My first rotation in graduate school was in Dr. Lawrence (“Larry”) Stark’s Oculomotor Research Lab¹. My father (a real doctor) was visiting, and I was excited to show off the lab. He was seemingly mesmerized by a wall full of journals on Presbyopia. But after a long period of concentration he said, “Presbyopia? You get old; you need reading glasses. What else is there to say?” I found that hard to disagree with, so I struggled to explain why I found eye movements so interesting.

我在研究生院的第一个工作是在Stark的动眼研究实验室¹中的Lawrence(“ Larry”)博士中进行的。 我的父亲(一位真正的医生)来了，我很高兴炫耀实验室。 他似乎被一堵堆满老花眼杂志的墙迷住了。 但是经过长时间的专注，他说：“老花眼？ 你变老了 你需要老花镜。 还有什么要说的？” 我发现很难不同意，所以我很难解释为什么我发现眼动如此有趣。

Yet, the study of eye movements played a critical role throughout the history of Science and — inexorably intertwined with study of vision and perception — served as the crucible for emerging fields of psychology, neuroscience, and cybernetics. Eye movements have fascinated — and eluded — some of the greatest minds over the millennia, including Aristotle, Ptolemy, Galen, Alhazen, da Vinci, Bacon, Descartes, Helmholtz, and Sherrington.

然而，对眼动的研究在整个科学史上都起着至关重要的作用，并且与视觉和知觉研究无可避免地交织在一起，成为心理学，神经科学和控制论新兴领域的关键。 几千年来，眼动一直着迷，而使人们无法企及，包括亚里斯多德，托勒密，盖伦，阿尔哈曾，达芬奇，培根，笛卡尔，亥姆霍兹和谢灵顿。

Perhaps the most influential of the ancients was Galen of Pergamon (129–200 AD). He was one of the most prolific writers in antiquity, his surviving works exceed 1 million words. (He was also personal physician to Roman Emperors Marcus Aurelius, Lucius Verus, Commodus, Septimius Severus, and Caracalla.) Galen gave us the first detailed understanding of muscular contraction. He recognized muscles worked in agonist/antagonist pairs and speculated that they were powered by “animal spirits” flowing through the nerves. He performed dissections of rhesus monkeys, detailed the organization and structure of the six extraocular muscles, and even performed surgeries to correct strabismus and cataracts. Not bad for 200 A.D.

也许最有影响力的古代人是Perl加蒙的盖伦(Galen of Pergamon，公元129-200年)。 他是古代最多产的作家之一，其尚存的作品超过一百万字。 (他还是罗马皇帝Marcus Aurelius，Lucius Verus，Commodus，Septimius Severus和Caracalla的私人医生。)Galen对肌肉收缩有了第一个详细的了解。 他认识到肌肉在激动剂/拮抗剂对中起作用，并推测它们由流过神经的“动物精神”驱动。 他进行了猕猴的解剖，详细介绍了六眼眼外肌的组织和结构，甚至进行了手术以矫正斜视和白内障。 公元200年还不错

Over most of the next millennium, most advances in mathematics and sciences can be attributed to the “Islamic Golden Age.” Arab mathematician Ḥasan Ibn al-Haytham (Latinized Alhazen) expanded on the ideas of Aristotle, Ptolemy, and Galen and was the first to apply these theories to the “scientific method” of hypothesis testing. His contributions preceded or anticipated many developments over the next thousand years. He reasoned that vision was the result of light impinging on the retina, rather than emanating from the eyes. He calculated the existence of a surface in space, the horopter, where vision is monocular (both eyes see the same image). Alhazen (as well as Ptolemy) also noted that eye movements were either conjugate (the same) or disjunctive (opposite). In the 1800’s, this phenomenon was formally established as “Hering’s Law,” and continues to be a significant topic of study and debate in neuroscience and psychology.

在下一个千年的大部分时间里，数学和科学的大多数进步都可以归因于“伊斯兰黄金时代”。 阿拉伯数学家ḤasanIbn al-Haytham( 拉丁语为 Alhazen)扩展了亚里斯多德，托勒密和盖伦的思想，并且是第一个将这些理论应用于假设检验的“科学方法”的人。 在接下来的一千多年中，他的贡献先于或预期了许多发展。 他认为视觉是光线照射到视网膜上而不是从眼睛发出的结果。 他计算了太空中存在的表面，即horopter，其中视觉是单眼的(两只眼睛都看到相同的图像)。 Alhazen(以及托勒密)还指出，眼球运动是共轭的(相同的)或析取的(相反的)。 在1800年代，这种现象正式被确立为“海灵定律”，并且一直是神经科学和心理学领域研究和辩论的重要话题。

Alhazen had been commissioned by Caliphs of Egypt, to regulate the flooding of the Nile at Aswan. But his plan proved unworkable, and he was arrested by caliph Al-Hakin bi-Amr Allah. While under house arrest, Alhazen wrote his seven-volume Book of Optics (1011–1021). This is widely credited with having established Optics as the first, modern scientific discipline, and Alhazen is often referred to as “The Father of Optics.” His work was first translated into Latin 200 years later and became widely influential on Renaissance scientists after it was printed in 1571.

