Law Of Equal Innervation Research Articles

Monocular microsaccades are visual-task related.

During visual fixation, we constantly move our eyes. These microscopic eye movements are composed of tremor, drift, and microsaccades. Early studies concluded that microsaccades, like larger saccades, are binocular and conjugate, as expected from Hering's law of equal innervation. Here, we document the existence of monocular microsaccades during both fixation and a discrimination task, reporting the location of the gap in a foveal, low-contrast letter C. Monocular microsaccades differ in frequency, amplitude, and peak velocity from binocular microsaccades. Our analyses show that these differences are robust to different velocity and duration criteria that have been used previously to identify microsaccades. Also, the frequency of monocular microsaccades differs systematically according to the task: monocular microsaccades occur more frequently during fixation than discrimination, the opposite of their binocular equivalents. However, during discrimination, monocular microsaccades occur more often around the discrimination threshold, particularly for each subject's dominant eye and in case of successful discrimination. We suggest that monocular microsaccades play a functional role in the production of fine corrections of eye position and vergence during demanding visual tasks.

Binocular coordination of eye movements – Hering’s Law of equal innervation or uniocular control?

The neurophysiological basis for binocular control of eye movements in primates has been characterized by a scientific controversy that has its origin in the historical conflict of Hering and Helmholtz in the 19th century. This review focuses on two hypotheses, linked to that conflict, that seek to account for binocular coordination - Hering's Law vs. uniocular control of each eye. In an effort to manage the length of the review, the focus is on extracellular single-unit studies of premotor eye movement cells and extraocular motoneurons. In the latter half of the 20th century, these studies provided a wealth of neurophysiological data pertaining to the control of vergence and conjugate eye movements. The data were initially supportive of Hering's Law. More recent data, however, have provided support for uniocular control of each eye consistent with Helmholtz's original idea. The controversy is far from resolved. New anatomical descriptions of the disparate inputs to multiply and singly innervated extraocular muscle fibers challenge the concept of a 'final common pathway' as they suggest there may be separate groups of motoneurons involved in vergence and conjugate control of eye position. These data provide a new challenge for interpretation of uniocular premotor control networks and how they cooperate to produce coordinated eye movements.

Japanese street performer mimes violation of Hering's Law

Mime artists often use movement to imply the breaking of physical laws: suitcases levitate, air becomes as impermeable as glass. We present the simulated (and actual) violation of a physiologic principle, Hering's Law of Equal Innervation. To provide stereopsis while avoiding double vision, the movements of forward-facing primate eyes must be closely coordinated. In a 19th-century debate, Helmholtz contended that this coordination is a learned process, taming naturally independent eyes. Hering, meanwhile, believed the eyes to be inherently reined to each other and driven by a single control signal.1 Hering's view predominated and this final common pathway for horizontal eye movement came to be accepted as a unilateral signal to the abducens nucleus. This directly controls the lateral rectus of the ipsilateral, abducting, eye but also necessarily adducts the other eye, via interneurons to the contralateral oculomotor nucleus. More recent neurophysiologic evidence, however, indicates that primate saccadic commands can be encoded monocularly,2 in common with the laterally mounted, independently moving eyes of our distant evolutionary forebears. Binocular coordination might therefore not arise as a necessary consequence of neuroanatomic connectivity. If so, it might be possible to execute voluntary monocular saccades. We present a case of a …

Pioneers of eye movement research.

Recent advances in the technology affording eye movement recordings carry the risk of neglecting past achievements. Without the assistance of this modern armoury, great strides were made in describing the ways the eyes move. For Aristotle the fundamental features of eye movements were binocular, and he described the combined functions of the eyes. This was later given support using simple procedures like placing a finger over the eyelid of the closed eye and culminated in Hering's law of equal innervation. However, the overriding concern in the 19th century was with eye position rather than eye movements. Appreciating discontinuities of eye movements arose from studies of vertigo. The characteristics of nystagmus were recorded before those of saccades and fixations. Eye movements during reading were described by Hering and by Lamare in 1879; both used similar techniques of listening to sounds made during contractions of the extraocular muscles. Photographic records of eye movements during reading were made by Dodge early in the 20th century, and this stimulated research using a wider array of patterns. In the mid-20th century attention shifted to the stability of the eyes during fixation, with the emphasis on involuntary movements. The contributions of pioneers from Aristotle to Yarbus are outlined.

