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Cellular and circuit remodeling of the primate foveal midget pathway after acute photoreceptor loss
Proceedings of the National Academy of Sciences of the United States of America ( IF 9.4 ) Pub Date : 2024-09-04 , DOI: 10.1073/pnas.2413104121
Ryutaro Akiba 1, 2, 3 , Shane Lind Boniec 1 , Sharm Knecht 1 , Hirofumi Uyama 2 , Hung-Ya Tu 2, 4 , Takayuki Baba 3 , Masayo Takahashi 2, 5 , Michiko Mandai 2, 5 , Rachel O Wong 1
Proceedings of the National Academy of Sciences of the United States of America ( IF 9.4 ) Pub Date : 2024-09-04 , DOI: 10.1073/pnas.2413104121
Ryutaro Akiba 1, 2, 3 , Shane Lind Boniec 1 , Sharm Knecht 1 , Hirofumi Uyama 2 , Hung-Ya Tu 2, 4 , Takayuki Baba 3 , Masayo Takahashi 2, 5 , Michiko Mandai 2, 5 , Rachel O Wong 1
Affiliation
The retinal fovea in human and nonhuman primates is essential for high acuity and color vision. Within the fovea lies specialized circuitry in which signals from a single cone photoreceptor are largely conveyed to one ON and one OFF type midget bipolar cell (MBC), which in turn connect to a single ON or OFF midget ganglion cell (MGC), respectively. Restoring foveal vision requires not only photoreceptor replacement but also appropriate reconnection with surviving ON and OFF MBCs and MGCs. However, our current understanding of the effects of cone loss on the remaining foveal midget pathway is limited. We thus used serial block-face electron microscopy to determine the degree of plasticity and potential remodeling of this pathway in adult Macaca fascicularis several months after acute photoreceptor loss upon photocoagulation. We reconstructed MBC structure and connectivity within and adjacent to the region of cone loss. We found that MBC dendrites within the scotoma retracted and failed to reach surviving cones to form new connections. However, both surviving cones and ON and OFF MBC dendrites at the scotoma border exhibited remodeling, suggesting that these neurons can demonstrate plasticity and rewiring at maturity. At six months postlesion, disconnected OFF MBCs clearly lost output ribbon synapses with their postsynaptic partners, whereas the majority of ON MBCs maintained their axonal ribbon numbers, suggesting differential timing or extent in ON and OFF midget circuit remodeling after cone loss. Our findings raise rewiring considerations for cell replacement approaches in the restoration of foveal vision.
中文翻译:
急性光感受器丧失后灵长类中心凹侏儒通路的细胞和电路重塑
人类和非人类灵长类动物的视网膜中央凹对于高敏锐度和色觉至关重要。中央凹内有专门的电路,其中来自单个视锥光感受器的信号大部分被传送到一个开型和一个关型小型双极细胞(MBC),然后分别连接到单个开型或关型小型神经节细胞(MGC)。恢复中央凹视力不仅需要更换感光器,还需要与幸存的 ON 和 OFF MBC 和 MGC 进行适当的重新连接。然而,我们目前对视锥细胞损失对剩余中心凹侏儒通路影响的理解是有限的。因此,我们使用连续块面电子显微镜来确定成年猕猴在光凝导致光感受器急性丧失几个月后该通路的可塑性程度和潜在重塑程度。我们重建了视锥损失区域内及其附近的 MBC 结构和连接性。我们发现暗点内的 MBC 树突收缩,无法到达幸存的视锥细胞形成新的连接。然而,幸存的视锥细胞以及暗点边界处的 ON 和 OFF MBC 树突均表现出重塑,表明这些神经元在成熟时可以表现出可塑性和重新布线。病变后六个月,断开的 OFF MBC 明显失去了与其突触后伙伴的输出带状突触,而大多数 ON MBC 保持了轴突带数量,这表明锥体丢失后 ON 和 OFF 侏儒电路重塑的时间或程度存在差异。我们的研究结果提出了在中心凹视力恢复中细胞替代方法的重新布线考虑。
更新日期:2024-09-04
中文翻译:
急性光感受器丧失后灵长类中心凹侏儒通路的细胞和电路重塑
人类和非人类灵长类动物的视网膜中央凹对于高敏锐度和色觉至关重要。中央凹内有专门的电路,其中来自单个视锥光感受器的信号大部分被传送到一个开型和一个关型小型双极细胞(MBC),然后分别连接到单个开型或关型小型神经节细胞(MGC)。恢复中央凹视力不仅需要更换感光器,还需要与幸存的 ON 和 OFF MBC 和 MGC 进行适当的重新连接。然而,我们目前对视锥细胞损失对剩余中心凹侏儒通路影响的理解是有限的。因此,我们使用连续块面电子显微镜来确定成年猕猴在光凝导致光感受器急性丧失几个月后该通路的可塑性程度和潜在重塑程度。我们重建了视锥损失区域内及其附近的 MBC 结构和连接性。我们发现暗点内的 MBC 树突收缩,无法到达幸存的视锥细胞形成新的连接。然而,幸存的视锥细胞以及暗点边界处的 ON 和 OFF MBC 树突均表现出重塑,表明这些神经元在成熟时可以表现出可塑性和重新布线。病变后六个月,断开的 OFF MBC 明显失去了与其突触后伙伴的输出带状突触,而大多数 ON MBC 保持了轴突带数量,这表明锥体丢失后 ON 和 OFF 侏儒电路重塑的时间或程度存在差异。我们的研究结果提出了在中心凹视力恢复中细胞替代方法的重新布线考虑。