埃及哈里发政府委托Alhazen来规范尼罗河在阿斯旺的洪水。 但是他的计划被证明是行不通的，他被哈里发·哈金·阿姆·阿拉所逮捕。 在软禁期间，Alhazen撰写了他的七卷《光学之书》 (1011-1021)。 人们将建立光学作为第一门现代科学学科而广受赞誉，而Alhazen通常被称为“光学之父”。 200年后，他的著作首次被翻译成拉丁文，并于1571年出版后，对文艺复兴时期的科学家产生了广泛的影响。

The most significant advance in Western science was the invention of corrective eyeglasses in Italy (circa 1280), but the eye movements gained renewed attention in the Renaissance. Leonardo da Vinci created hundreds of anatomical studies or the eyes and brain (using cows, as human dissections were forbidden). He was one of the first to recognize the optic nerves crossed hemispheres (Fig. 2). Johannes Kepler’s work on the retinal image extended Alhazen’s ideas. Even Francis Bacon had something to say about eye movements, though admittedly, not his best work:

西方科学领域最重要的进步是在意大利(约1280年)发明了矫正眼镜，但在文艺复兴时期，眼球运动受到了新的关注。 达·芬奇(Leonardo da Vinci)进行了数百项解剖学研究，或者对眼睛和大脑进行了解剖学研究(使用牛，因为禁止人类解剖)。 他是最早认识到视神经横越半球的人之一(图2)。 约翰内斯·开普勒(Johannes Kepler)在视网膜图像上的工作扩展了Alhazen的想法。 即使是弗朗西斯·培根(Francis Bacon)也有关于眼球运动的言论，尽管可以承认，这并不是他的最佳作品：

“The eyes do move one and the same way; for when one eye moveth to the nostril, the other moveth from the nostril. The cause is motion of consent, which in the spirits and parts spiritual is strong².”

“ 眼睛的确以相同的方式移动； 因为当一只眼睛向鼻Kong移动时，另一只眼睛从鼻Kong移动。 原因在于同意的动议，在精神和精神层面上都是很强烈的²。 ”

The Eyes and The Scientific Revolution

眼睛与科学革命

To history buffs, it probably comes as no surprise that Rene Descartes was to have the most lasting impact on the field. Through his seminal studies of the optics of the retina, the reflex arc, and oculomotor mechanics, he offered one of the first, integrated views of neurobiology. Cartesian physics was uncompromisingly mechanistic, placing the enterprise on a testable, scientific foundation and ushering in the Scientific Revolution across several branches of biology.

对于历史爱好者来说，Rene Descartes对这一领域产生最持久的影响也许并不奇怪。 通过对视网膜光学，反射弧和动眼力学的开创性研究，他提供了神经生物学的最早的综合观点之一。 笛卡尔物理学是毫不妥协的机制，使企业处于可测试的科学基础上，并跨生物学的多个分支发起了科学革命。

For instance, his “balloon theory” of ocular muscle operation (1664), launched a 300-year quest to unravel the mechanisms of muscular contraction. Descartes proposed muscles were powered by hydraulic fluids from a central reservoir (the ventricles of the brain [Fig. 3]). His theory had a short reign, being disproved in 1667 by Jan Swammerdam, who demonstrated muscles did not change volume when contracting³. (From this point on the canonical muscle of study transitioned to the more convenient, frog legs.) Galvani (1791) demonstrated electricity can trigger muscle contraction, leading to electromotive theories (and inspiring re-animation in Mary Shelly’s Frankenstein). Protein folding and spring theories dominated the field for 100 years. The modern, sliding filament theory was developed in 1954–1969 by Andrew Huxley⁴. Incidentally, Andrew Huxley received the Nobel Prize in Physiology and Medicine, but not for his work on muscle. He and Alan Hodgkin developed the mathematical model for the propagation of neural action potentials with Alan Hodgkin in 1952. His half-brother, Aldous Huxley, wrote Brave New World.

例如，他的眼球手术“气球理论”(1664年)发起了长达300年的探索，以阐明肌肉收缩的机制。 笛卡尔提出的肌肉由来自中央蓄水池(脑室)的液压油提供动力(图3)。 他的理论统治时间很短，在1667年由扬·斯瓦默丹(Jan Swammerdam)提出了反证，他证明了收缩时肌肉并没有改变体积3。 (从这一点上，研究的典型肌肉过渡到更方便的青蛙腿。)Galvani(1791)证明了电可以触发肌肉收缩，从而产生电动理论(并激发了玛丽·雪莱的《 科学怪人》中的 动画效果 ) 。 蛋白质折叠和弹簧理论在该领域占据了100年的主导地位。 现代的滑动长丝理论是由安德鲁·赫⁴黎(Andrew Huxley in)在1954–1969年提出的。 顺便说一句，安德鲁·赫x黎(Andrew Huxley)因其在肌肉方面的研究而获得诺贝尔生理学和医学奖。 他和艾伦·霍奇金(Alan Hodgkin)于1952年与艾伦·霍奇金(Alan Hodgkin)共同开发了用于传播神经动作电位的数学模型。他的同父异母兄弟Aldous Huxley写了《 勇敢的新世界》。

Why Eye Movements?

