Visual Stimulation Switches the Polarity of Excitatory Input to Starburst Amacrine Cells

• Published in: Neuron (Cambridge, Mass.) Mass.), 2014-09, Vol.83 (5), p.1172-1184
• Main Authors: Vlasits, Anna L., Bos, Rémi, Morrie, Ryan D., Fortuny, Cécile, Flannery, John G., Feller, Marla B., Rivlin-Etzion, Michal
• Format: Article
• Language: English
• Subjects: Adaptation, Physiological - drug effects; Adaptation, Physiological - genetics; Amacrine Cells - drug effects; Amacrine Cells - physiology; Animals; Cell Polarity - drug effects; Cell Polarity - genetics; Cell Polarity - physiology; Circuits; Connexins - deficiency; Connexins - genetics; GABA Antagonists - pharmacology; Gap Junction delta-2 Protein; Glycine Agents - pharmacology; Life Sciences; Ligands; Membrane Potentials - drug effects; Membrane Potentials - genetics; Membrane Transport Proteins - genetics; Membrane Transport Proteins - metabolism; Mice; Mice, Inbred C57BL; Mice, Transgenic; Neural Inhibition - drug effects; Neural Inhibition - genetics; Neurobiology; Neurons and Cognition; Phosphinic Acids - pharmacology; Photic Stimulation; Propionates - pharmacology; Pyridazines - pharmacology; Pyridines - pharmacology; Receptors, Glycine - metabolism; Retina; Retina - cytology; Strychnine - pharmacology; Visual Pathways - drug effects; Visual Pathways - physiology
• ISSN: 0896-6273; 1097-4199
• DOI: 10.1016/j.neuron.2014.07.037

Direction-selective ganglion cells (DSGCs) are tuned to motion in one direction. Starburst amacrine cells (SACs) are thought to mediate this direction selectivity through precise anatomical wiring to DSGCs. Nevertheless, we previously found that visual adaptation can reverse DSGCs’s directional tuning, overcoming the circuit anatomy. Here we explore the role of SACs in the generation and adaptation of direction selectivity. First, using pharmacogenetics and two-photon calcium imaging, we validate that SACs are necessary for direction selectivity. Next, we demonstrate that exposure to an adaptive stimulus dramatically alters SACs’ synaptic inputs. Specifically, after visual adaptation, On-SACs lose their excitatory input during light onset but gain an excitatory input during light offset. Our data suggest that visual stimulation alters the interactions between rod- and cone-mediated inputs that converge on the terminals of On-cone BCs. These results demonstrate how the sensory environment can modify computations performed by anatomically defined neuronal circuits. •Reversibly silencing starburst amacrine cells eliminates direction selectivity•After visual stimulation, On-starburst amacrine cells respond at light offset•Response is mediated by glutamate release from On-bipolar cells at light offset•Polarity switch could mediate reversal of direction-selective ganglion cells Vlasits et al. demonstrate that starburst amacrine cells reverse their light response after visual stimulation, with On cells becoming Off cells. Through interactions between photoreceptor signaling pathways, the visual environment influences basic properties of receptive fields of downstream retinal neurons.