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The Journal of Neuroscience, January 7, 2009, 29(1):70-85; doi:10.1523/JNEUROSCI.4104-08.2009

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Cellular/Molecular
Laminar Specificity of Functional Input to Distinct Types of Inhibitory Cortical Neurons

Xiangmin Xu^1,2 and Edward M. Callaway¹

¹Systems Neurobiology Laboratories, The Salk Institute for Biological Studies, La Jolla, California 92037, and ²Department of Anatomy and Neurobiology, School of Medicine, University of California, Irvine, Irvine, California 92697-1275

Correspondence should be addressed to Dr. Edward M. Callaway, Systems Neurobiology Laboratories, The Salk Institute for Biological Studies, 10010 North Torrey Pines Road, La Jolla, CA 92037. Email: callaway{at}salk.edu

Despite the presence of numerous inhibitory cell types, laminar excitatory input has only been characterized for limited identified types, and it is unknown whether there are differences between cell types in their laminar sources of inhibitory input. In the present study, we characterized sources of local input to nine distinct types of layer 2/3 inhibitory neurons in living slices of mouse somatosensory cortex. Whole-cell recordings from identified cell types, facilitated by use of transgenic mice expressing green fluorescent protein in limited inhibitory neuron populations, were combined with laser scanning photostimulation. We found that each inhibitory cell type received distinct excitatory and inhibitory laminar input patterns. Excitatory inputs could be grouped into three categories. All inhibitory cell types received strong excitation from layer 2/3, and for calretinin (CR)-positive Martinotti cells and burst-spiking interneurons, this was their dominant source of excitatory input. Three other cell types, including fast-spiking basket cells, CR-negative Martinotti cells, and bipolar interneurons, also received strong excitatory input from layer 4. The remaining four inhibitory cell types, including chandelier cells, neurogliaform cells, irregular spiking basket cells, and regular spiking presumptive basket cells, received strong excitatory input from layer 5A and not layer 4. Laminar sources of inhibitory input varied between cell types and could not be predicted from the sources of excitatory input. Thus, there are cell-type specific differences in laminar sources of both excitation and inhibition, and complementary input patterns from layer 4 versus layer 5A suggest cell type differences in their relationships to lemniscal versus paralemniscal pathways.

Key words: photostimulation; barrel cortex; transgenic; GFP; interneurons; somatosensory cortex

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Received Aug. 19, 2008; revised Sept. 27, 2008; accepted Nov. 20, 2008.

Correspondence should be addressed to Dr. Edward M. Callaway, Systems Neurobiology Laboratories, The Salk Institute for Biological Studies, 10010 North Torrey Pines Road, La Jolla, CA 92037. Email: callaway{at}salk.edu

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