为什么要眼动？

What was the scientific appeal of eye movements? Beyond our natural fascination with the visual senses, the oculomotor system possesses three, unique advantages as a system of study.

眼球运动的科学吸引力是什么？ 除了对视觉的自然迷恋之外，动眼系统还具有三个独特的学习系统优势。

First, unlike almost everything else in Science — the goal, or purpose, of an eye movement is obvious. They are subject to both conscious and unconscious control, allowing lines of research into reflexes, volitional control, as well as psychological processes.

首先，与《科学》中的几乎所有其他事物不同，眼动的目的或目的是显而易见的。 他们受到有意识和无意识的控制，从而可以对反射，意志控制以及心理过程进行研究。

Second, the oculomotor system is almost the simplest mechanical system imaginable. The human eyeball is nearly spherical, and the eye does not physically interact with the environment (it does not have to lift anything). This greatly simplifies the dynamical equations used to model its’ operation. The eye is controlled by an ensemble of 6 extraocular muscles. For the most part, horizontal eye movements are driven by a single pair of muscles (medial and lateral rectii). Vertical and cyclorotary movements are only slightly more complicated. For instance, the Superior Oblique muscle operates using a pulley fashioned from a loop of tendon, the Trochlea (Fig. 4A), efficiently leveraging muscle force, while reversing its’ direction. Another interesting tidbit: owls and hawks have the full complement of 6 extraocular muscles, despite the fact that they can barely move their oddly-shaped eyes (Fig. 4B). The head movements of owls are analogous to mammalian eye movements.

其次，动眼系统几乎是可想象的最简单的机械系统。 人眼几乎是球形的，并且眼睛与环境没有物理相互作用(它不需要举起任何东西)。 这大大简化了用于对其运行进行建模的动力学方程。 眼睛由6个眼外肌的合奏控制。 在大多数情况下，水平眼运动是由一对肌肉(内侧和外侧直肠)驱动的。 垂直和旋转运动只是稍微复杂一点。 例如，上斜肌使用由肌腱环Trochlea制成的滑轮(图4A)操作，有效地利用肌肉力，同时反转其方向。 另一个有趣的花絮：猫头鹰和鹰具有6种眼外肌的完整互补，尽管它们几乎不能移动其奇形怪状的眼睛(图4B)。 猫头鹰的头部运动类似于哺乳动物的眼睛运动。

Third, there are only a handful of distinct types of eye movements:

第三，只有少数几种不同类型的眼睛运动：

1. Saccades: rapid “jerks” of the eye to reposition the eye in space, like while reading. “Saccade” is French for “jerk.” Human infants are unable to produce saccades.

1.扫视：快速的眼睛“颠簸”，使眼睛在空间中重新定位，就像在阅读时一样。 “ Saccade”是法语中的“混蛋”。 人类婴儿无法产生扫视。

2. Tracking movements (smooth pursuit, optokinetic, whole field tracking): Deficiencies in tracking eye movements are evidence of schizophrenia, autism, and other disorders.

2.跟踪运动(平稳跟踪，视动，全场跟踪)：跟踪眼动的缺陷是精神分裂症，自闭症和其他疾病的证据。

3. Vergence: simultaneous movements of both eyes in opposite directions, to maintain binocular vision. An extreme example of vergence is to go “cross-eyed.”

3.散度：两只眼睛同时向相反方向移动，以保持双眼视力。 收敛的一个极端例子是“斗鸡眼”。

4. The Vestibular Ocular Reflex: counter-rotation of the eyes to stabilize the gaze as the head rotates. The three vestibular semi-circular canals detect angular acceleration, acting as biological gyroscopes. Disorders of the VOR can lead to motion sickness and vertigo.

4.前庭眼反射：随着头部旋转，眼睛反向旋转以稳定视线。 三个前庭半圆形管检测角加速度，充当生物陀螺仪。 VOR疾病可导致晕车和眩晕。

…and the intraocular movements:

…以及眼内运动：

5. Accommodation: changing the focal length by reshaping the lens.

5.调节：通过重塑镜头来改变焦距。

6. Pupillary: shrinking the pupil to reduce light intensity. Head trauma can cause asymmetrical pupillary response.

6.瞳Kong：缩小瞳Kong以减少光强度。 头部外伤可引起瞳Kong不对称React。

As we will see, these 6 movements are driven by separate control systems, yet are integrated in function. The simple dynamics of eye movements allowed focussed, incremental research, often leading to breakthroughs far ahead of other areas in physiology and neurobiology.

正如我们将看到的，这6个机芯是由独立的控制系统驱动的，但功能已集成。 眼球运动的简单动态允许进行集中的渐进式研究，通常会导致远远超过生理学和神经生物学其他领域的突破。

The Laws of Eye Movements

眼动定律

Eye movements are essentially two-dimensional, but the eye can move with three degrees of freedom (horizontal, vertical, and cyclorotary). There is little in the anatomy of the eye muscles themselves to prevent the eye from doing some very weird things (think of the chameleon). This observation led to a line of research to understand why they don’t. In the 19th Century, it was fashion to cast nearly any relationship between observations as a natural “law.” Accordingly, the era witnessed the discovery of several “laws of eye movements,” building toward an understanding that it was neurobiological control, rather than mechanical constraints, that governed eye movements.

