TY - JOUR
T1 - Molecular fingerprinting of on–off direction-selective retinal ganglion cells across species and relevance to primate visual circuits
AU - Dhande, Onkar S.
AU - Stafford, Benjamin K.
AU - Franke, Katrin
AU - El-Danaf, Rana
AU - Percival, Kumiko A.
AU - Phan, Ann H.
AU - Li, Peichao
AU - Hansen, Bryan J.
AU - Nguyen, Phong L.
AU - Berens, Philipp
AU - Taylor, W. Rowland
AU - Callaway, Edward
AU - Euler, Thomas
AU - Huberman, Andrew D.
N1 - Publisher Copyright:
© 2019 the authors.
PY - 2019/1/2
Y1 - 2019/1/2
N2 - 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.
AB - 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.
KW - Direction selectivity
KW - Mouse vision
KW - Primate
KW - Retina
KW - Retinal ganglion cells
KW - Visual circuits
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U2 - 10.1523/JNEUROSCI.1784-18.2018
DO - 10.1523/JNEUROSCI.1784-18.2018
M3 - Article
C2 - 30377226
AN - SCOPUS:85059501230
SN - 0270-6474
VL - 39
SP - 78
EP - 95
JO - Journal of Neuroscience
JF - Journal of Neuroscience
IS - 1
ER -