Department of Neuroscience, Baylor College of Medicine, Houston, TX, USA.
Hunter College and the Graduate Center, The City University of New York, New York, USA.
J Physiol. 2023 Oct;601(19):4355-4373. doi: 10.1113/JP284022. Epub 2023 Sep 6.
In animal species ranging from invertebrate to mammals, visually guided escape behaviours have been studied using looming stimuli, the two-dimensional expanding projection on a screen of an object approaching on a collision course at constant speed. The peak firing rate or membrane potential of neurons responding to looming stimuli often tracks a fixed threshold angular size of the approaching stimulus that contributes to the triggering of escape behaviours. To study whether this result holds more generally, we designed stimuli that simulate acceleration or deceleration over the course of object approach on a collision course. Under these conditions, we found that the angular threshold conveyed by collision detecting neurons in grasshoppers was sensitive to acceleration whereas the triggering of escape behaviours was less so. In contrast, neurons in goldfish identified through the characteristic features of the escape behaviours they trigger, showed little sensitivity to acceleration. This closely mirrored a broader lack of sensitivity to acceleration of the goldfish escape behaviour. Thus, although the sensory coding of simulated colliding stimuli with non-zero acceleration probably differs in grasshoppers and goldfish, the triggering of escape behaviours converges towards similar characteristics. Approaching stimuli with non-zero acceleration may help refine our understanding of neural computations underlying escape behaviours in a broad range of animal species. KEY POINTS: A companion manuscript showed that two mathematical models of collision-detecting neurons in grasshoppers and goldfish make distinct predictions for the timing of their responses to simulated objects approaching on a collision course with non-zero acceleration. Testing these experimental predictions showed that grasshopper neurons are sensitive to acceleration while goldfish neurons are not, in agreement with the distinct models proposed previously in these species using constant velocity approaches. Grasshopper and goldfish escape behaviours occurred after the stimulus reached a fixed angular size insensitive to acceleration, suggesting further downstream processing in grasshopper motor circuits to match what was observed in goldfish. Thus, in spite of different sensory processing in the two species, escape behaviours converge towards similar solutions. The use of object acceleration during approach on a collision course may help better understand the neural computations implemented for collision avoidance in a broad range of species.
在从无脊椎动物到哺乳动物等各种动物物种中，人们已经使用逼近刺激物研究了视觉引导的逃避行为，逼近刺激物是指在以恒定速度接近碰撞路线的屏幕上，物体二维扩展的投影。对逼近刺激物做出反应的神经元的峰值放电率或膜电位通常会跟踪逼近刺激物的固定角度大小阈值，该阈值有助于触发逃避行为。为了研究这一结果是否更普遍，我们设计了模拟物体在碰撞路线上接近过程中加速或减速的刺激物。在这些条件下，我们发现，在蝗虫中，检测碰撞的神经元传递的角度阈值对加速度敏感，而逃避行为的触发则不那么敏感。相比之下，通过它们触发的逃避行为的特征来识别的金鱼神经元对加速度的敏感性则较小。这与金鱼逃避行为对加速度的广泛缺乏敏感性非常吻合。因此，尽管具有非零加速度的模拟碰撞刺激的感觉编码在蝗虫和金鱼中可能有所不同，但逃避行为的触发则趋向于类似的特征。具有非零加速度的接近刺激可能有助于更深入地了解广泛的动物物种中逃避行为的神经计算。关键点：一份配套的手稿表明，两种蝗虫和金鱼的碰撞检测神经元的数学模型对其对具有非零加速度的模拟物体接近碰撞路线时的反应时间做出了截然不同的预测。测试这些实验预测表明，蝗虫神经元对加速度敏感，而金鱼神经元则不敏感，这与之前在这两个物种中使用恒定速度方法提出的截然不同的模型一致。蝗虫和金鱼的逃避行为在刺激物达到不敏感于加速度的固定角度大小后发生，这表明在蝗虫的运动电路中存在进一步的下游处理，以匹配在金鱼中观察到的情况。因此，尽管这两个物种的感觉处理不同，但逃避行为趋向于类似的解决方案。在碰撞路线上接近时使用物体加速度可能有助于更好地理解在广泛的物种中实现避碰的神经计算。