眼睛的运动本质上是二维的，但是眼睛可以以三个自由度(水平，垂直和回转)运动。 眼睛肌肉本身的解剖结构很少阻止眼睛做一些非常奇怪的事情(例如变色龙)。 这种观察导致了一系列研究，以了解他们为什么不这样做 。 在19世纪，将观察之间的几乎任何关系转换为自然的“定律”是一种时尚。 因此，这个时代见证了几项“眼球运动定律”的发现，从而使人们认识到，眼球运动是神经生物学控制而非机械约束。

Donder’s Law (Franciscus Cornelius Donders 1818–89)

唐德定律(Franciscus Cornelius Donders 1818–89)

If eye movements were simple rotations about the axis, a 45-degree oblique eye movement would be very different than two movements (horizontal, then vertical) to the same position, with the eye/retina being rotated 10 degrees. Donder’s law states that for any one gaze direction the eye’s 3D spatial orientation is unique and independent of how the eye reached that gaze direction.

如果眼睛运动是围绕轴的简单旋转，则45度倾斜的眼睛运动与将眼睛/视网膜旋转10度的两个运动(水平，然后垂直)移动到同一位置会有很大不同。 唐德定律指出，对于任何一个凝视方向，眼睛的3D空间方向都是唯一的，并且与眼睛如何到达该凝视方向无关。

Listing’s Law (Johann Benedict Listing 1808–1882)

列表法(约翰·本尼迪克特列表1808–1882)

Listing’s law states that all achieved eye orientations can be reached by starting from one specific “primary” reference orientation and then rotating about an axis that lies within the plane orthogonal to the primary orientation’s gaze direction. In other words, Donder’s Law tells us that the final orientation of the eye is independent of the path of eye movements, and Listing Law tells us what that orientation is.

列表法则指出，可以通过从一个特定的“主要”参考方向开始然后围绕与主要方向的视线方向正交的平面内的轴旋转来实现所有已实现的眼睛方向。 换句话说，唐德定律告诉我们，眼睛的最终方向与眼睛运动的路径无关，而《上市定律》告诉我们该方向是什么。

To visualize these laws scientists built sophisticated physical models, to study rotations of the eye and the action of the ocular muscles. The inventor of the first such device, Christian Georg Theodor Ruete, called it an “ophthalmotrope” (Fig. 1). Both Donder’s and Listing’s laws can be demonstrated on this model. The degree of muscle contraction or extension are measured on a scale at the back of the model. Other versions operated with suspended weights, to create muscle tension.

为了可视化这些定律，科学家建立了复杂的物理模型，以研究眼睛的旋转和眼肌的动作。 第一个此类设备的发明者Christian Georg Theodor Ruete称其为“检眼镜”(图1)。 唐德定律和列斯特定律都可以在该模型上得到证明。 肌肉收缩或伸展的程度在模型背面的刻度上进行测量。 其他版本使用负重进行操作，以产生肌肉张力。

Hermann von Helmholtz (1821–1894)

赫尔曼·冯·亥姆霍兹(1821-1894)

A unifying figure in the field was the polymath, Hermann von Helmholtz. Today, he is perhaps more widely known for his studies of electromagnetism, the Helmholtz wave equation⁶, and the Helmholtz theorems in fluid mechanics, but his comprehensive studies of physiological optics and ophthalmology had perhaps even greater impact⁷.

该领域的一个统一人物是多面手，赫尔曼·冯·亥姆霍兹。 如今，他可能以电磁学，亥姆霍兹波方程和流体力学中的亥姆霍兹定理的研究而广为人知，但是他对生理光学和眼科学的综合研究也许产生了更大的影响。

Helmholtz experimentally confirmed Listing’s law, comparing visual afterimages at various eye positions to Listing’s predictions. He invented of the ophthalmoscope, the familiar device doctors use to look into your eye. He was also the first to measure the speed of neural signals (which at the time, were thought to be instantaneous, like electricity).

亥姆霍兹(Helmholtz)通过实验证实了Listing的定律，将各个眼睛位置的视觉余像与Listing的预测进行了比较。 他发明了检眼镜 ，这是医生们用来观察眼睛的熟悉设备。 他也是第一个测量神经信号速度的人(当时，神经信号的速度被认为是瞬时的，就像电一样)。

His students are perhaps even more famous, including Heinrich Hertz and Nobel Prize winners Albert Michelson and Max Plank. Another of his students was Wilhelm Maximilian Wundt (1832–1920). While working in his lab, Wundt developed his skills in experimental methods and developed an advanced design of an ophthalmotrope. He established himself as a highly influential neurophysiologist. Wundt would go on to be the first person to call himself a “psychologist” and is often referred to as the “father of experimental psychology.” Wundt, in turn, trained a whopping 170 Ph.D. students over his career, intellectually colonizing two fields — neuroscience and psychology.

