Abstract
Previously, we found that in the mammalian retina, inhibitory inputs onto starburst amacrine cells (SACs) are required for robust direction selectivity of On-Off direction-selective ganglion cells (On-Off DSGCs) against noisy backgrounds (Chen et al., 2016). However, the source of the inhibitory inputs to SACs and how this inhibition confers noise resilience of DSGCs are unknown. Here, we show that when visual noise is present in the background, the motion-evoked inhibition to an On-Off DSGC is preserved by a disinhibitory motif consisting of a serially connected network of neighboring SACs presynaptic to the DSGC. This preservation of inhibition by a disinhibitory motif arises from the interaction between visually evoked network dynamics and short-term synaptic plasticity at the SAC-DSGC synapse. Although the disinhibitory microcircuit is well studied for its disinhibitory function in brain circuits, our results highlight the algorithmic flexibility of this motif beyond disinhibition due to the mutual influence between network and synaptic plasticity mechanisms.
Highlights
Neural circuits exhibit remarkable complexity and specificity of their wiring patterns
The enhanced null-direction spiking triggered by the moving bar in the direction-selective ganglion cell (DSGC) of the Gabra2 cKO group was due to attenuated inhibitory postsynaptic currents (IPSCs) of DSGCs (Figure 1g–j), which come from the GABAergic outputs of starburst amacrine cells (SACs) (Briggman et al, 2011; Fried et al, 2002; Lee et al, 2010; Taylor and Vaney, 2002; Wei et al, 2011)
Our study revealed an unexpected algorithm of the SAC-SAC-DSGC disinhibitory motif that mediates the noise resilience of retinal direction selectivity
Summary
Neural circuits exhibit remarkable complexity and specificity of their wiring patterns. One approach to achieve this goal is to dissect complex circuitry into elementary building blocks, often termed microcircuit motifs (Braganza and Beck, 2018; Cajal, 1937) These motifs consist of a small number of neurons that are connected in characteristic patterns and are thought to perform defined algorithmic functions in neuronal signal processing across brain regions. Disinhibitory microcircuits are prominently involved in sensory processing, learning, and memory in the neocortex and the hippocampus (Jiang et al, 2013; Lee et al, 2013; Letzkus et al, 2011; Pfeffer et al, 2013; Pi et al, 2013), and in action selection in basal ganglia (reviewed in Chevalier and Deniau, 1990; Letzkus et al, 2015) Their functions in these diverse circuits have so far been exclusively attributed to their disinhibitory influences on the principal neurons by relieving the principal neurons from ongoing inhibition
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