title: Specific wiring of distinct amacrine cells in the directionally selective retinal circuit permits independent coding of direction and size.
abstract: Local and global forms of inhibition controlling directionally selective ganglion cells (DSGCs) in the mammalian retina are well documented. It is established that local inhibition arising from GABAergic starburst amacrine cells (SACs) strongly contributes to direction selectivity. Here, we demonstrate that increasing ambient illumination leads to the recruitment of GABAergic wide-field amacrine cells (WACs) endowing the DS circuit with an additional feature: size selectivity. Using a combination of electrophysiology, pharmacology, and light/electron microscopy, we show that WACs predominantly contact presynaptic bipolar cells, which drive direct excitation and feedforward inhibition (through SACs) to DSGCs, thus maintaining the appropriate balance of inhibition/excitation required for generating DS. This circuit arrangement permits high-fidelity direction coding over a range of ambient light levels, over which size selectivity is adjusted. Together, these results provide novel insights into the anatomical and functional arrangement of multiple inhibitory interneurons within a single computational module in the retina.
authors: Department of Biology, University of Victoria, Victoria, BC V8W 3N5, Canada.
authors: Alex
authors: A
authors: Hoggarth
authors: Department of Biology, University of Victoria, Victoria, BC V8W 3N5, Canada.
authors: Amanda J
authors: AJ
authors: McLaughlin
authors: Department of Biology, University of Victoria, Victoria, BC V8W 3N5, Canada.
authors: Kara
authors: K
authors: Ronellenfitch
authors: Department of Biology, University of Victoria, Victoria, BC V8W 3N5, Canada.
authors: Stuart
authors: S
authors: Trenholm
authors: Department of Biology, University of Victoria, Victoria, BC V8W 3N5, Canada.
authors: Rishi
authors: R
authors: Vasandani
authors: Department of Biology, University of Victoria, Victoria, BC V8W 3N5, Canada.
authors: Santhosh
authors: S
authors: Sethuramanujam
authors: Department of Physics & Astronomy, Northwestern University, 2145 Sheridan Road F165, Evanston, IL 60208, USA.
authors: David
authors: D
authors: Schwab
authors: Circuit Dynamics and Connectivity Unit, National Institutes of Health, Bethesda, MD 20892, USA.
authors: Kevin L
authors: KL
authors: Briggman
authors: Department of Biology, University of Victoria, Victoria, BC V8W 3N5, Canada. Electronic address: gautam@uvic.ca.
authors: Gautam B
authors: GB
authors: Awatramani
mesh_terms: D025042:Amacrine Cells / Q000187:drug effects / Q000502:physiology* / Q000648:ultrastructure; D000779:Anesthetics, Local / Q000494:pharmacology; D000818:Animals; D019706:Excitatory Postsynaptic Potentials / Q000187:drug effects; D018756:GABA Antagonists / Q000494:pharmacology; D018398:Homeodomain Proteins / Q000235:genetics / Q000378:metabolism; D008027:Light; D051379:Mice; D008822:Mice, Transgenic; D009415:Nerve Net / Q000502:physiology* / Q000648:ultrastructure; D009433:Neural Inhibition / Q000187:drug effects / Q000502:physiology; D010721:Phosphinic Acids / Q000494:pharmacology; D010775:Photic Stimulation; D010852:Picrotoxin / Q000494:pharmacology; D017729:Presynaptic Terminals / Q000502:physiology / Q000648:ultrastructure; D011725:Pyridines / Q000494:pharmacology; D012160:Retina / Q000166:cytology*; D012165:Retinal Ganglion Cells / Q000187:drug effects / Q000502:physiology; D012858:Size Perception / Q000502:physiology*; D013028:Space Perception / Q000502:physiology*; D013569:Synapses / Q000648:ultrastructure; D013779:Tetrodotoxin / Q000494:pharmacology; D013997:Time Factors; D014157:Transcription Factors / Q000235:genetics / Q000378:metabolism; D014794:Visual Fields / Q000187:drug effects
chemical_list: D000779:Anesthetics, Local; D018756:GABA Antagonists; D018398:Homeodomain Proteins; D010721:Phosphinic Acids; D010852:Picrotoxin; D011725:Pyridines; D013779:Tetrodotoxin; D014157:Transcription Factors; C101879:(1,2,5,6-tetrahydropyridin-4-yl)methylphosphinic acid; C084059:Hb9 protein, mouse