他的学生也许更为著名，包括海因里希·赫兹(Heinrich Hertz)和诺贝尔奖获得者阿尔伯特·米歇尔森(Albert Michelson)和马克斯·普朗克(Max Plank)。 他的另一个学生是威廉·马克西米利安·旺特(Wilhelm Maximilian Wundt，1832–1920年)。 在实验室工作期间，Wundt培养了他在实验方法上的技能，并开发了一种高级的检眼镜设计。 他确立了自己作为有影响力的神经生理学家的地位。 温特将继续成为第一个自称“心理学家”的人，通常被称为“实验心理学之父”。 反过来，Wundt则培训了多达170名博士。 学生在他的职业生涯中，在智力上殖民了两个领域-神经科学和心理学。

Hering’s Law (Karl Ewald Constantine Hering 1834–1918)

赫林定律(Karl Ewald Constantine Hering 1834–1918)

Hering’s Law of equal innervation states that eye movements are always equal in the two eyes, but not in direction. In conjugate eye movements (saccades and smooth pursuit), the eyes move equally together. For disjunctive movements (like vergence), the innervation is equal, but opposite. What this means is counterintuitive, but easy to demonstrate. Consider the task of refoveating both eyes on a new target (Fig. 5). The simplest solution would be to change the eye positions independently. But, the eyes instead move according to Hering’s Law, where both eyes move to the new visual direction, then in the opposite direction (vergence) to re-establish binocular vision. This was a formalization of the observations by Ptolemy and Alhazen was further evidence that the eye movements were constrained by some kind of neural control logic. Perhaps surprisingly, Hering’s law is violated during REM sleep, where most of the time the individual eye movements are more-or-less independent of each other. This contradicts the notion that dreams generate eye movements to visualize scenes, “unless each eye is experiencing a different dream⁸”(Fig. 6).

相等神经支配的赫林定律指出，两只眼睛的眼球运动总是相等的，但方向却不相等。 在共轭的眼球运动(扫视和平滑追踪)中，眼睛会同等运动。 对于析取运动(例如收敛)，神经支配是相等的，但相反。 这意味着违反直觉，但易于证明。 考虑一下将双眼移到新目标上的任务(图5)。 最简单的解决方案是独立改变眼睛的位置。 但是，眼睛会根据黑灵定律移动，即两只眼睛都朝新的视觉方向移动，然后朝相反的方向(收敛)移动以重新建立双目视觉。 这是托勒密(Ptolemy)的观察结果的形式化，而阿尔哈岑(Alhazen)进一步证明了眼睛运动受到某种神经控制逻辑的约束。 也许令人惊讶的是，在快速眼动睡眠期间违反了黑灵定律，在这种情况下，大多数情况下，各个眼睛的运动或多或少相互独立。 这与“梦产生眼动以可视化场景”的观点相矛盾，“除非每只眼睛都经历着不同的梦”(图6)。

As with many great scientists, Hering and Helmholtz were both colleagues and rivals. Helmholtz thought Hering’s Law was learned behaviour; Hering thought it was instinctual, or ‘hard-wired.’ Each independently derived the binocular horopter, the locus of points in space that have the same anatomical disparity on both retinas, or points of single vision (first described by Alhazen). Hering developed a theory of visual hyperacuity, showing how the resolution of an array of photoreceptors can exceed that of the size of an individual receptor. He also proposed the “opponent theory” of color vision (Helmholtz advocated the alternative, three-color receptor theory of Thomas Young and James Clerk Maxwell).

像许多伟大的科学家一样，Hering和Helmholtz都是同事和竞争对手。 亥姆霍兹认为黑灵定律是学会的行为。 Hering认为这是本能，或者是“硬连线”。 每个人都独立地得出双眼horopter，即在两个视网膜上具有相同解剖差异的空间点的位置，或者是单一视觉的位置(首先由Alhazen描述)。 Hering开发了一种视觉敏锐度理论，表明了一系列感光体的分辨率如何超过单个受体的分辨率。 他还提出了色觉的“对手理论”(Helmholtz提倡Thomas Young和James Clerk Maxwell的另一种三色受体理论)。

Sherrington’s Law (Charles Scott Sherrington 1857–1952)

谢灵顿定律(查尔斯·斯科特·谢灵顿1857–1952)

The last law of the 19th Century is Sherrington’s Law of Reciprocal Innervation, whereby action of the antagonist muscle is accompanied by reciprocal relaxation of the antagonist muscle. This essentially is a restatement of Descartes’ balloon theory in the context of modern neurobiology. He also introduced the term proprioception, to describe the sixth sense of kinaesthesia (“muscle sense”), leading to the discovery of sensory neurons that detect muscle stretching, tension, and velocity, such as the Golgi tendon organs and muscle spindles. Sherrington received the Nobel Prize for his work on neuron function, synaptic communication, and reflexes.

19世纪的最后一条定律是舍灵顿定律的往复神经定律，在此定律中，拮抗肌的作用伴随着拮抗肌的相互放松。 这本质上是在现代神经生物学的背景下重述笛卡尔的气球理论。 他还引入了本体感受一词来描述运动感觉的第六种感觉(“肌肉感觉”)，从而导致发现可检测肌肉拉伸，张力和速度的感觉神经元，例如高尔基腱器官和肌肉纺锤体。 谢灵顿因在神经元功能，突触沟通和反射方面的工作而获得诺贝尔奖。

Early 20th Century: Breakthroughs in Theoretical Biology

20世纪初：理论生物学的突破

More pieces of the puzzle came together in the mid-20th Century, with two crowning achievements of the physiology: (i) the Hodgkin-Huxley Model of nerve conduction (which, among other things, explains the biochemical process that governs the speed of neural signals measured by Helmholtz) and (ii) the Huxley Sliding Filament model of muscle contraction³, which also gives an explanation the force-velocity and length-tension relationships of muscle. The development of electrophysiological recording techniques allowed investigators to measure the signals generated by individual neurons.

