Tadokoro Shin, Shinji Yusuke, Yamanaka Toshimi, Hirata Yutaka
Department of Robotic Science and Technology, Graduate School of Engineering, Chubu University, Kasugai, Japan.
Department of Otolaryngology, Head and Neck Surgery, National Defense Medical College, Tokorozawa, Japan.
Front Neurol. 2024 May 7;15:1304496. doi: 10.3389/fneur.2024.1304496. eCollection 2024.
Spatial orientation refers to the perception of relative location and self-motion in space. The accurate formation of spatial orientation is essential for animals to survive and interact safely with their environment. The formation of spatial orientation involves the integration of sensory inputs from the vestibular, visual, and proprioceptive systems. Vestibular organs function as specialized head motion sensors, providing information regarding angular velocity and linear acceleration via the semicircular canals and otoliths, respectively. However, because forces arising from the linear acceleration (translation) and inclination relative to the gravitational axis (tilt) are equivalent, they are indistinguishable by accelerometers, including otoliths. This is commonly referred to as the tilt - translation ambiguity, which can occasionally lead to the misinterpretation of translation as a tilt. The major theoretical frameworks addressing this issue have proposed that the interpretation of tilt versus translation may be contingent on an animal's previous experiences of motion. However, empirical confirmation of this hypothesis is lacking.
In this study, we conducted a behavioral experiment using goldfish to investigate how an animal's motion experience influences its interpretation of tilt vs. translation. We examined a reflexive eye movement called the vestibulo-ocular reflex (VOR), which compensatory-rotates the eyes in response to head motion and is known to reflect an animal's three-dimensional head motion estimate.
We demonstrated that the VORs of naïve goldfish do not differentiate between translation and tilt at 0.5 Hz. However, following prolonged visual-translation training, which provided appropriate visual stimulation in conjunction with translational head motion, the VORs were capable of distinguishing between the two types of head motion within 3 h. These results were replicated using the Kalman filter model of spatial orientation, which incorporated the variable variance of process noise corresponding to the accumulated motion experience.
Based on these experimental and computational findings, we discuss the neural mechanism underlying the resolution of tilt-translation ambiguity within a context analogous to, yet distinct from, previous cross-axis VOR adaptations.
空间定向是指对空间中相对位置和自身运动的感知。准确形成空间定向对于动物生存以及安全地与环境互动至关重要。空间定向的形成涉及来自前庭、视觉和本体感觉系统的感觉输入整合。前庭器官作为专门的头部运动传感器，分别通过半规管和耳石提供有关角速度和线性加速度的信息。然而，由于线性加速度（平移）和相对于重力轴的倾斜产生的力是等效的，包括耳石在内的加速度计无法区分它们。这通常被称为倾斜 - 平移模糊性，偶尔会导致将平移误解为倾斜。解决这个问题的主要理论框架提出，倾斜与平移的解释可能取决于动物以前的运动经历。然而，这一假设缺乏实证证实。
在本研究中，我们使用金鱼进行了一项行为实验，以研究动物的运动经历如何影响其对倾斜与平移的解释。我们研究了一种称为前庭眼反射（VOR）的反射性眼球运动，它会根据头部运动进行补偿性眼球旋转，并且已知能反映动物的三维头部运动估计。
我们证明，未受过训练的金鱼的前庭眼反射在0.5赫兹时无法区分平移和倾斜。然而，经过长时间的视觉平移训练，即结合平移头部运动提供适当的视觉刺激后，前庭眼反射能够在3小时内区分这两种头部运动类型。使用空间定向的卡尔曼滤波器模型复制了这些结果，该模型纳入了与累积运动经验相对应的过程噪声的可变方差。
基于这些实验和计算结果，我们在与先前的跨轴前庭眼反射适应类似但又不同的背景下，讨论了解决倾斜 - 平移模糊性的神经机制。
