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The Journal of Neuroscience, August 26, 2009, 29(34):10520-10532; doi:10.1523/JNEUROSCI.1915-09.2009

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Behavioral/Systems/Cognitive
Visual Receptive Field Structure of Cortical Inhibitory Neurons Revealed by Two-Photon Imaging Guided Recording

Bao-hua Liu,¹ Pingyang Li,¹ Ya-tang Li,¹ Yujiao J. Sun,¹ Yuchio Yanagawa,⁴ Kunihiko Obata,⁵ Li I. Zhang,^1,3 and Huizhong W. Tao^1,2

¹Zilkha Neurogenetic Institute and ²Departments of Cell and Neurobiology and ³Physiology and Biophysics, Keck School of Medicine, University of Southern California, Los Angeles, California 90089, ⁴Gunma University Graduate School of Medicine, Maebashi 371-8511, Japan, and ⁵Brain Science Institute, RIKEN, Wako 351-0198, Japan

Correspondence should be addressed to either Huizhong W. Tao or Li I. Zhang at the above address. Email: htao{at}usc.edu or Email: liizhang{at}usc.edu

Synaptic inhibition plays an important role in shaping receptive field (RF) properties in the visual cortex. However, the underlying mechanisms remain not well understood, partly because of difficulties in systematically studying functional properties of cortical inhibitory neurons in vivo. Here, we established two-photon imaging guided cell-attached recordings from genetically labeled inhibitory neurons and nearby "shadowed" excitatory neurons in the primary visual cortex of adult mice. Our results revealed that in layer 2/3, the majority of excitatory neurons exhibited both On and Off spike subfields, with their spatial arrangement varying from being completely segregated to overlapped. In contrast, most layer 4 excitatory neurons exhibited only one discernable subfield. Interestingly, no RF structure with significantly segregated On and Off subfields was observed for layer 2/3 inhibitory neurons of either the fast-spike or regular-spike type. They predominantly possessed overlapped On and Off subfields with a significantly larger size than the excitatory neurons and exhibited much weaker orientation tuning. These results from the mouse visual cortex suggest that different from the push-pull model proposed for simple cells, layer 2/3 simple-type neurons with segregated spike On and Off subfields likely receive spatially overlapped inhibitory On and Off inputs. We propose that the phase-insensitive inhibition can enhance the spatial distinctiveness of On and Off subfields through a gain control mechanism.

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Received April 22, 2009; accepted July 18, 2009.

Correspondence should be addressed to either Huizhong W. Tao or Li I. Zhang at the above address. Email: htao{at}usc.edu or Email: liizhang{at}usc.edu

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