Department of Brain and Cognitive Sciences, Center for Visual Science, University of Rochester, Rochester, New York 14627.
Department of Neurobiology, University of Chicago, Chicago, Illinois 60637.
J Neurosci. 2023 Mar 15;43(11):1888-1904. doi: 10.1523/JNEUROSCI.1885-22.2023. Epub 2023 Feb 1.
Smooth eye movements are common during natural viewing; we frequently rotate our eyes to track moving objects or to maintain fixation on an object during self-movement. Reliable information about smooth eye movements is crucial to various neural computations, such as estimating heading from optic flow or judging depth from motion parallax. While it is well established that extraretinal signals (e.g., efference copies of motor commands) carry critical information about eye velocity, the rotational optic flow field produced by eye rotations also carries valuable information. Although previous work has shown that dynamic perspective cues in optic flow can be used in computations that require estimates of eye velocity, it has remained unclear where and how the brain processes these visual cues and how they are integrated with extraretinal signals regarding eye rotation. We examined how neurons in the dorsal region of the medial superior temporal area (MSTd) of two male rhesus monkeys represent the direction of smooth pursuit eye movements based on both visual cues (dynamic perspective) and extraretinal signals. We find that most MSTd neurons have matched preferences for the direction of eye rotation based on visual and extraretinal signals. Moreover, neural responses to combinations of these signals are well predicted by a weighted linear summation model. These findings demonstrate a neural substrate for representing the velocity of smooth eye movements based on rotational optic flow and establish area MSTd as a key node for integrating visual and extraretinal signals into a more generalized representation of smooth eye movements. We frequently rotate our eyes to smoothly track objects of interest during self-motion. Information about eye velocity is crucial for a variety of computations performed by the brain, including depth perception and heading perception. Traditionally, information about eye rotation has been thought to arise mainly from extraretinal signals, such as efference copies of motor commands. Previous work shows that eye velocity can also be inferred from rotational optic flow that accompanies smooth eye movements, but the neural origins of these visual signals about eye rotation have remained unknown. We demonstrate that macaque neurons signal the direction of smooth eye rotation based on visual signals, and that they integrate both visual and extraretinal signals regarding eye rotation in a congruent fashion.
自然观察中眼球运动通常很平滑；我们经常转动眼睛来跟踪移动物体，或者在自身运动时保持对物体的注视。关于平滑眼球运动的可靠信息对于各种神经计算至关重要，例如根据光流估计朝向或根据运动视差判断深度。虽然已经证实，视网膜外信号（例如，运动指令的传出副本）携带有关眼球速度的关键信息，但眼球转动产生的旋转视流场也携带有价值的信息。尽管先前的工作表明，光流中的动态透视线索可用于需要估计眼球速度的计算，但仍然不清楚大脑在何处以及如何处理这些视觉线索，以及它们如何与关于眼球转动的视网膜外信号进行整合。我们检查了两只雄性猕猴中内侧上颞区（MSTd）背侧区域的神经元如何根据视觉线索（动态透视）和视网膜外信号来表示平滑追踪眼球运动的方向。我们发现，大多数 MSTd 神经元都具有基于视觉和视网膜外信号的眼球转动方向匹配偏好。此外，这些信号的组合的神经反应可以很好地由加权线性求和模型预测。这些发现为基于旋转视流来表示平滑眼球运动速度提供了一个神经基础，并确立了 MSTd 区域作为将视觉和视网膜外信号整合到更一般的平滑眼球运动表示中的关键节点。在自身运动过程中，我们经常转动眼睛以平滑地跟踪感兴趣的物体。关于眼球速度的信息对于大脑执行的各种计算至关重要，包括深度感知和朝向感知。传统上，眼球转动的信息主要来自视网膜外信号，例如运动指令的传出副本。先前的工作表明，眼球速度也可以根据伴随平滑眼球运动的旋转视流来推断，但是这些关于眼球转动的视觉信号的神经起源仍然未知。我们证明，猕猴神经元根据视觉信号发出平滑眼球转动的方向，并且它们以一致的方式整合关于眼球转动的视觉和视网膜外信号。
