Nonlinear Spatiotemporal Integration by Electrical and Chemical Synapses in the Retina

Abstract

Summary Electrical and chemical synapses coexist in circuits throughout the CNS. Yet, it is not well understood how electrical and chemical synaptic transmission interact to determine the functional output of networks endowed with both types of synapse. We found that release of glutamate from bipolar cells onto retinal ganglion cells (RGCs) was strongly shaped by gap junction-mediated electrical coupling within the bipolar cell network of the mouse retina. Specifically, electrical synapses spread signals laterally between bipolar cells, and this lateral spread contributed to a nonlinear enhancement of bipolar cell output to visual stimuli presented closely in space and time. Our findings thus (1) highlight how electrical and chemical transmission can work in concert to influence network output, and (2) reveal a previously unappreciated circuit mechanism that increases RGC sensitivity to spatiotemporally correlated input, such as that produced by motion.

Divisive suppression explains high-precision firing and contrast adaptation in retinal ganglion cells

“…Therefore, our results demonstrate that the temporal precision in the early visual system likely originates from nonlinear processing in the inputs to retinal ganglion cells. Note that the full spiking-DivS model did not incorporate any form of direct synaptic inhibition onto the ON-Alpha cell, consistent with findings that the impact of such inhibition is relatively weak and that excitation dominates the spike response in the stimulus regime that we studied (Kuo et al, 2016; Murphy and Rieke, 2006). …”

Synaptic Rectification Controls Nonlinear Spatial Integration of Natural Visual Inputs

“…causing the RGC response to depend on the spatial distribution of light, not just the total amount of light, within the RF center. At least in some cases, bipolar cells presynaptic to the RGC are the physiological basis of the rectified RF subunits (Demb et al , 2001; Schwartz et al , 2012; Freeman et al , 2015; Kuo et al , 2016). …”

“…Thus, an impressive body of work demonstrates the ubiquity of nonlinear spatial integration, the circuit and synaptic mechanisms that give rise to a nonlinear RF, and some of the computations that a nonlinear RF can support (Olveczky et al , 2003; Gollisch & Meister, 2008; Schwartz et al , 2012; Kuo et al ., 2016, for review see Gollisch & Meister, 2010; Schwartz & Rieke, 2011). Beyond the retina, the classical energy model of complex cells in V1 also relies on nonlinear transformation of multiple linear filter outputs before integration (Adelson & Bergen, 1985), and more recent evidence suggests that a nonlinear subunit RF structure is appropriate for both simple and complex cells in primary visual cortex (Rust et al , 2005; Vintch et al 2012; Vintch et al , 2015).…”

Molecular Chaperone ERp29: A Potential Target for Cellular Protection in Retinal and Neurodegenerative Diseases

“…bipolar cells, horizontal cells, amacrine cells, RGCs, photoreceptors, and glia; Danesh-Meyer et al 2016). Though the specific functional consequences of many of these distinct couplings is unknown, the gap junctions enabling electrical coupling among bipolar cells have recently been discovered to affect the release of glutamate in the inner plexiform layer in a manner that laterally spreads bipolar cell signaling and specifically enhances RGC sensitivity to motion (Kuo et al 2016). …”