A Role for Synaptic Input Distribution in a Dendritic Computation of Motion Direction in the Retina

Anna L Vlasits; Ryan D Morrie; Alexandra Tran-Van-Minh; Adam Bleckert; Christian F Gainer; David A DiGregorio; Marla B Feller

doi:10.1016/j.neuron.2016.02.020

A Role for Synaptic Input Distribution in a Dendritic Computation of Motion Direction in the Retina

Neuron. 2016 Mar 16;89(6):1317-1330. doi: 10.1016/j.neuron.2016.02.020.

Authors

Anna L Vlasits¹, Ryan D Morrie², Alexandra Tran-Van-Minh³, Adam Bleckert⁴, Christian F Gainer⁵, David A DiGregorio⁶, Marla B Feller⁷

Affiliations

¹ Helen Wills Neuroscience Institute, University of California, Berkeley, Berkeley, CA 94720, USA.
² Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, CA 94720, USA.
³ Unit of Dynamic Neuronal Imaging, Institut Pasteur, 75724 Paris Cedex 15, France; Centre National de la Recherche Scientifique, Unité Mixte de Recherche 3571, 75724 Paris Cedex 15, France.
⁴ Department of Biological Structure, University of Washington, Seattle, WA 98195, USA.
⁵ Department of Optometry, University of California, Berkeley, Berkeley, CA 94704, USA.
⁶ Unit of Dynamic Neuronal Imaging, Institut Pasteur, 75724 Paris Cedex 15, France; Centre National de la Recherche Scientifique, Unité Mixte de Recherche 3571, 75724 Paris Cedex 15, France. Electronic address: david.digregorio@pasteur.fr.
⁷ Helen Wills Neuroscience Institute, University of California, Berkeley, Berkeley, CA 94720, USA; Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, CA 94720, USA. Electronic address: mfeller@berkeley.edu.

Abstract

The starburst amacrine cell in the mouse retina presents an opportunity to examine the precise role of sensory input location on neuronal computations. Using visual receptive field mapping, glutamate uncaging, two-photon Ca(2+) imaging, and genetic labeling of putative synapses, we identify a unique arrangement of excitatory inputs and neurotransmitter release sites on starburst amacrine cell dendrites: the excitatory input distribution is skewed away from the release sites. By comparing computational simulations with Ca(2+) transients recorded near release sites, we show that this anatomical arrangement of inputs and outputs supports a dendritic mechanism for computing motion direction. Direction-selective Ca(2+) transients persist in the presence of a GABA-A receptor antagonist, though the directional tuning is reduced. These results indicate a synergistic interaction between dendritic and circuit mechanisms for generating direction selectivity in the starburst amacrine cell.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

Acetylcholinesterase / genetics
Acetylcholinesterase / metabolism
Amacrine Cells / drug effects
Amacrine Cells / physiology*
Animals
Animals, Newborn
Calcium / metabolism
Computer Simulation
Dendrites / physiology*
Disks Large Homolog 4 Protein
Excitatory Postsynaptic Potentials / drug effects
Excitatory Postsynaptic Potentials / physiology
Glutamic Acid / pharmacology
Guanylate Kinases / metabolism
Membrane Proteins / metabolism
Mice
Mice, Inbred C57BL
Mice, Transgenic
Models, Neurological*
Motion Perception / drug effects
Motion Perception / physiology*
Orientation / physiology*
Receptors, AMPA / genetics
Receptors, AMPA / metabolism
Retina / cytology*
Synapses / drug effects
Synapses / physiology*
Synapses / ultrastructure
Visual Pathways / physiology

Substances

Disks Large Homolog 4 Protein
Dlg4 protein, mouse
Membrane Proteins
Receptors, AMPA
Glutamic Acid
Guanylate Kinases
Acetylcholinesterase
glutamate receptor ionotropic, AMPA 2
Calcium

Abstract

Publication types

MeSH terms

Substances

Grants and funding