State Key Laboratory of Cognitive Neuroscience and Learning & IDG/McGovern Institute for Brain Research, Beijing Normal University, Beijing, 100875, China.
College of Life Sciences, Beijing Normal University, Beijing, 100875, China.
J Neurosci. 2023 Aug 2;43(31):5668-5684. doi: 10.1523/JNEUROSCI.0168-23.2023. Epub 2023 Jul 24.
Black and white information is asymmetrically distributed in natural scenes, evokes asymmetric neuronal responses, and causes asymmetric perceptions. Recognizing the universality and essentiality of black-white asymmetry in visual information processing, the neural substrates for black-white asymmetry remain unclear. To disentangle the role of the feedforward and recurrent mechanisms in the generation of cortical black-white asymmetry, we recorded the V1 laminar responses and LGN responses of anesthetized cats of both sexes. In a cortical column, we found that black-white asymmetry starts at the input layer and becomes more pronounced in the output layer. We also found distinct dynamics of black-white asymmetry between the output layer and the input layer. Specifically, black responses dominate in all layers after stimulus onset. After stimulus offset, black and white responses are balanced in the input layer, but black responses still dominate in the output layer. Compared with that in the input layer, the rebound response in the output layer is significantly suppressed. The relative suppression strength evoked by white stimuli is notably stronger and depends on the location within the ON-OFF cortical map. A model with delayed and polarity-selective cortical suppression explains black-white asymmetry in the output layer, within which prominent recurrent connections are identified by Granger causality analysis. In addition to black-white asymmetry in response strength, the interlaminar differences in spatial receptive field varied dynamically. Our findings suggest that the feedforward and recurrent mechanisms are dynamically recruited for the generation of black-white asymmetry in V1. Black-white asymmetry is universal and essential in visual information processing, yet the neural substrates for cortical black-white asymmetry remain unknown. Leveraging V1 laminar recordings, we provided the first laminar pattern of black-white asymmetry in cat V1 and found distinct dynamics of black-white asymmetry between the output layer and the input layer. Comparing black-white asymmetry across three visual hierarchies, the LGN, V1 input layer, and V1 output layer, we demonstrated that the feedforward and recurrent mechanisms are dynamically recruited for the generation of cortical black-white asymmetry. Our findings not only enhance our understanding of laminar processing within a cortical column but also elucidate how feedforward connections and recurrent connections interact to shape neuronal response properties.
黑白色信息在自然场景中呈非对称分布，引起非对称的神经元反应，并导致非对称的感知。鉴于黑白色非对称在视觉信息处理中的普遍性和重要性，其神经基础仍不清楚。为了厘清前馈和反馈机制在皮层黑白色非对称产生中的作用，我们记录了雌雄两性麻醉猫的 V1 层响应和外侧膝状体（LGN）响应。在一个皮层柱内，我们发现黑白色非对称始于输入层，并在输出层变得更加明显。我们还发现了输出层和输入层之间黑白色非对称的不同动态。具体来说，在刺激开始后，黑白色响应在所有层中均占主导地位。在刺激结束后，输入层中黑白色响应平衡，但在输出层中黑响应仍占主导地位。与输入层相比，输出层中的反弹响应显著受到抑制。由白色刺激引起的相对抑制强度显著更强，并取决于 ON-OFF 皮层图内的位置。一个具有延迟和极性选择性皮层抑制的模型解释了输出层中的黑白色非对称，其中通过格兰杰因果关系分析确定了显著的反馈连接。除了响应强度的黑白色非对称之外，层间的空间感受野差异也具有动态变化。我们的发现表明，前馈和反馈机制被动态募集用于产生 V1 中的黑白色非对称。黑白色非对称在视觉信息处理中具有普遍性和重要性，但皮层黑白色非对称的神经基础仍不清楚。利用 V1 层记录，我们提供了猫 V1 中黑白色非对称的第一个层模式，并发现了输出层和输入层之间黑白色非对称的不同动态。通过比较三个视觉层次（外侧膝状体、V1 输入层和 V1 输出层）中的黑白色非对称，我们证明了前馈和反馈机制被动态募集用于产生皮层黑白色非对称。我们的发现不仅增强了我们对皮层柱内层处理的理解，还阐明了前馈连接和反馈连接如何相互作用以塑造神经元响应特性。