Phoria adaptation as a mechanism for maintaining good binocular coordination in normal subjects

Papers written about phoria adaptation often discuss the modification of eye alignment as evidence for mechanisms that compensate for changes in the oculomotor system due to development, disease and injury. While clinicians often encounter patients with diplopia or other signs of ocular misalignment, most people, in fact, have nearly perfect eye alignment even when viewing far targets with one eye occluded. Evidence that good eye alignment is the result of adaptive mechanisms can be seen with the binocular misalignment that results from the monocular patching of one eye in normal subjects for extended periods of time. We have tested extensively the ability of subjects to adapt the alignment of their eyes in various viewing conditions that present binocular disparities in the context of different version, vergence and head postures. Our conclusion from these studies is that one of the primary functions of phoria adaptive mechanisms is to manage the parsing of extraocular muscle forces during everyday viewing situations. The concept of Hering’s law of equal innervation is an oversimplification of a very complex process in which the relative participation of the twelve extraocular muscles needs to vary with the distance and eccentricity of the object of interest as well as the pitch and roll angles of the head. We note also that the problem of maintaining good coordination of the eyes is exacerbated with dynamic eye and head movements. I will review our work on the adaptation of vertical phoria and cyclophoria in relation to orbital eye position and head posture.

Incomitance of ocular rotation axes in trochlear nerve palsy.

Strabismus due to palsy of a single muscle in one eye is always incomitant, which is a consequence of Hering's law of equal innervation. We asked whether this law had similar consequences on the orientation of ocular rotation axes. Patients with unilateral trochlear nerve palsy were oscillated about the nasooccipital (= roll) axis (+/-35 degrees, 0.3 Hz), and monocularly fixed on targets on a head-fixed Hess screen. Both the covered and uncovered eyes were measured with dual search coils. The rotation axis of the covered eye (paretic or healthy) tilted more nasally from the line of sight when gaze was directed toward the side of the healthy eye. The rotation axis of the viewing eye (paretic or healthy), however, remained roughly aligned with the line of sight. We conclude that incomitance due to eye muscle palsy extends to ocular rotation axes during vestibular stimulation.

Simulation of oculomotility in craniosynostosis patients

Craniosynostosis syndromes can be associated with missing extraocular muscles, or muscles with abnormal insertions, and so provide useful test cases for assessing our understanding of the mechanics of the extraocular muscles. Patient with craniosynostosis syndromes often show eye movements in which a horizontal movement by one eye is accompanied by upshoot or downshoot in the other eye.An hypothesis which has been put forward to explain these movements is that the muscles in the patients are excyclorotated and that the upshoots and downshoots follow directly from the application of Hering’s law of equal innervation. We modelled the mechanics of the excyclorotated muscles and verified this hypothesis. However, excyclorotation of the orbit often occurs in combination with anomalous muscle anatomy in craniosynostosis syndromes. In keeping with this finding, we have found that surgical transposition of the rectus muscles is insufficient by itself to correct the anomalous eye movements, but that transposition in combination with weakening of the obliques is effective.

Neural basis of disjunctive eye movements.

New evidence has challenged a widely accepted interpretation of Hering's law of equal innervation, which states that disjunctive saccades are produced by the linear addition of conjugate and vergence innervation commands produced by independent oculomotor subsystems. We hypothesize, instead, that saccades are produced by a monocular premotor control network. A model, based on this hypothesis and consistent with known brain-stem anatomy, simulates realistic disjunctive saccades including initial and late slow vergence movements.

Premotor commands encode monocular eye movements.

Binocular coordination of eye movements is essential for stereopsis (depth perception) and to prevent double vision. More than a century ago, Hering and Helmholtz debated the neural basis of binocular coordination. Helmholtz believed that each eye is controlled independently and that binocular coordination is learned. Hering believed that both eyes are innervated by common command signals that yoke the eye movements (Hering's law of equal innervation). Here we provide evidence that Hering's law is unlikely to be correct. We show that premotor neurons in the paramedian pontine reticular formation that were thought to encode conjugate velocity commands for saccades (rapid eye movements) actually encode monocular commands for either right or left eye saccades. However, 66% of the abducens motor neurons, which innervate the ipsilateral lateral rectus muscle, fire as a result of movements of either eye. The distribution of sensitivity to ipsilateral and contralateral eye movements across the abducens motor neuron pool may provide a basis for learning binocular coordination in infancy and adapting it throughout life.

