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Long, intrinsic horizontal axons radiating through and beyond rat barrel cortex have spatial distributions similar to horizontal spreads of activity evoked by whisker stimulation

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Abstract

Stimulation of a single whisker evokes a peak of activity that is centered over the associated barrel in rat primary somatosensory cortex, and yet the evoked local field potential and the intrinsic signal optical imaging response spread symmetrically away from this barrel for over 3.5 mm to cross cytoarchitectonic borders into other “unimodal” sensory cortical areas. To determine whether long horizontal axons have the spatial distribution necessary to underlie this activity spread, we injected adeno-associated viral vectors into barrel cortex and characterized labeled axons extending from the injection site in transverse sections of flattened cortex. Combined qualitative and quantitative analyses revealed labeled axons radiating diffusely in all directions for over 3.5 mm from supragranular injection sites, with density declining over distance. The projection pattern was similar at four different cortical depths, including infragranular laminae. Infragranular vector injections produced patterns similar to the supragranular injections. Long horizontal axons were detected both using a vector with a permissive cytomegalovirus promoter to label all neuronal subtypes and using a calcium/calmodulin-dependent protein kinase II α vector to restrict labeling to excitatory cortical pyramidal neurons. Individual axons were successfully reconstructed from series of supragranular sections, indicating that they traversed gray matter only. Reconstructed axons extended from the injection site, left the barrel field, branched, and sometimes crossed into other sensory cortices identified by cytochrome oxidase staining. Thus, radiations of long horizontal axons indeed have the spatial characteristics necessary to explain horizontal activity spreads. These axons may contribute to multimodal cortical responses and various forms of cortical neural plasticity.

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Acknowledgments

This work was supported by the United States National Institute for Neurological Disorders and Stroke (PHS Grants NS-055832 and NS-066001). We thank Daniel D. Johnson for designing many of the quantitative approaches used here, and for writing custom MatLab software to facilitate data collection and analysis. We also thank many students who performed imaging, tracing, and axon reconstruction described here: Joel Ramirez, Theodore Nieblas, Ajitesh Singh, Karishma Patel, Gordon Man, Roblen Guevarra, Raymond Jed Singson, Keli Tahara, Pejman Majd, Jason Louie, Rika Takada, Keith Uyeno, Jeremy Chen, Joel Fong, Velinda Liao, Bahram Rabbani, Marina Gerges, Julie Liang, Camillia Azimi, Maria Najam, Paul Lang, George Khamo, Hilda Zuñiga, Julian Huynh, Tiffany Do, Sean Siguenza, Ambrose Ha, Min Kim, Troy Ruff, Francisco Lee, Justin Hung, and John Hakim. We acknowledge further the creative contributions of Paul Lang, Camillia Azimi, Keli Tahara, Joel Ramirez, Roblen Guevarra, Gordon Man, Pejman Majd, Jason Louie, and Theodore Nieblas. Finally, we thank Cynthia Chen-Bee and Nathan Jacobs for valuable suggestions throughout the project and Dr. Cynthia Woo for comments on the manuscript.

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Authors and Affiliations

  1. Department of Neurobiology and Behavior, University of California, Irvine, Irvine, CA, 92697-4550, USA

    B. A. Johnson & R. D. Frostig

  2. Department of Biomedical Engineering and Center for the Neurobiology of Learning and Memory, University of California, Irvine, Irvine, CA, 92697, USA

    R. D. Frostig

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Johnson, B.A., Frostig, R.D. Long, intrinsic horizontal axons radiating through and beyond rat barrel cortex have spatial distributions similar to horizontal spreads of activity evoked by whisker stimulation. Brain Struct Funct 221, 3617–3639 (2016). https://doi.org/10.1007/s00429-015-1123-7

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