Synaptic Convergence Patterns onto Retinal Ganglion Cells Are Preserved despite Topographic Variation in Pre- and Postsynaptic Territories
Wan-Qing Yu,
Rana N. El-Danaf,
Haruhisa Okawa,
Justin M. Pacholec,
Ulf Matti,
Karin Schwarz,
Benjamin Odermatt,
Felice A. Dunn,
Leon Lagnado,
Frank Schmitz,
Andrew D. Huberman,
Rachel O.L. Wong
Affiliations
Wan-Qing Yu
Department of Biological Structure, University of Washington, Seattle, WA 98195, USA
Rana N. El-Danaf
Department of Neurobiology, Stanford University School of Medicine, Stanford, CA 94305, USA
Haruhisa Okawa
Department of Biological Structure, University of Washington, Seattle, WA 98195, USA
Justin M. Pacholec
Department of Biological Structure, University of Washington, Seattle, WA 98195, USA
Ulf Matti
Department of Neuroanatomy, Medical School Homburg/Saar, Institute for Anatomy and Cell Biology, Saarland University, 66421 Homburg/Saar, Germany
Karin Schwarz
Department of Neuroanatomy, Medical School Homburg/Saar, Institute for Anatomy and Cell Biology, Saarland University, 66421 Homburg/Saar, Germany
Benjamin Odermatt
Institute of Anatomy, University of Bonn, 53115 Bonn, Germany
Felice A. Dunn
Department of Ophthalmology, University of California, San Francisco, San Francisco, CA 94143, USA
Leon Lagnado
School of Life Sciences, University of Sussex, Brighton BN1 9QG, UK
Frank Schmitz
Department of Neuroanatomy, Medical School Homburg/Saar, Institute for Anatomy and Cell Biology, Saarland University, 66421 Homburg/Saar, Germany
Andrew D. Huberman
Department of Neurobiology, Stanford University School of Medicine, Stanford, CA 94305, USA; Departments of Neurobiology and Ophthalmology, Stanford Neurosciences Institute, and BioX, Stanford University School of Medicine, Stanford, CA 94305, USA
Rachel O.L. Wong
Department of Biological Structure, University of Washington, Seattle, WA 98195, USA; Corresponding author
Summary: Sensory processing can be tuned by a neuron’s integration area, the types of inputs, and the proportion and number of connections with those inputs. Integration areas often vary topographically to sample space differentially across regions. Here, we highlight two visual circuits in which topographic changes in the postsynaptic retinal ganglion cell (RGC) dendritic territories and their presynaptic bipolar cell (BC) axonal territories are either matched or unmatched. Despite this difference, in both circuits, the proportion of inputs from each BC type, i.e., synaptic convergence between specific BCs and RGCs, remained constant across varying dendritic territory sizes. Furthermore, synapse density between BCs and RGCs was invariant across topography. Our results demonstrate a wiring design, likely engaging homotypic axonal tiling of BCs, that ensures consistency in synaptic convergence between specific BC types onto their target RGCs while enabling independent regulation of pre- and postsynaptic territory sizes and synapse number between cell pairs. : Yu et al. show that the density of excitatory synapses on retinal output neurons is invariant of retinal location, even though connectivity between pre- and postsynaptic cell pairs can vary. These results have implications for understanding topographic variations in processing of visual stimuli and for understanding consistency of CNS wiring diagrams.