在20世纪中叶，更多的难题汇聚在一起，在生理学上取得了两项最高成就：(i)神经传导的霍奇金-赫克斯利模型(除其他外，它解释了控制神经速度的生化过程) (Helmholtz测得的信号)和(ii)肌肉收缩的赫Sl黎滑动细丝模型³，这也可以解释肌肉的力-速度和长度-长度关系。 电生理记录技术的发展使研究人员能够测量单个神经元产生的信号。

Meanwhile, McCulloch and Pitts’ 1943 paper showed how networks of neurons could perform the same logical and mathematical operations as a computer. In 1949, Donald Hebb proposed the first rule for synaptic modification, showing how simple processes could be responsible for re-wiring networks with experience — thus ushering in a new field of computational biology and neural networks.

同时，McCulloch和Pitts在1943年发表的论文展示了神经元网络如何执行与计算机相同的逻辑和数学运算。 1949年，唐纳德·赫布(Donald Hebb)提出了突触修饰的第一条规则，展示了简单的过程如何负责重新连接具有经验的网络，从而开创了计算生物学和神经网络的新领域。

Cybernetics

控制论

Electrophysiology, combined with models of all the components (the mechanical plant, muscles, and neurons) offered the unique opportunity to study neuromuscular control at “systems” level. This allowed researchers to look farther back into the neural circuitry to understand how eye movement commands are planned, coordinated, executed in the brain.

电生理学与所有组件(机械植物，肌肉和神经元)的模型相结合，为研究“系统”级别的神经肌肉控制提供了独特的机会。 这使研究人员可以更深入地研究神经回路，以了解如何在大脑中计划，协调和执行眼球运动命令。

In 1948, Norbert Weiner defined this emerging field as Cybernetics as “the scientific study of control and communication in the animal and the machine”. His insight was that the huge arsenal of analytic methodologies developed for the analysis of signals and control systems (in electrical and mechanical engineering) could be applied to understand neurobiological control.

1948年，诺伯特·韦纳(Norbert Weiner)将这一新兴领域定义为控制论，即“对动物和机器中控制与通信的科学研究”。 他的见解是，为信号和控制系统(电气和机械工程)分析而开发的庞大分析方法库可用于理解神经生物学控制。

One of the first important results in cybernetics was the work of none other than my advisor, Larry Stark. Of course, the work was related to eye movements. He measured the time delay of neural feedback in the pupillary reflex, by inducing oscillations applications of frequency analysis and control theory⁹ ¹⁰10. Knowing the duration of the delay and the speed of neural signals helps pinpoint the location of the circuitry.

控制论的第一个重要成果就是我的顾问拉里·史塔克(Larry Stark)的工作。 当然，这项工作与眼球运动有关。 他通过诱导频率分析和控制理论⁹10的应用，测量了瞳Kong反射中神经反馈的时间延迟。 知道延迟的持续时间和神经信号的速度有助于查明电路的位置。

More were to follow, as each of the four types of extraocular eye movements had different latencies, indicating different upstream neural processing and separate control systems (VOR 50–100 ms, smooth pursuit 100–130 ms, vergence 160–180 ms, saccades 200 ms). Indeed, Hering’s Law implicitly suggested this. For example, when eyes begin to follow a target, the smooth pursuit system kicks in first, tracking direction and speed, followed by a corrective (“catch-up”) saccade to foveate on the target¹¹ (Fig. 7).

随之而来的还有更多，因为四种眼外运动的每种都有不同的潜伏期，表明不同的上游神经处理和独立的控制系统(VOR 50–100 ms，平稳追赶100–130 ms，发散度160–180 ms，扫视200多发性硬化症)。 确实，黑灵定律暗示了这一点。 例如，当眼睛开始跟随目标时，平滑跟踪系统将首先踢动，跟踪方向和速度，然后进行矫正(“追赶”)扫视以集中在目标上¹(图7)。

Contemporaries (notably David Robinson at Johns Hopkins) began to combine electrophysiology with control theory, to study individual neurons involved in planning and executing eye movements. This allowed the creation of quantitative, testable circuit diagrams of the control systems involved in generating saccadic, smooth pursuit, VOR, and vergence eye movements.

同时代人(特别是约翰·霍普金斯大学的戴维·罗宾逊)开始将电生理学与控制理论结合起来，研究参与计划和执行眼球运动的单个神经元。 这样就可以创建控制系统的定量，可测试的电路图，这些电路涉及产生generating声，平稳跟踪，VOR和发散眼动。

Robinson’s landmark work on saccadic feedback control¹² was performed on macaque monkeys — the same species subjected to Galen’s dissections. Another model he created (Figure 7) is one possible model of integrated smooth pursuit and VOR control, though it is by no means unique. These models suggest that eye movements are driven by feedback control systems, wherein the motor neurons are driven to minimize the error between the target velocity or position and the actual. Either this is a happy accident of using control theory to study the eyes, or testament to the efficiency of nature.

