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

Abstract

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.

Hidden Complexity of Synaptic Receptive Fields in Cat V1

“…We also found a substantial proportion of Complex-like inhibitory subunit, which exhibited no orientation selectivity, especially in Simple cells. These inhibitory components constitute additional evidences favoring the existence of an orientation unselective Complex inhibition, which could participate, at least in some V1 cells (ϳ45%, 5 of 11; in our population), to the contrast-invariance of V1 cell selectivity Lauritzen and Miller, 2003;Nowak et al, 2008;Liu et al, 2009;Shapley and Xing, 2013). Interestingly, our data further show that the balance between the relative weights of inhibitory and excitatory Complex-like subunits tends to increase with the RF Simpleness.…”

Mice Can Use Second-Order, Contrast-Modulated Stimuli to Guide Visual Perception

“…To estimate receptive field (RF) position, we mapped ON and OFF subfields of RFs using a sparse noise stimulus (Liu et al, 2009). This stimulus consisted of white or black squares (4°diameter) briefly flashed (150 or 200 ms) on a square grid (40°or 60°diameter).…”

Orientation selectivity in cat primary visual cortex: local and global measurement

“…Using genetic and imaging tools, recent evidence for orientation selectivity in mouse V1 has not found inhibitory neurons with simple-cell-like RFs, but has found interneurons with complex-cell-like RFs and hardly any orientation selectivity [51] . More evidence shows that the push-pull circuit (in cat V1) [1,52,53] cannot be a major synaptic mechanism underlying simple RFs in mouse V1 and the inhibitory circuit (driven by cortex) may contribute in a different way than in cat V1 to form orientation selectivity in simple cells [51,54,55] .…”

“…More evidence shows that the push-pull circuit (in cat V1) [1,52,53] cannot be a major synaptic mechanism underlying simple RFs in mouse V1 and the inhibitory circuit (driven by cortex) may contribute in a different way than in cat V1 to form orientation selectivity in simple cells [51,54,55] .…”