Abstract
In the mammalian retina, direction-selectivity is thought to originate in the dendrites of GABAergic/cholinergic starburst amacrine cells, where it is first observed. However, here we demonstrate that direction selectivity in downstream ganglion cells remains remarkably unaffected when starburst dendrites are rendered non-directional, using a novel strategy combining a conditional GABAA α2 receptor knockout mouse with optogenetics. We show that temporal asymmetries between excitation/inhibition, arising from the differential connectivity patterns of starburst cholinergic and GABAergic synapses to ganglion cells, form the basis for a parallel mechanism generating direction selectivity. We further demonstrate that these distinct mechanisms work in a coordinated way to refine direction selectivity as the stimulus crosses the ganglion cell's receptive field. Thus, precise spatiotemporal patterns of inhibition and excitation that determine directional responses in ganglion cells are shaped by two 'core' mechanisms, both arising from distinct specializations of the starburst network.
Highlights
The direction-selective (DS) circuit in the retina is arguably one of the most well-defined circuits in the mammalian brain
Direction is encoded by output DS ganglion cells (DSGCs), whose response properties are shaped by DS inputs arising from GABAergic/cholinergic starburst amacrine cells and non-DS inputs from glutamatergic bipolar cells (Figure 1A)
Selectively eliminating mutual inhibition between anti-parallel starburst dendrites using the GABAA a2 receptor KO mouse line (Gabra2 KO) leaves starburst DS largely intact (Chen et al, 2016). Consistent with these findings, we found the DS output of the starbursts measured as inhibitory postsynaptic currents (IPSCs) in DSGCs, was similar in Gabra2 KO mice and wild type mice
Summary
The direction-selective (DS) circuit in the retina is arguably one of the most well-defined circuits in the mammalian brain (reviewed by Mauss et al, 2017; Vaney et al, 2012) In this circuit, direction is encoded by output DS ganglion cells (DSGCs), whose response properties are shaped by DS inputs arising from GABAergic/cholinergic starburst amacrine cells (starbursts) and non-DS inputs from glutamatergic bipolar cells (Figure 1A). The second network mechanism relies on the specific wiring of temporally distinct bipolar cells along the proximal-distal axis of the starburst dendrite. This arrangement results in an optimal summation of inputs when the stimulus moves centrifugally (from soma-to dendrite) along the starbursts dendrites (Fransen and Borghuis, 2017; Kim et al, 2014).
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