Heeman Jessica, White Brian J, Van der Stigchel Stefan, Theeuwes Jan, Itti Laurent, Munoz Douglas P
Faculty of Social and Behavioral Sciences, Experimental Psychology, Helmholtz Institute, Utrecht University, Utrecht 3584, the Netherlands
Institute Brain and Behavior Amsterdam, Department of Experimental and Applied Psychology, Vrije Universiteit Amsterdam, Amsterdam, the Netherlands.
J Neurosci. 2025 Jan 15;45(3):e0428242024. doi: 10.1523/JNEUROSCI.0428-24.2024.
Eye movements in daily life occur in rapid succession and often without a predefined goal. Using a free viewing task, we examined how fixation duration prior to a saccade correlates to visual saliency and neuronal activity in the superior colliculus (SC) at the saccade goal. Rhesus monkeys (three male) watched videos of natural, dynamic, scenes while eye movements were tracked and, simultaneously, neurons were recorded in the superficial and intermediate layers of the superior colliculus (SCs and SCi, respectively), a midbrain structure closely associated with gaze, attention, and saliency coding. Saccades that were directed into the neuron's receptive field (RF) were extrapolated from the data. To interpret the complex visual input, saliency at the RF location was computed during the pre-saccadic fixation period using a computational saliency model. We analyzed if visual saliency and neural activity at the saccade goal predicted pre-saccadic fixation duration. We report three major findings: (1) Saliency at the saccade goal inversely correlated with fixation duration, with motion and edge information being the strongest predictors. (2) SC visual saliency responses in both SCs and SCi were inversely related to fixation duration. (3) SCs neurons, and not SCi neurons, showed higher activation for two consecutive short fixations, suggestive of concurrent saccade processing during free viewing. These results reveal a close correspondence between visual saliency, SC processing, and the timing of saccade initiation during free viewing and are discussed in relation to their implication for understanding saccade initiation during real-world gaze behavior.
日常生活中的眼球运动快速且连续发生，并且常常没有预先设定的目标。我们使用自由观看任务，研究了扫视前的注视持续时间与扫视目标处上丘（SC）的视觉显著性和神经元活动之间的相关性。恒河猴（三只雄性）观看自然动态场景的视频，同时追踪眼球运动，并记录上丘浅层和中层（分别为SCs和SCi）的神经元活动，上丘是一个与注视、注意力和显著性编码密切相关的中脑结构。从数据中推断出指向神经元感受野（RF）的扫视。为了解释复杂的视觉输入，在扫视前的注视期使用计算显著性模型计算RF位置的显著性。我们分析了扫视目标处的视觉显著性和神经活动是否能预测扫视前的注视持续时间。我们报告了三个主要发现：（1）扫视目标处的显著性与注视持续时间呈负相关，运动和边缘信息是最强的预测因素。（2）SCs和SCi中的SC视觉显著性反应均与注视持续时间呈负相关。（3）SCs神经元而非SCi神经元在连续两次短注视时表现出更高的激活，这表明在自由观看期间存在并发的扫视处理。这些结果揭示了自由观看期间视觉显著性、SC处理和扫视起始时间之间的密切对应关系，并就它们对理解现实世界注视行为中扫视起始的意义进行了讨论。
