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Molecular Fingerprinting of On-Off Direction-Selective Retinal Ganglion Cells Across Species and Relevance to Primate Visual Circuits.

The Journal of neuroscience : the official journal of the Society for Neuroscience | 2019

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 circuit-mapping 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.SIGNIFICANCE STATEMENT The ability to detect object motion is a fundamental feature of almost all visual systems. Here, we identify a novel marker for retinal ganglion cells encoding directional motion that is evolutionarily conserved in mice and rabbits, but not in primates. We show in macaque monkeys that retinal ganglion cells (RGCs) that express this marker comprise a single type and are morphologically distinct from mouse and rabbit direction-selective RGCs. Our findings indicate that On-Off direction-selective retinal neurons may have evolutionarily diverged in primates and more generally provide novel insight into the identity and organization of primate parallel visual pathways.

Pubmed ID: 30377226 RIS Download

Associated grants

  • Agency: NEI NIH HHS, United States
    Id: R01 EY026100
  • Agency: NEI NIH HHS, United States
    Id: R01 EY022577
  • Agency: NEI NIH HHS, United States
    Id: P30 EY026877
  • Agency: NEI NIH HHS, United States
    Id: R01 EY022070
  • Agency: NINDS NIH HHS, United States
    Id: U01 NS090562
  • Agency: NEI NIH HHS, United States
    Id: R01 EY014888
  • Agency: NEI NIH HHS, United States
    Id: R01 EY022157

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This is a list of tools and resources that we have found mentioned in this publication.


Anti-Green Fluorescent Protein Antibody (antibody)

RRID:AB_10000240

This polyclonal targets Green Fluorescent Protein (GFP)

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SATB2 antibody (antibody)

RRID:AB_2301417

This polyclonal targets SATB2 antibody

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Anti-RBPMS Antibody (antibody)

RRID:AB_2492226

This polyclonal targets RBPMS

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Anti-Choline Acetyltransferase Antibody (antibody)

RRID:AB_2079751

This polyclonal targets Choline Acetyltransferase

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Mouse Osteopontin (OPN) Affinity Purified Polyclonal Ab (antibody)

RRID:AB_2194992

This polyclonal targets Mouse Osteopontin (OPN) Affinity Purified Ab

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Anti-Green Fluorescent Protein Antibody (antibody)

RRID:AB_10000240

This polyclonal targets Green Fluorescent Protein (GFP)

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Mouse Osteopontin (OPN) Affinity Purified Polyclonal Ab (antibody)

RRID:AB_2194992

This polyclonal targets Mouse Osteopontin (OPN) Affinity Purified Ab

View all literature mentions

SATB2 antibody (antibody)

RRID:AB_2301417

This polyclonal targets SATB2 antibody

View all literature mentions

Anti-Choline Acetyltransferase Antibody (antibody)

RRID:AB_2079751

This polyclonal targets Choline Acetyltransferase

View all literature mentions

Anti-RBPMS Antibody (antibody)

RRID:AB_2492226

This polyclonal targets RBPMS

View all literature mentions