Hering's law and eyebrow position.

A patient with bilateral but asymmetrical brow ptosis is presented in whom the frontalis action on the relative position of the eyebrows could be demonstrated to obey Hering's law of equal innervation. The neurological basis for this finding is discussed, along with the implications for the surgical management of brow ptosis.

Binocular eye movements not coordinated during REM sleep.

Rapid eye movements (REMs) are a defining characteristic of REM sleep during which vivid dreams occur. It has been suggested that REMs may be binocularly coordinated and related to "watching" dream images. For the first time, binocular eye movements were recorded during natural REM sleep in monkeys to test the conjugate nature of the oculomotor system and the "scanning hypothesis" of REMs during sleep. During REM sleep, the lines of sight of the two eyes are frequently misaligned up to 30 degrees horizontally and/or vertically. Since the lines of sight usually don't intersect, there is no fixation point. Instead, each eye is aimed at a different part of the visual field during REM sleep. Furthermore, REMs are not usually conjugate, but are disjunctive or even monocular in horizontal or vertical directions. These data argue against the idea that REMs actually "track" dream images, unless each eye is watching its own dream! Binocular misalignment and disjunctive (even monocular) REMs during sleep suggest that separate left eye and right eye pathways generate saccades in each eye and control the position of each eye. Binocular coordination cannot be the passive result of anatomical connectivity as has been argued previously, but instead must result from a high-level process associated with the awake state that coordinates activity in left-eye and right-eye pathways. Hering's law of equal innervation is not consistent with these data.

Slow-velocity Asymmetrical Convergence: A Decisive Failure of “Hering's Law”

With targets aligned in the midsagittal plane, six of seven subjects tested were often able to make smooth symmetrical convergence movements in which no detectable saccade occurred during the initial 300 msec of the eye movement (12–95% of their trials). With targets located in a plane parallel to, but appreciably to one side of the midsagittal plane, those same six subjects were also often able to make smooth, slow, “saccade-free” asymmetrical convergence movements that were appropriate in magnitude and velocity to the target location (ratio of excursions about 2 to 1). Vergence movements are thus more versatile than can be accounted for by a single generator of binocularly symmetrical input to the eye muscles (Hering's Law of Equal Innervation). The occurrence of “saccade-free” asymmetrical convergence suggests instead that during binocular viewing, each eye can respond independently to that eye's view of the target, resulting in binocularly simultaneous slow-velocity nasalward eye movements—which will represent symmetrical or asymmetrical convergence depending on the arrangement of the targets. A similar interpretation is also apparently demanded by recent data on the initiation of disjunctive smooth-pursuit movements in the monkey [King and Zhou (1995)Vision Research, 35, 3389–3400]. Copyright © 1996 Elsevier Science Ltd.

Some observations on abduction nystagmus in internuclear ophthalmoplegia

The findings in 220 consecutive patients with internuclear ophthalmoplegia (INO) investigated by direct-current electro-oculography (EOG) are reported. Abduction nystagmus is significantly more frequent in patients with severe INO and increases with increasing lateral movements in the direction of the paretic medial rectus muscle. In a series of 12 unselected patients, additional recordings were made immediately after patching the paretic eye, and in six of them also immediately after patching the non-pa-retic eye. Patching the paretic eye was followed by a decreased pulse-step mismatch and a decreased pulse duration causing decreased amplitudes of abduction and adduction saccades in most patients. Patching the non-paretic eye was followed by an increased pulse-step mismatch and an increased pulse duration causing increased amplitudes of abduction and adduction saccades in most patients. The author's findings support the adaptation hypothesis of abduction nystagmus in most patients with INO, and are in accordance with Hering's law of equal innervation. The increased innervation is adjusted to the adduction paresis and generated immediately after onset of the paresis. Abduction nystagmus in INO depends on the medial rectus paresis and presumably is initiated by a visual error signal.

