results

Whole-cell patch recordings were performed to evaluate the effects of briefly applied GABA on pyramidal neurons in adult rodent sensorimotor cortical slice before and after 1 s, 20 Hz suprathreshold electrical stimulation of the junction between layer 6 and the underlying white matter (L6/WM stimulation). Immediately after L6/WM stimulation, GABA puffs produced neuronal depolarization in the center of the column-shaped region. However, both prior to or 30s after stimulation GABA puffs produced hyperpolarization of neurons. 2-photon imaging in neurons infected with adenovirus carrying a chloride sensor Clomeleon revealed that GABA induced depolarization is due to an increase in [Cl-]i after stimulation. To reveal the spatial extent of excitatory action of GABA, isoguvacine, a GABAA receptors agonist, was applied right after stimulation while monitoring the intracellular Ca2+ concentration in pyramidal neurons. Isoguvacine induced an increase in [Ca2+]i in pyramidal neurons especially in the center of the column but not in the peripheral regions of the column. The global pattern of the Ca2+ signal showed a column-shaped distribution along the stimulation site.

Conclusion

These results demonstrate that the well-known inhibitory transmitter GABA rapidly switches from hyperpolarization to depolarization upon synaptic activity in adult somatosensory cortical neurons.