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From Receptive to Perceptive Fields: Size-Dependent Asymmetries in Both Negative Afterimages and Subcortical On and Off Post-Stimulus Responses
Journal of Neuroscience ( IF 5.3 ) Pub Date : 2021-09-15 , DOI: 10.1523/jneurosci.0300-21.2021
Xu Liu , Hui Li , Ye Wang , Tianhao Lei , Jijun Wang , Lothar Spillmann , Ian Max Andolina , Wei Wang

Negative afterimages are perceptual phenomena that occur after physical stimuli disappear from sight. Their origin is linked to transient post-stimulus responses of visual neurons. The receptive fields (RFs) of these subcortical ON- and OFF-center neurons exhibit antagonistic interactions between central and surrounding visual space, resulting in selectivity for stimulus polarity and size. These two features are closely intertwined, yet their relationship to negative afterimage perception remains unknown. Here we tested whether size differentially affects the perception of bright and dark negative afterimages in humans of both sexes, and how this correlates with neural mechanisms in subcortical ON and OFF cells. Psychophysically, we found a size-dependent asymmetry whereby dark disks produce stronger and longer-lasting negative afterimages than bright disks of equal contrast at sizes >0.8°. Neurophysiological recordings from retinal and relay cells in female cat dorsal lateral geniculate nucleus showed that subcortical ON cells exhibited stronger sustained post-stimulus responses to dark disks, than OFF cells to bright disks, at sizes >1°. These sizes agree with the emergence of center-surround antagonism, revealing stronger suppression to opposite-polarity stimuli for OFF versus ON cells, particularly in dorsal lateral geniculate nucleus. Using a network-based retino-geniculate model, we confirmed stronger antagonism and temporal transience for OFF-cell post-stimulus rebound responses. A V1 population model demonstrated that both strength and duration asymmetries can be propagated to downstream cortical areas. Our results demonstrate how size-dependent antagonism impacts both the neuronal post-stimulus response and the resulting afterimage percepts, thereby supporting the idea of perceptual RFs reflecting the underlying neuronal RF organization of single cells.

SIGNIFICANCE STATEMENT Visual illusions occur when sensory inputs and perceptual outcomes do not match, and provide a valuable tool to understand transformations from neural to perceptual responses. A classic example are negative afterimages that remain visible after a stimulus is removed from view. Such perceptions are linked to responses in early visual neurons, yet the details remain poorly understood. Combining human psychophysics, neurophysiological recordings in cats and retino-thalamo-cortical computational modeling, our study reveals how stimulus size and the receptive-field structure of subcortical ON and OFF cells contributes to the parallel asymmetries between neural and perceptual responses to bright versus dark afterimages. Thus, this work provides a deeper link from the underlying neural mechanisms to the resultant perceptual outcomes.



中文翻译:

从感受野到感知领域:负残像和皮层下开启和关闭刺激后反应的大小相关的不对称性

负残像是在物理刺激从视线中消失后发生的感知现象。它们的起源与视觉神经元的瞬时刺激后反应有关。这些皮层下 ON 和 OFF 中心神经元的感受野 (RF) 表现出中央和周围视觉空间之间的拮抗相互作用,从而导致对刺激极性和大小的选择性。这两个特征紧密交织在一起,但它们与负面残像感知的关系仍然未知。在这里,我们测试了大小是否会不同地影响两性人类对明暗负残像的感知,以及这与皮层下 ON 和 OFF 细胞的神经机制有何关联。从心理上来说,我们发现了一种与尺寸相关的不对称性,即在尺寸大于 0.8° 的情况下,暗盘比同等对比度的亮盘产生更强、更持久的负残像。来自雌性猫背外侧膝状体核中视网膜和中继细胞的神经生理学记录表明,皮质下 ON 细胞对暗盘表现出比 OFF 细胞对亮盘更强的持续刺激后反应,大小 >1°。这些大小与中心周围拮抗作用的出现一致,揭示了 OFF 与 ON 细胞对相反极性刺激的更强抑制,特别是在背外侧膝状体核中。使用基于网络的 retino-geniculate 模型,我们证实了对 OFF 细胞刺激后反弹反应更强的拮抗作用和时间短暂性。V1 人口模型表明,强度和持续时间的不对称都可以传播到下游的皮质区域。我们的结果证明了大小依赖性拮抗作用如何影响神经元刺激后反应和由此产生的残像感知,从而支持感知 RFs 反映单个细胞的潜在神经元 RF 组织的想法。

意义声明当感官输入和知觉结果不匹配时会出现视觉错觉,并提供了一个有价值的工具来理解从神经到知觉反应的转换。一个典型的例子是从视野中移除刺激后仍然可见的负残像。这种感知与早期视觉神经元的反应有关,但细节仍然知之甚少。结合人类心理物理学、猫的神经生理学记录和视网膜 - 丘脑 - 皮质计算模型,我们的研究揭示了刺激大小和皮层下 ON 和 OFF 细胞的感受野结构如何导致神经和知觉对亮与暗残像的反应之间的平行不对称. 因此,这项工作提供了从潜在神经机制到由此产生的感知结果的更深层次的联系。

更新日期:2021-09-16
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