Are laws that govern behavior embedded in the structure of the CNS? The case of Hering's law

The pattern of axonal terminations of individual premotoneuronal medium lead burst neurons (MLBs) has been elucidated with the help of the intraaxonal recording and horseradish peroxidase injection technique in alert behaving monkeys. These findings indicate that individual MLBs do not influence individual muscles; instead they influence groups of muscles. Horizontal medium lead burst neurons (EBNs) project to ipsilateral lateral rectus motoneurons directly, and could contact contralateral medial rectus motoneurons indirectly, through the internuclear neurons of the ipsilateral abducens nucleus. Also, upward MLBs project to motoneurons innervating both the superior rectus and the inferior oblique muscles of both eyes. Finally, downward MLBs project to ipsilateral motoneurons innervating the ipsilateral inferior rectus muscle and the contralateral superior oblique muscle. All in all, the pattern of oculomotor terminations of MLBs provides experimental support for Hering's law of equal innervation. EBNs also project to the nucleus prepositus hypoglossi while vertical MLBs also project to the interstitial nucleus of Cajal (NIC). These structures are thought to participate in the process of “velocity to position integration”, in the horizontal and vertical planes respectively. Intracellular recording from individual neurons of the NIC in alert behaving monkeys followed by biocytin or horseradish peroxidase injections demonstrates that their axons pass through the posterior commissure on their way to vertical extraocular motoneurons. It also demonstrates that these fibers carry a phasic signal related to saccades and a tonic signal related to eye position in a precise quantitative manner. Work is in progress to determine whether their pattern of oculomotor terminations is also appropriate for Hering's law.

Initiation of disjunctive smooth pursuit in monkeys: Evidence that Hering's law of equal innervation is not obeyed by the smooth pursuit system

Monkeys generated disjunctive smooth pursuit eye movements when they tracked visual targets that moved toward or away from them. Eye acceleration was computed during the initial 100 msec of pursuit (the open-loop interval) for various target trajectories. The initial acceleration of either eye was a function of the target's motion with respect to that eye, regardless of whether or not the pursuit was conjugate or disjunctive, or performed with one eye occluded. Eye movements produced by fusional vergence could be separated temporally from eye movements produced by smooth pursuit using step-ramp paradigms. The separation of the two responses demonstrates that the fusional vergence system operates in parallel with the smooth pursuit system, presumably to minimize disparity, but not to generate disjunctive components of smooth pursuit eye movements.

Accommodative Vergence and Hering's Law of Equal Innervation -II-

Accommodative Vergence and Hering's Law of Equal Innervation -II-

The Role of Ocular Muscle Proprioception in Visual Localization of Targets

The role of ocular muscle proprioception in the localization of visual targets has been investigated in normal humans by deviating one eye to create an experimental strabismus. The passively deviated eye was covered and the other eye viewed the target. With a hand-pointing task, targets were systematically mislocalized in the direction of the deviated nonviewing eye. A 4- to 6-degree error resulted when the nonviewing eye was offset 30 degrees from straight ahead. When the eye was deviated, the perceived "straight-ahead" was also displaced, by a similar amount, in the same direction. Since the efferent motor commands to the displaced and to the nondisplaced eyes are presumably identical by the law of equal innervation, the mislocalization of visual objects must be attributed to the change in proprioceptive information issued from the nonviewing, deviated eye. Thus proprioception contributes to the localization of objects in space.

Accommodative Vergence and Hering' Law of Equal Innervation

Accommodative Vergence and Hering' Law of Equal Innervation

Abduction nystagmus in internuclear ophthalmoplegia.

We tested the hypothesis that abnormalities of the abducting eye in internuclear ophthalmoplegia reflect an adaptive process that helps overcome the adduction weakness of the opposite eye. This response operates under the constraints of Hering's law of equal innervation: any attempt to increase the innervation to a weak muscle in one eye must be accompanied by a commensurate increase in innervation to the yoke muscle in the other eye. In 4 patients with internuclear ophthalmoplegia, we patched one eye for 1 to 5 days to allow time for the central nervous system to optimize innervation for the habitually viewing eye. We predicted that there would be a conjugate adjustment of innervation that would diminish the abduction overshoot and backward postsaccadic drift made by the habitually viewing eye. This was the case in 3 of our 4 patients. Our findings show that the abduction nystagmus is a manifestation of a normal adaptive response in some patients with INO.

Extreme eye position and Hering's law of equal innervation.

La loi de Hering sur la variation de la position horizontale extreme de l'œil en fonction de la distance de vue est mise a l'epreuve par des mesures objectives et subjectives maintenant constante ou faisant varier l'elevation de l'eil