Lateral competition for cortical space by layer-specific horizontal circuits

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Abstract

The cerebral cortex constructs a coherent representation of the world by integrating distinct features of the sensory environment. Although these features are processed vertically across cortical layers, horizontal projections interconnecting neighbouring cortical domains allow these features to be processed in a context-dependent manner. Despite the wealth of physiological and psychophysical studies addressing the function of horizontal projections, how they coordinate activity among cortical domains remains poorly understood. We addressed this question by selectively activating horizontal projection neurons in mouse somatosensory cortex, and determined how the resulting spatial pattern of excitation and inhibition affects cortical activity. We found that horizontal projections suppress superficial layers while simultaneously activating deeper cortical output layers. This layer-specific modulation does not result from a spatial separation of excitation and inhibition, but from a layer-specific ratio between these two opposing conductances. Through this mechanism, cortical domains exploit horizontal projections to compete for cortical space.

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Figure 1: Photoinduced gamma activity in vivo and in vitro.
Figure 2: Vertical match of excitation and inhibition across layers.
Figure 3: Horizontal match of excitation and inhibition within layers.
Figure 4: Lateral suppression and feed-forward facilitation in vivo and in vitro.
Figure 5: Layer-specific excitation/inhibition ratio.

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Acknowledgements

We thank P. Abelkop for immunohistochemical labelling, J. Isaacson and R. Malinow for critical reading of the manuscript and the members of the Scanziani and Isaacson laboratory for advice during the course of the study. We thank K. Svoboda for pCAGGS-ChR2-Venus (Addgene 15753), C. Cepko for pCAG-GFP (Addgene 11150) and K. Deisseroth for sharing reagents. This work was supported in part by a grant from the National Institute for Mental Health (R01 MH70058). H.A. was supported by the Helen Hay Whitney Foundation. M.S. is an investigator of the Howard Hughes Medical Institute.

Author Contributions H.A. and M.S. designed the study. H.A. conducted all experiments and analysis. H.A. and M.S. wrote the paper.

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Correspondence to Massimo Scanziani.

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Adesnik, H., Scanziani, M. Lateral competition for cortical space by layer-specific horizontal circuits. Nature 464, 1155–1160 (2010) doi:10.1038/nature08935

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