Specific wiring of distinct amacrine cells in the directionally selective retinal circuit permits independent coding of direction and size

Alex Hoggarth; Amanda J McLaughlin; Kara Ronellenfitch; Stuart Trenholm; Rishi Vasandani; Santhosh Sethuramanujam; David Schwab; Kevin L Briggman; Gautam B Awatramani

doi:10.1016/j.neuron.2015.02.035

Specific wiring of distinct amacrine cells in the directionally selective retinal circuit permits independent coding of direction and size

Neuron. 2015 Apr 8;86(1):276-91. doi: 10.1016/j.neuron.2015.02.035. Epub 2015 Mar 19.

Authors

Alex Hoggarth¹, Amanda J McLaughlin¹, Kara Ronellenfitch¹, Stuart Trenholm¹, Rishi Vasandani¹, Santhosh Sethuramanujam¹, David Schwab², Kevin L Briggman³, Gautam B Awatramani⁴

Affiliations

¹ Department of Biology, University of Victoria, Victoria, BC V8W 3N5, Canada.
² Department of Physics & Astronomy, Northwestern University, 2145 Sheridan Road F165, Evanston, IL 60208, USA.
³ Circuit Dynamics and Connectivity Unit, National Institutes of Health, Bethesda, MD 20892, USA.
⁴ Department of Biology, University of Victoria, Victoria, BC V8W 3N5, Canada. Electronic address: gautam@uvic.ca.

PMID: 25801705
DOI: 10.1016/j.neuron.2015.02.035

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.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Amacrine Cells / drug effects
Amacrine Cells / physiology*
Amacrine Cells / ultrastructure
Anesthetics, Local / pharmacology
Animals
Excitatory Postsynaptic Potentials / drug effects
GABA Antagonists / pharmacology
Homeodomain Proteins / genetics
Homeodomain Proteins / metabolism
Light
Mice
Mice, Transgenic
Nerve Net / physiology*
Nerve Net / ultrastructure
Neural Inhibition / drug effects
Neural Inhibition / physiology
Phosphinic Acids / pharmacology
Photic Stimulation
Picrotoxin / pharmacology
Presynaptic Terminals / physiology
Presynaptic Terminals / ultrastructure
Pyridines / pharmacology
Retina / cytology*
Retinal Ganglion Cells / drug effects
Retinal Ganglion Cells / physiology
Size Perception / physiology*
Space Perception / physiology*
Synapses / ultrastructure
Tetrodotoxin / pharmacology
Time Factors
Transcription Factors / genetics
Transcription Factors / metabolism
Visual Fields / drug effects

Substances

(1,2,5,6-tetrahydropyridin-4-yl)methylphosphinic acid
Anesthetics, Local
GABA Antagonists
Homeodomain Proteins
Phosphinic Acids
Pyridines
Transcription Factors
Picrotoxin
Hb9 protein, mouse
Tetrodotoxin

Grants and funding

CIHR- 130268-2013/Canadian Institutes of Health Research/Canada