Department of Bio and Brain Engineering.
Program of Brain and Cognitive Engineering, Korea Advanced Institute of Science and Technology, Daejeon 34141, Republic of Korea.
J Neurosci. 2020 Aug 19;40(34):6584-6599. doi: 10.1523/JNEUROSCI.0649-20.2020. Epub 2020 Jul 17.
In the primary visual cortex (V1) of higher mammals, long-range horizontal connections (LHCs) are observed to develop, linking iso-orientation domains of cortical tuning. It is unknown how this feature-specific wiring of circuitry develops before eye-opening. Here, we suggest that LHCs in V1 may originate from spatiotemporally structured feedforward activities generated from spontaneous retinal waves. Using model simulations based on the anatomy and observed activity patterns of the retina, we show that waves propagating in retinal mosaics can initialize the wiring of LHCs by coactivating neurons of similar tuning, whereas equivalent random activities cannot induce such organizations. Simulations showed that emerged LHCs can produce the patterned activities observed in V1, matching the topography of the underlying orientation map. The model can also reproduce feature-specific microcircuits in the salt-and-pepper organizations found in rodents. Our results imply that early peripheral activities contribute significantly to cortical development of functional circuits. Long-range horizontal connections (LHCs) in the primary visual cortex (V1) are observed to emerge before the onset of visual experience, thereby selectively connecting iso-domains of orientation map. However, it is unknown how such feature-specific wirings develop before eye-opening. Here, we show that LHCs in V1 may originate from the feature-specific activation of cortical neurons by spontaneous retinal waves during early developmental stages. Our simulations of a visual cortex model show that feedforward activities from the retina initialize the spatial organization of activity patterns in V1, which induces visual feature-specific wirings in the V1 neurons. Our model also explains the origin of cortical microcircuits observed in rodents, suggesting that the proposed developmental mechanism is universally applicable to circuits of various mammalian species.
在高等哺乳动物的初级视觉皮层 (V1) 中，观察到长程水平连接 (LHCs) 的发展，将皮层调谐的同方向域连接起来。在睁眼之前，这种特定于特征的电路布线是如何发展的尚不清楚。在这里，我们提出 V1 中的 LHC 可能起源于自发视网膜波产生的时空结构的前馈活动。使用基于视网膜解剖结构和观察到的活动模式的模型模拟，我们表明，在视网膜镶嵌体中传播的波可以通过共同激活具有相似调谐的神经元来初始化 LHC 的布线，而等效的随机活动不能诱导这种组织。模拟表明，出现的 LHC 可以产生在 V1 中观察到的图案化活动，与底层取向图的拓扑结构相匹配。该模型还可以再现啮齿动物中发现的椒盐组织中的特征特定微电路。我们的结果表明，早期的外围活动对皮质功能电路的发育有重要贡献。初级视觉皮层 (V1) 中的长程水平连接 (LHC) 在视觉经验开始之前出现，从而选择性地连接方位图的同域。然而，尚不清楚在睁眼之前这种特定于特征的布线是如何发展的。在这里，我们表明，V1 中的 LHC 可能起源于早期发育阶段自发视网膜波对皮质神经元的特征特异性激活。我们的视觉皮层模型模拟表明，来自视网膜的前馈活动初始化了 V1 中活动模式的空间组织，从而诱导了 V1 神经元中视觉特征特定的布线。我们的模型还解释了在啮齿动物中观察到的皮质微电路的起源，表明所提出的发育机制普遍适用于各种哺乳动物物种的电路。