罗宾逊(Robinson)关于声调反馈控制的里程碑式工作是对猕猴进行的，猕猴是经过加伦(Galen)解剖的同一物种。 他创建的另一个模型(图7)是集成的平滑跟踪和VOR控制的一种可能模型，尽管它绝非唯一。 这些模型表明，眼睛运动由反馈控制系统驱动，其中运动神经元被驱动以最小化目标速度或位置与实际速度之间的误差。 这要么是使用控制理论来研究眼睛的大喜事，要么是自然效率的证明。

Several years after my lab rotation, I worked with another Electrical Engineering professor (and colleague of Robinson), Edward Keller, who was conducting research on the population behaviour of monkey brainstem neurons involved in the planning and execution of saccades. One region of the brain, the Superior Colliculus, maintains a spatial map not of the visual disparity or the geometric location, but of the error signal between the eye’s position and the target of interest (Fig. 9). Here, unlike with the motor neurons, it is the location of the neural activity, rather than its intensity, that determines the magnitude of the eye movement¹³. The efferent pathways downstream transform this spatial signal into a temporal control signal, which is required for the motor neurons.

实验室轮换几年后，我与另一位电气工程学教授(也是鲁滨逊大学的同事)爱德华·凯勒(Edward Keller)合作，他正在研究参与扫视计划和执行的猴脑干神经元的种群行为。 大脑的一个区域，即上丘囊，保持的空间图不是视觉差异或几何位置，而是眼睛位置和目标之间的误差信号(图9)。 在这里，与运动神经元不同，决定眼睛运动幅度的是神经活动的位置而不是强度。 下游的传出通路将该空间信号转换成运动神经元所需的时间控制信号。

Electrode recording of lower brain stem activity seemingly indicated that eye movements are executed before the subject’s awareness, stirring up debates about free will. A more comforting explanation is that the brain is constantly engaged in contingency planning for motor control.

电极记录下脑干活动似乎表明，在受试者意识到之前执行了眼球运动，激起了有关自由意志的争论。 一个更令人欣慰的解释是，大脑不断参与运动控制的应急计划。

So, What?

所以呢？

Scores of genetic, medical, and psychological disorders can be diagnosed from irregularities in eye movements¹⁴. At my alma mater, ocular motility is a required course for first year optometry students, for their potential to diagnose unknown medical conditions, such as strokes or brain tumours. Since most people never visit a neurologist, often the only opportunity for early detection is with an optometrist. Simple eye movement testing is also part of a general physical.

可以从眼球运动的异常情况中诊断出许多遗传，医学和心理疾病。 在我的母校，眼科运动是一年级视光学学生的必修课，因为他们有潜力诊断未知的医疗状况，例如中风或脑瘤。 由于大多数人从不去看神经科医师，因此，早期发现的唯一机会通常就是验光师。 简单的眼球运动测试也是一般身体检查的一部分。

The use of psilocybin effectively lowers the ‘gain’ of the positional feedback system, so subjects will move their eyes only 20% as much when viewing a scene. 60% of schizophrenics demonstrate involuntary nystagmus, a rapid jerking back and forth of the eyes. With heavy alcohol consumption, the smooth pursuit system begins to fail, and the eyes track instead with jerky eye movements (as revealed in the standard field sobriety test). Infants have the opposite response, only being able to produce tracking movements, but not saccades.

psilocybin的使用有效地降低了位置反馈系统的“增益”，因此，在观看场景时，被摄对象的眼睛移动幅度仅为20％。 60％的精神分裂症患者表现为非自愿性眼球震颤，眼睛来回快速跳动。 随着大量饮酒，顺滑的追踪系统开始失效，并且眼睛会随着眼球的动摇而跟踪(如标准的现场清醒测试所揭示的那样)。 婴儿的React相反，只能产生追踪动作，而不是扫视动作。

Try it out yourself, next time there is a new addition to the family. Amuse your friends or disturb the in-laws by testing baby’s eye movements. In the first six months, all you can elicit is tracking movements. But, no matter how much alcohol you give the baby, he will probably still pass a field sobriety test.

自己尝试一下，下次再增加一个新成员。 通过测试婴儿的眼球运动来逗您的朋友或打扰公婆。 在头六个月中，您所能获得的只是跟踪运动。 但是，无论您给婴儿喝多少酒，他都可能仍会通过现场清醒测试。

Do you still think eye movements are not interesting?

您是否仍然认为眼动并不有趣？

I give up. You’re just like my dad.

我放弃。 你就像我爸一样

= end =

=结束=

Russell Anderson has published several pseudo-histories of Science on Medium. He has a Bachelor’s in Electrical Engineering and Ph.D. in Bioengineering from the University of California. At least 5 of his professors conducted research on eye movements (Lawrence Stark, Ed Keller, Steve Lehman, Edwin Lewis, and Steven Heinen). He taught laboratory sessions to Larry Stark’s course on “Ocular Motility,” served as editor for Biological Cybernetics, and conducted postdoctoral research with Ed Keller at Smith-Kettlewell Eye Research Institute. After leaving academia, he has worked over 20 years building commercial predictive solutions at HNC Software, J.P. Morgan, Halifax Bank of Scotland, Opera Solutions, KPMG, and IBM… always with eye movements always on his mind.

