title: Contributions of Rod and Cone Pathways to Retinal Direction Selectivity Through Development.
abstract: Direction selectivity is a robust computation across a broad stimulus space that is mediated by activity of both rod and cone photoreceptors through the ON and OFF pathways. However, rods, S-cones, and M-cones activate the ON and OFF circuits via distinct pathways and the relative contribution of each to direction selectivity is unknown. Using a variety of stimulation paradigms, pharmacological agents, and knockout mice that lack rod transduction, we found that inputs from the ON pathway were critical for strong direction-selective (DS) tuning in the OFF pathway. For UV light stimulation, the ON pathway inputs to the OFF pathway originated with rod signaling, whereas for visible stimulation, the ON pathway inputs to the OFF pathway originated with both rod and M-cone signaling. Whole-cell voltage-clamp recordings revealed that blocking the ON pathway reduced directional tuning in the OFF pathway via a reduction in null-side inhibition, which is provided by OFF starburst amacrine cells (SACs). Consistent with this, our recordings from OFF SACs confirmed that signals originating in the ON pathway contribute to their excitation. Finally, we observed that, for UV stimulation, ON contributions to OFF DS tuning matured earlier than direct signaling via the OFF pathway. These data indicate that the retina uses multiple strategies for computing DS responses across different colors and stages of development.
  
  
  
  The retina uses parallel pathways to encode different features of the visual scene. In some cases, these distinct pathways converge on circuits that mediate a distinct computation. For example, rod and cone pathways enable direction-selective (DS) ganglion cells to encode motion over a wide range of light intensities. Here, we show that although direction selectivity is robust across light intensities, motion discrimination for OFF signals is dependent upon ON signaling. At eye opening, ON directional tuning is mature, whereas OFF DS tuning is significantly reduced due to a delayed maturation of S-cone to OFF cone bipolar signaling. These results provide evidence that the retina uses multiple strategies for computing DS responses across different stimulus conditions.
authors.affiliation: Department of Molecular and Cell Biology and.
authors.forename: Juliana M
authors.identifier: 0000-0003-0857-3746
authors.initials: JM
authors.lastname: Rosa
authors.affiliation: Department of Molecular and Cell Biology and.
authors.forename: Ryan D
authors.identifier: 0000-0001-9227-4997
authors.initials: RD
authors.lastname: Morrie
authors.affiliation: Department of Molecular and Cell Biology and.
authors.forename: Hans C
authors.identifier: 0000-0002-4080-5597
authors.initials: HC
authors.lastname: Baertsch
authors.affiliation: Department of Molecular and Cell Biology and Helen Wills Neurosciences Institute, University of California, Berkeley, California 94720 mfeller@berkeley.edu.
authors.forename: Marla B
authors.identifier: 0000-0002-9137-5849
authors.initials: MB
authors.lastname: Feller
mesh_terms: D000200:Action Potentials; D000818:Animals; D055358:Cone Opsins / Q000378:metabolism; D008027:Light; D055537:Light Signal Transduction / Q000187:drug effects; D051379:Mice; D008810:Mice, Inbred C57BL; D008822:Mice, Transgenic; D009949:Orientation / Q000502:physiology*; D010775:Photic Stimulation; D018091:Receptors, AMPA / Q000235:genetics / Q000378:metabolism; D015375:Receptors, Interleukin-2 / Q000235:genetics / Q000378:metabolism; D018025:Receptors, Thyrotropin-Releasing Hormone / Q000235:genetics / Q000378:metabolism; D012160:Retina / Q000166:cytology*; D017949:Retinal Cone Photoreceptor Cells / Q000502:physiology*; D012165:Retinal Ganglion Cells; D017948:Retinal Rod Photoreceptor Cells / Q000502:physiology*; D017299:Rod Opsins / Q000378:metabolism; D055366:Synaptic Potentials / Q000502:physiology; D014466:Ultraviolet Rays; D014795:Visual Pathways / Q000502:physiology*
chemical_list: D055358:Cone Opsins; D018091:Receptors, AMPA; D015375:Receptors, Interleukin-2; D018025:Receptors, Thyrotropin-Releasing Hormone; D017299:Rod Opsins; C104722:glutamate receptor ionotropic, AMPA 2
keywords: Gnat1; development; direction selective ganglion cells; direction selectivity; retina; rod/cone pathway