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The Journal of Neuroscience, March 29, 2006, 26(13):3434-3443; doi:10.1523/JNEUROSCI.4076-05.2006

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Cellular/Molecular
Gap Junctions among Dendrites of Cortical GABAergic Neurons Establish a Dense and Widespread Intercolumnar Network

Takaichi Fukuda,^1,2 Toshio Kosaka,¹ Wolf Singer,² and Ralf A. W. Galuske^2,3

¹Department of Anatomy and Neurobiology, Graduate School of Medical Sciences, Kyushu University, Fukuoka 812-8582, Japan, ²Department of Neurophysiology, Max Planck Institute for Brain Research, 60528 Frankfurt am Main, Germany, and ³Department of Biology, Technical University Darmstadt, 64283 Darmstadt, Germany

Correspondence should be addressed to Takaichi Fukuda, Department of Anatomy and Neurobiology, Graduate School of Medical Sciences, Kyushu University, Maidashi 3-1-1, Higashiku, Fukuoka 812-8582, Japan. Email: fukuda{at}a3rd.med.kyushu-u.ac.jp

Gap junctions are common between cortical GABAergic interneurons but little is known about their quantitative distribution along dendritic profiles. Here, we provide direct morphological evidence that parvalbumin-containing GABAergic neurons in layer 2/3 of the cat visual cortex form dense and far-ranging networks through dendritic gap junctions. Gap junction-coupled networks of parvalbumin neurons were visualized using connexin36 immunohistochemistry and confocal laser-scanning microscopy (CLSM). The direct correspondence of connexin36-immunopositve puncta and gap junctions was confirmed by examining the same structures in both CLSM and electron microscopy. Single parvalbumin neurons with large somata (200 µm²) formed 60.3 ± 12.2 (mean ± SD) gap junctions with other cells whereby these contacts were not restricted to proximal dendrites but occurred at distances of up to 380 µm from the soma. In a Sholl analysis of large-type parvalbumin neurons, 21.9 ± 7.9 gap junctions were within 50 µm of the soma, 21.7 ± 7.6 gap junctions in a segment between 50 and 100 µm, 11.2 ± 4.7 junctions between 100 and 150 µm, and 5.6 ± 3.6 junctions were in more distal segments. Serially interconnected neurons could be traced laterally in a boundless manner through multiple gap junctions. Comparison to the orientation-preference columns revealed that parvalbumin-immunoreactive cells distribute randomly whereby their large dendritic fields overlap considerably and cover different orientation columns. It is proposed that this dense and homogeneous electrical coupling of interneurons supports the precise synchronization of neuronal populations with differing feature preferences thereby providing a temporal frame for the generation of distributed representations.

Key words: gap junction; connexin36; interneuron; parvalbumin; visual cortex; orientation column

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Received Sept. 26, 2005; revised Feb. 13, 2006; accepted Feb. 14, 2006.

Correspondence should be addressed to Takaichi Fukuda, Department of Anatomy and Neurobiology, Graduate School of Medical Sciences, Kyushu University, Maidashi 3-1-1, Higashiku, Fukuoka 812-8582, Japan. Email: fukuda{at}a3rd.med.kyushu-u.ac.jp

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