罗素·安德森(Russell Anderson) 已发表了几本关于媒介科学的伪历史。 他拥有电气工程学士学位和博士学位。 加州大学生物工程专业。 他的教授中至少有5位对眼睛运动进行了研究(劳伦斯·史塔克，埃德·凯勒，史蒂夫·雷曼，埃德温·刘易斯和史蒂芬·海宁)。 他在拉里·史塔克(Larry Stark)的“眼动性”课程中教授实验室课程，并担任过生物控制论的编辑，并与史密斯·基特韦尔眼研究所的埃德·凯勒进行了博士后研究。 离开学术界后，他已经在HNC Software，JP Morgan，苏格兰哈利法克斯银行，Opera Solutions，KPMG和IBM等公司工作了20多年，致力于商业预测解决方案的开发工作……时刻都在关注着眼球运动。

Questions/Comments: anderson.transactionanalytics@outlook.com

问题/意见： anderson.transactionanalytics@outlook.com

1. Even for Berkeley, Dr. Stark was an eccentric. He was on the faculty in three, seemingly unrelated departments: Physiological Optics (School of Optometry), Neuroscience (UCSF), and Electrical Engineering (UCB). This, in spite of the fact that he did not have a Ph.D. himself. He got his MD at age 21, as part of a World War II acceleration program. He practiced medicine briefly in the Korean War, then landed in academia.

1.即使是大学伯克利分校，斯塔克博士是一个怪人。 他在三个看似无关的部门任教：生理光学(眼视光学学校)，神经科学(UCSF)和电气工程(UCB)。 尽管他没有博士学位。 他自己。 作为第二次世界大战加速计划的一部分，他在21岁时获得了医学博士学位。 他在抗美援朝中短暂地从事医学工作，然后进入学术界。

2. Bacon, F. (1561–1626). In: The Works of Francis Bacon. J Spedding, RL Ellis, DD Heath, editors. London. 1857 (page 628)

2.培根，F。(1561–1626)。 在： 弗朗西斯·培根作品 。 J Spedding，RL Ellis，DD Heath，编辑。 伦敦。 1857(第628页)

3. Cobb, M. (2002). “Timeline: Exorcizing the animal spirits: Jan Swammerdam on nerve function”. Nature Reviews Neuroscience. 3(5): 395–400.

3. Cobb，M.(2002)。 “时间轴：驱除动物精神：Jan Swammerdam的神经功能” 。 自然评论神经科学 。 3(5)： 395–400。

4. Huxley, A.F and Niedergerke, R. (1954). “Interference microscopy of living muscle fibres”. Nature. 173 (4412): 971–973

4. Huxley，AF和Niedergerke，R。(1954)。 “活肌纤维的干涉显微镜”。 大自然 。 173 (4412)：971–973

5. Martin, G.R. (2017). What drives bird vision? Bill control and predator detection overshadow flight. Frontiers in Neuroscience 11: 619.

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6. The Helmholtz Equation takes the form ∇² (f) = -k² * f , and has a wide range of applications to problems, such as spatial wave propagation and diffusion.

6.亥姆霍兹方程的形式为∇²( f) =-k²* f ，并且对于诸如空间波传播和扩散之类的问题具有广泛的应用。

7. Helmholtz, H. (1910). Treatise on Physiological Optics. New York: Dover

7. Helmholtz，H.(1910)。 生理光学论 。 纽约：多佛

8. Zhou, W. and King, W.M. (1997). Binocular eye movements not coordinated during REM sleep. Exp Brain Res 1997 117(1):153–60.

8. Zhou W.和King WM(1997)。 REM睡眠期间双眼运动不协调。 Exp Brain Res 1997 117(1)： 153-60。

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9.斯塔克，L。和谢尔曼，PM(1957年)。 自愿性瞳Kong对光反射的伺服分析研究。 J.神经生理学 20：17。

10.To a good approximation, the oculomotor can be modeled as a second-order, linear system. This is fortuitous, as there is even more complete mathematical theory that can be used for analysis. On the other hand, Professor Stark assured me, “God designed everything to look like a second order linear differential equation.”

10.可以很好地将动眼运动建模为二阶线性系统。 这是偶然的，因为甚至可以使用更完整的数学理论进行分析。 另一方面，斯塔克教授向我保证：“上帝设计的一切看起来都像二阶线性微分方程。”

11.Fuchs, A.C. (1967). Saccadic and smooth pursuit eye movements in the monkey. J. Physiol. 191, pp. 609–631

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12.达克罗宾逊(1981)。 控制系统分析在眼球运动神经生理学中的应用。 安 Rev. Neuroscience 4 ：463–503

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14.Srivastava, A., Ahmad, O.F., Pacia, C.F., Hallet, M. & Lungu, C. (2018). The Relationship between Saccades and Locomotion. Journal of Movement Disorders 11(3):93–106.

14. Srivastava，A.，Ahmad，OF，Pacia，CF，Hallet，M.＆Lungu，C.(2018)。 扫视与运动之间的关系。 运动障碍杂志 11(3)： 93-106。