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The Journal of Neuroscience, May 10, 2006, 26(19):5069-5082; doi:10.1523/JNEUROSCI.0661-06.2006
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Behavioral/Systems/Cognitive
Distinct Subtypes of Somatostatin-Containing Neocortical Interneurons Revealed in Transgenic Mice
Yunyong Ma,1,5 Hang Hu,1,5 Albert S. Berrebi,1,2,5 Peter H. Mathers,2,3,4,5 andAriel Agmon1,5 Departments of 1Neurobiology and Anatomy, 2Otolaryngology, 3Biochemistry and 4Ophthalmology, and the 5Sensory Neuroscience Research Center, West Virginia University, Morgantown, West Virginia 26506
Correspondence should be addressed to Ariel Agmon, Department of Neurobiology and Anatomy, P.O. Box 9128, West Virginia University Health Science Center, Morgantown, WV 26506-9128. Email: aric.agmon{at}gmail.com
GABA-releasing inhibitory interneurons in the cerebral cortex can be classified by their neurochemical content, firing patterns, or axonal targets, to name the most common criteria, but whether classifications using different criteria converge on the same neuronal subtypes, and how many such subtypes exist, is a matter of much current interest and considerable debate. To address these issues, we generated transgenic mice expressing green fluorescent protein (GFP) under control of the GAD67 promoter. In two of these lines, named X94 and X98, GFP expression in the barrel cortex was restricted to subsets of somatostatin-containing (SOM+) GABAergic interneurons, similar to the previously reported "GIN" line (Oliva et al., 2000), but the laminar distributions of GFP-expressing (GFP+) cell bodies in the X94, X98, and GIN lines were distinct and nearly complementary. We compared neurochemical content and axonal distribution patterns of GFP+ neurons among the three lines and analyzed in detail electrophysiological properties in a dataset of 150 neurons recorded in whole-cell, current-clamp mode. By all criteria, there was nearly perfect segregation of X94 and X98 GFP+ neurons, whereas GIN GFP+ neurons exhibited intermediate properties. In the X98 line, GFP expression was found in infragranular, calbindin-containing, layer 1-targeting ("Martinotti") cells that had a propensity to fire low-threshold calcium spikes, whereas X94 GFP+ cells were stuttering interneurons with quasi fast-spiking properties, residing in and targeting the thalamo-recipient neocortical layers. We conclude that much of the variability previously attributed to neocortical SOM+ interneurons can be accounted for by their natural grouping into distinct subtypes.
Key words: neocortex; GABAergic; somatostatin; transgenic mice; inhibitory interneuron; barrel cortex
Received July 25, 2005; revised April 3, 2006; accepted April 4, 2006.
Correspondence should be addressed to Ariel Agmon, Department of Neurobiology and Anatomy, P.O. Box 9128, West Virginia University Health Science Center, Morgantown, WV 26506-9128. Email: aric.agmon{at}gmail.com
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