Department of Brain Sciences, Weizmann Institute of Science, Rehovot, Israel.
J Physiol. 2024 Nov;602(22):6301-6328. doi: 10.1113/JP286581. Epub 2024 Oct 27.
A key feature of the receptive field of neurons in the visual system is their centre-surround antagonism, whereby the centre and the surround exhibit responses of opposite polarity. This organization is thought to enhance visual acuity, but whether and how such antagonism plays a role in more complex processing remains poorly understood. Here, we investigate the role of centre and surround receptive fields in retinal direction selectivity by exposing posterior-preferring On-Off direction-selective ganglion cells (pDSGCs) to adaptive light and recording their response to globally moving objects. We reveal that light adaptation leads to surround expansion in pDSGCs. The pDSGCs maintain their original directional tuning in the centre receptive field, but present the oppositely tuned response in their surround. Notably, although inhibition is the main substrate for retinal direction selectivity, we found that following light adaptation, both the centre- and surround-mediated responses originate from directionally tuned excitatory inputs. Multi-electrode array recordings show similar oppositely tuned responses in other DSGC subtypes. Together, these data attribute a new role for excitation in the direction-selective circuit. This excitation carries an antagonistic centre-surround property, possibly designed to sharpen the detection of motion direction in the retina. KEY POINTS: Receptive fields of direction-selective retinal ganglion cells expand asymmetrically following light adaptation. The increase in the surround receptive field generates a delayed spiking phase that is tuned to the null direction and is mediated by excitation. Following light adaptation, excitation rules the computation in the centre receptive field and is tuned to the preferred direction. GABAergic and glycinergic inputs modulate the null-tuned delayed response differentially. Null-tuned delayed spiking phases can be detected in all types of direction-selective retinal ganglion cells. Light adaptation exposes a hidden directional excitation in the circuit, which is tuned to opposite directions in the centre and surround receptive fields.
视觉系统中神经元的感受野的一个关键特征是其中心-周围拮抗作用，即中心和周围区域表现出相反极性的反应。这种组织被认为可以提高视觉锐度，但这种拮抗作用在更复杂的处理中是否以及如何发挥作用仍知之甚少。在这里，我们通过向优先于后极的 ON-OFF 方向选择性神经节细胞（pDSGC）暴露自适应光并记录它们对全局移动物体的反应，研究了中心和周围感受野在视网膜方向选择性中的作用。我们揭示了光适应导致 pDSGC 周围区域扩大。pDSGC 在中心感受野中保持其原始方向调谐，但在其周围呈现相反调谐的反应。值得注意的是，尽管抑制是视网膜方向选择性的主要基质，但我们发现，在光适应后，中心和周围介导的反应都源自方向调谐的兴奋性输入。多电极阵列记录显示其他 DSGC 亚型也存在类似的相反调谐反应。这些数据共同为方向选择性电路中的兴奋赋予了新的作用。这种兴奋具有拮抗的中心-周围特性，可能旨在提高视网膜中运动方向的检测精度。关键点：光适应后，方向选择性视网膜神经节细胞的感受野不对称扩大。周围感受野的增加产生了与零方向调谐的延迟脉冲相位，并且由兴奋介导。光适应后，兴奋控制中心感受野中的计算，并与首选方向调谐。GABA 能和甘氨酸能输入对零调谐的延迟反应进行不同的调制。在所有类型的方向选择性视网膜神经节细胞中都可以检测到零调谐的延迟脉冲相位。光适应暴露了电路中的隐藏方向兴奋，其在中心和周围感受野中调谐到相反的方向。
