Molecular fingerprinting of on–off direction-selective retinal ganglion cells across species and relevance to primate visual circuits

Onkar S. Dhande, Benjamin K. Stafford, Katrin Franke, Rana El-Danaf, Kumiko A. Percival, Ann H. Phan, Peichao Li, Bryan J. Hansen, Phong L. Nguyen, Philipp Berens, W. Rowland Taylor, Edward Callaway, Thomas Euler, Andrew D. Huberman

Research output: Contribution to journalArticle

8 Scopus citations

Abstract

The ability to detect moving objects is an ethologically salient function. Direction-selective neurons have been identified in the retina, thalamus, and cortex of many species, but their homology has remained unclear. For instance, it is unknown whether direction-selective retinal ganglion cells (DSGCs) exist in primates and, if so, whether they are the equivalent to mouse and rabbit DSGCs. Here, we used a molecular/circuit approach in both sexes to address these issues. In mice, we identify the transcription factor Satb2 (special AT-rich sequence-binding protein 2) as a selective marker for three RGC types: On–Off DSGCs encoding motion in either the anterior or posterior direction, a newly identified type of Off-DSGC, and an Off-sustained RGC type. In rabbits, we find that expression of Satb2 is conserved in On–Off DSGCs; however, it has evolved to include On–Off DSGCs encoding upward and downward motion in addition to anterior and posterior motion. Next, we show that macaque RGCs express Satb2 most likely in a single type. We used rabies virus-based circuitmapping tools to reveal the identity of macaque Satb2-RGCs and discovered that their dendritic arbors are relatively large and monostratified. Together, these data indicate Satb2-expressing On–Off DSGCs are likely not present in the primate retina. Moreover, if DSGCs are present in the primate retina, it is unlikely that they express Satb2.

Original languageEnglish (US)
Pages (from-to)78-95
Number of pages18
JournalJournal of Neuroscience
Volume39
Issue number1
DOIs
StatePublished - Jan 2 2019

Keywords

  • Direction selectivity
  • Mouse vision
  • Primate
  • Retina
  • Retinal ganglion cells
  • Visual circuits

ASJC Scopus subject areas

  • Neuroscience(all)

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    Dhande, O. S., Stafford, B. K., Franke, K., El-Danaf, R., Percival, K. A., Phan, A. H., Li, P., Hansen, B. J., Nguyen, P. L., Berens, P., Taylor, W. R., Callaway, E., Euler, T., & Huberman, A. D. (2019). Molecular fingerprinting of on–off direction-selective retinal ganglion cells across species and relevance to primate visual circuits. Journal of Neuroscience, 39(1), 78-95. https://doi.org/10.1523/JNEUROSCI.1784-18.2018