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Research ArticleResearch Article: New Research, Development

Retinal Input Is Required for the Maintenance of Neuronal Laminae in the Ventrolateral Geniculate Nucleus

Katelyn Stebbins, Rachana Deven Somaiya, Ubadah Sabbagh, Parsa Khaksar, Yanping Liang, Jianmin Su and Michael A. Fox
eNeuro 19 August 2024, 11 (9) ENEURO.0022-24.2024; https://doi.org/10.1523/ENEURO.0022-24.2024
Katelyn Stebbins
1Fralin Biomedical Research Institute at Virginia Tech Carilion, Roanoke, Virginia 24016
2Graduate Program in Translational Biology, Medicine, and Health, Virginia Tech, Blacksburg, Virginia 24061
3Virginia Tech Carilion School of Medicine, Roanoke, Virginia 24016
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Rachana Deven Somaiya
1Fralin Biomedical Research Institute at Virginia Tech Carilion, Roanoke, Virginia 24016
2Graduate Program in Translational Biology, Medicine, and Health, Virginia Tech, Blacksburg, Virginia 24061
4Department of Molecular and Cell Biology, University of California Berkeley, Berkeley, California 94720
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Ubadah Sabbagh
1Fralin Biomedical Research Institute at Virginia Tech Carilion, Roanoke, Virginia 24016
2Graduate Program in Translational Biology, Medicine, and Health, Virginia Tech, Blacksburg, Virginia 24061
5McGovern Institute for Brain Research, Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, Massachusetts 02138
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Parsa Khaksar
1Fralin Biomedical Research Institute at Virginia Tech Carilion, Roanoke, Virginia 24016
3Virginia Tech Carilion School of Medicine, Roanoke, Virginia 24016
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Yanping Liang
1Fralin Biomedical Research Institute at Virginia Tech Carilion, Roanoke, Virginia 24016
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Jianmin Su
1Fralin Biomedical Research Institute at Virginia Tech Carilion, Roanoke, Virginia 24016
6School of Neuroscience, College of Science, Virginia Tech, Blacksburg, Virginia 24061
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Michael A. Fox
1Fralin Biomedical Research Institute at Virginia Tech Carilion, Roanoke, Virginia 24016
4Department of Molecular and Cell Biology, University of California Berkeley, Berkeley, California 94720
7Department of Biological Sciences, College of Science, Virginia Tech, Blacksburg, Virginia 24061
8Department of Biology, College of Natural Sciences, University of Massachusetts Amherst, Amherst, Massachusetts 01003
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Abstract

Retinal ganglion cell (RGC) axons provide direct input into several brain regions, including the dorsal lateral geniculate nucleus (dLGN), which is important for image-forming vision, and the ventrolateral geniculate nucleus (vLGN), which is associated with nonimage-forming vision. Through both activity- and morphogen-dependent mechanisms, retinal inputs play important roles in the development of dLGN, including the refinement of retinal projections, morphological development of thalamocortical relay cells (TRCs), timing of corticogeniculate innervation, and recruitment and distribution of inhibitory interneurons. In contrast, little is known about the role of retinal inputs in the development of vLGN. Grossly, vLGN is divided into two domains, the retinorecipient external vLGN (vLGNe) and nonretinorecipient internal vLGN (vLGNi). Studies previously found that vLGNe consists of transcriptionally distinct GABAergic subtypes distributed into at least four adjacent laminae. At present, it remains unclear whether retinal inputs influence the development of these cell-type–specific neuronal laminae in vLGNe. Here, we elucidated the developmental timeline for these laminae in the mouse vLGNe, and results indicate that these laminae are specified at or before birth. We observed that mutant mice without retinal inputs have a normal laminar distribution of GABAergic cells at birth; however, after the first week of postnatal development, these mutants exhibited a dramatic disruption in the laminar organization of inhibitory neurons and clear boundaries between vLGNe and vLGNi. Overall, our results show that while the formation of cell-type–specific layers in mouse vLGNe does not depend on RGC inputs, retinal signals are critical for their maintenance.

  • GABAergic neuron
  • lateral geniculate nucleus
  • retina
  • retinal ganglion cells
  • visual thalamus

Footnotes

  • The authors declare no competing financial interests.

  • We thank the members of the MAF lab for the scientific discussion and comments on the manuscript. We thank Dr. Steven W. Wang for providing Math5−/− mice. This work was supported by the National Institutes of Health Grant EY033528 (M.A.F.), EY021222 (M.A.F.), NS113459 (U.S.), and EY035570 (K.S.).

  • ↵*These authors contributed equally.

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

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Retinal Input Is Required for the Maintenance of Neuronal Laminae in the Ventrolateral Geniculate Nucleus
Katelyn Stebbins, Rachana Deven Somaiya, Ubadah Sabbagh, Parsa Khaksar, Yanping Liang, Jianmin Su, Michael A. Fox
eNeuro 19 August 2024, 11 (9) ENEURO.0022-24.2024; DOI: 10.1523/ENEURO.0022-24.2024

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Retinal Input Is Required for the Maintenance of Neuronal Laminae in the Ventrolateral Geniculate Nucleus
Katelyn Stebbins, Rachana Deven Somaiya, Ubadah Sabbagh, Parsa Khaksar, Yanping Liang, Jianmin Su, Michael A. Fox
eNeuro 19 August 2024, 11 (9) ENEURO.0022-24.2024; DOI: 10.1523/ENEURO.0022-24.2024
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Keywords

  • GABAergic neuron
  • lateral geniculate nucleus
  • retina
  • retinal ganglion cells
  • visual thalamus

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