Werner Reichardt Centre for Integrative Neuroscience, Tübingen University, Tübingen, Germany.
Hertie Institute for Clinical Brain Research, Tübingen University, Tübingen, Germany.
J Neurophysiol. 2023 Nov 1;130(5):1282-1302. doi: 10.1152/jn.00289.2023. Epub 2023 Oct 11.
Saccadic inhibition refers to a short-latency transient cessation of saccade generation after visual sensory transients. This oculomotor phenomenon occurs with a latency that is consistent with a rapid influence of sensory responses, such as stimulus-induced visual bursts, on oculomotor control circuitry. However, the neural mechanisms underlying saccadic inhibition are not well understood. Here, we exploited the fact that macaque monkeys experience robust saccadic inhibition to test the hypothesis that inhibition time and strength exhibit systematic visual feature tuning properties to a multitude of visual feature dimensions commonly used in vision science. We measured saccades in three monkeys actively controlling their gaze on a target, and we presented visual onset events at random times. Across seven experiments, the visual onsets tested size, spatial frequency, contrast, orientation, motion direction, and motion speed dependencies of saccadic inhibition. We also investigated how inhibition might depend on the behavioral relevance of the appearing stimuli. We found that saccadic inhibition starts earlier, and is stronger, for large stimuli of low spatial frequencies and high contrasts. Moreover, saccadic inhibition timing depends on motion direction and orientation, with earlier inhibition systematically occurring for horizontally drifting vertical gratings. On the other hand, saccadic inhibition is stronger for faster motions and when the appearing stimuli are subsequently foveated. Besides documenting a range of feature tuning dimensions of saccadic inhibition to the properties of exogenous visual stimuli, our results establish macaque monkeys as an ideal model system for unraveling the neural mechanisms underlying a ubiquitous oculomotor phenomenon in visual neuroscience. Visual onsets dramatically reduce saccade generation likelihood with very short latencies. Such latencies suggest that stimulus-induced visual responses, normally jump-starting perceptual and scene analysis processes, can also directly impact the decision of whether to generate saccades or not, causing saccadic inhibition. Consistent with this, we found that changing the appearance of the visual onsets systematically alters the properties of saccadic inhibition. These results constrain neurally inspired models of coordination between saccade generation and exogenous sensory stimulation.
眼跳抑制是指在视觉感觉瞬变后，眼跳产生的短暂潜伏期内的短暂停止。这种眼球运动现象的潜伏期与感觉反应的快速影响一致，例如刺激诱导的视觉爆发，对眼球运动控制电路有影响。然而，眼跳抑制的神经机制尚不清楚。在这里，我们利用猕猴经历强烈的眼跳抑制的事实，来检验这样一个假设，即抑制时间和强度表现出对多种视觉特征维度的系统视觉特征调谐特性，这些维度在视觉科学中经常使用。我们在三只主动控制注视目标的猴子身上测量了眼跳，并在随机时间呈现视觉起始事件。在七个实验中，视觉起始事件测试了大小、空间频率、对比度、方向、运动方向和运动速度对眼跳抑制的依赖性。我们还研究了抑制可能如何依赖于出现刺激的行为相关性。我们发现，对于低空间频率和高对比度的大刺激，眼跳抑制开始得更早，强度也更大。此外，眼跳抑制的时间取决于运动方向和方向，对于水平漂移的垂直光栅，系统地出现更早的抑制。另一方面，当出现的刺激随后聚焦时，眼跳抑制更强，运动速度也更快。除了记录眼跳抑制对外源性视觉刺激的一系列特征调谐维度之外，我们的结果还确立了猕猴作为解开视觉神经科学中普遍存在的眼球运动现象的神经机制的理想模型系统。视觉起始事件以非常短的潜伏期极大地降低了眼跳产生的可能性。这种潜伏期表明，刺激诱导的视觉反应通常会启动感知和场景分析过程，也可以直接影响是否产生眼跳的决定，从而导致眼跳抑制。与这一观点一致的是，我们发现改变视觉起始事件的外观会系统地改变眼跳抑制的特性。这些结果限制了眼跳生成和外源性感觉刺激之间协调的神经启发模型。
