Regulation of Spatial Selectivity by Crossover Inhibition

Abstract

Signals throughout the nervous system diverge into parallel excitatory and inhibitory pathways that later converge on downstream neurons to control their spike output. Converging excitatory and inhibitory synaptic inputs can exhibit a variety of temporal relationships. A common motif is feedforward inhibition, in which an increase (decrease) in excitatory input precedes a corresponding increase (decrease) in inhibitory input. The delay of inhibitory input relative to excitatory input originates from an extra synapse in the circuit shaping inhibitory input. Another common motif is push-pull or “crossover” inhibition, in which increases (decreases) in excitatory input occur together with decreases (increases) in inhibitory input. Primate On midget ganglion cells receive primarily feedforward inhibition and On parasol cells receive primarily crossover inhibition; this difference provides an opportunity to study how each motif shapes the light responses of cell types that play a key role in visual perception. For full-field stimuli, feedforward inhibition abbreviated and attenuated responses of On midget cells, while crossover inhibition, though plentiful, had surprisingly little impact on the responses of On parasol cells. Spatially structured stimuli, however, could cause excitatory and inhibitory inputs to On parasol cells to increase together, adopting a temporal relation very much like that for feedforward inhibition. In this case, inhibitory inputs substantially abbreviated a cell’s spike output. Thus inhibitory input shapes the temporal stimulus selectivity of both midget and parasol ganglion cells, but its impact on responses of parasol cells depends strongly on the spatial structure of the light inputs.

A Mechanosensory Circuit that Mixes Opponent Channels to Produce Selectivity for Complex Stimulus Features

“…These two synaptic inputs produce positively correlated changes in the postsynaptic cell with regard to the first-order stimulus feature (luminance), but because they are rectified and then low-pass filtered, they produce anti-correlated effects with regard to the second-order stimulus feature (contrast). As a consequence, postsynaptic cells that integrate these inputs can encode the first-order stimulus while truncating their responses to the second-order stimulus (Cafaro and Rieke, 2013; Molnar et al, 2009; Werblin, 2010). …”

Corticogeniculate feedback sharpens the temporal precision and spatial resolution of visual signals in the ferret

“…Latencies and time courses for retinal and inhibitory PSTHs were adapted from the literature (58)(59)(60), and the CG PSTH was the average LEDR PSTH measured without LED stimulation.…”

Receptive field center-surround interactions mediate context-dependent spatial contrast encoding in the retina

“…In other words, individual bipolar cell subunits in (c) have their own RF surrounds. [40,41,42], and this RF organization can be important for encoding natural visual stimuli [43].…”

“…A sharply rectified bipolar output synapse, on the other hand, underlies nonlinear spatial integration in the RF center. This form of nonlinear integration prevents cancelation of light and dark regions of a scene, and causes RGCs to respond strongly to stimuli like gratings [40,41,34,39,42]. An important functional consequence of nonlinear spatial integration is that it endows a RGC with enhanced sensitivity to spatial contrast at a sub-RF center scale.…”