Abstract
The retina processes visual images to compute features such as the direction of image motion. Starburst amacrine cells (SACs), axonless feed-forward interneurons, are essential components of the retinal direction-selective circuitry. Recent work has highlighted that SAC-mediated dendro-dendritic inhibition controls the action potential output of direction-selective ganglion cells (DSGCs) by vetoing dendritic spike initiation. However, SACs co-release GABA and the excitatory neurotransmitter acetylcholine at dendritic sites. Here we use direct dendritic recordings to show that preferred direction light stimuli evoke SAC-mediated acetylcholine release, which powerfully controls the stimulus sensitivity, receptive field size and action potential output of ON-DSGCs by acting as an excitatory drive for the initiation of dendritic spikes. Consistent with this, paired recordings reveal that the activation of single ON-SACs drove dendritic spike generation, because of predominate cholinergic excitation received on the preferred side of ON-DSGCs. Thus, dendro-dendritic release of neurotransmitters from SACs bi-directionally gate dendritic spike initiation to control the directionally selective action potential output of retinal ganglion cells.
Highlights
The retina processes visual images to compute features such as the direction of image motion
In confirmation of previous findings obtained from ON-OFF-DSGCs16,26,34–36, our paired ON-Starburst amacrine cells (SACs) to ON-direction-selective ganglion cells (DSGCs) recordings revealed the dendro-dendritic co-release of ACh and GABA from SACs, which drove postsynaptic excitation and inhibition, mediated by the activation of nicotinic ACh receptors (nAChRs) and GABAA receptors, respectively
SACs positioned on the preferred side, which made close dendro-dendritic appositions from dendrites oriented in the preferred direction of DSGCs, generated net excitatory responses in DSGCs, whereas, SACs located on the null side generated, on average, postsynaptic inhibition
Summary
The retina processes visual images to compute features such as the direction of image motion. We use direct dendritic recordings to show that preferred direction light stimuli evoke SAC-mediated acetylcholine release, which powerfully controls the stimulus sensitivity, receptive field size and action potential output of ON-DSGCs by acting as an excitatory drive for the initiation of dendritic spikes. The direction-selective action potential output of DSGCs is believed to be computed by the integration of a directionally un-tuned excitatory input, predominately mediated by glutamate release from bipolar cells[11,12,13], with a directionally tuned inhibitory synaptic input generated by the dendritic release of GABA from axonless feed-forward interneurons, termed starburst amacrine cells (SACs)[9,14,15,16,17]. We use multi-site electrophysiological recording techniques to demonstrate that the dendro-dendritic release of ACh from SACs powerfully positively gates the initiation of dendritic spikes to control the stimulus-sensitivity, receptive field structure and the magnitude of light-evoked action potential output of DSGCs
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