|Year : 1993 | Volume
| Issue : 3 | Page : 117-120
Saccadic underaction in concomitant strabismus and Hering's law : a new neurophysiologic model for binocular motor correspondence
Pradeep Sharma, Prem Prakash, Vimala Menon
Dr. Rajendra Prasad Centre for Ophthalmic Sciences, New Delhi, India
Dr. R.P. Centre for Ophthalmic Sciences, All India Institute of Medical Sciences, New Delhi 110 029
Source of Support: None, Conflict of Interest: None
Hering's law of equal innervation has remained so far as an universal truth with no scientific basis. However, recent reports of Saccadic underactions in concomitant strabismus indicating asymmetric ocular motor innervation is in contradiction to the law. In an effort to understand the inequalities of binocular movements, we propose a neurophysiologic model for both normal and abnormal eye movements. The model hypothesizes that any binocular movement results from the yoking of two monocular reflex loops corresponding to the two eyes, during the plastic stage of development of ocular motor reflexes. The retinal target discrepancy triggers the reflex loop resulting in a monocular corrective movement. As there is a common binocular field, the stimuli to the two eyes are similar causing a similar binocular corrective movement. In abnormal cases coupling of asymmetric motor loops may occur resulting in alternate or unilateral saccadic underactions
Keywords: Saccadic underactions - Concomitant strabismus - Herin s law - Neurophysiologic model - Motor correspondence - Internuclear neurons para-abducens
|How to cite this article:|
Sharma P, Prakash P, Menon V. Saccadic underaction in concomitant strabismus and Hering's law : a new neurophysiologic model for binocular motor correspondence. Indian J Ophthalmol 1993;41:117-20
Since the time Hering enunciated that the movements of the two eyes are equal and symmetrical, it has been held as a universal truth with no scientific basis. , In our series of studies, we have observed inequality in the conjugate eye movements in the form of saccadic underactions in concomitant squint. , Such observations have also been reported by other investigators. , However, these observations cannot be reconciled by the analytic equation of Ono  or Rashbass and Westheimer.  In an attempt to understand this contradiction to Hering's law, we propose a neuro-physiologic model for the yoking of paired extraocular muscles in the plastic stage of development of ocular motor reflexes. The model not only provides a basis for Herin s law but also explains the observations of saccadic underactions in concomitant squint.
| Materials and methods|| |
The saccadic eye movements were studied by elect rooculography as described by Metz sub whereby voluntary refixation saccades and induced optokinetic nystagmus were recorded. Details of the materials and methods have been described previously. , Observations were made in 10 patients in each of the following groups: (1) essential alternating convergent squint; (2) unilateral concomitant convergent squint; and (3) lateral rectus palsy as a type of late onset paralytic squint. These observations were compared with the data in normal subjects which have been described in detail earlier.
| Observation|| |
The Phenomenon of Saccadic Underactions
Previous studies using electrooculargraphy have revealed saccadic underactions in concomitant convergent squints similar to those in paralytic squints but with certain differences. Though saccadic underactions have been described earlier, , they have been briefly reviewed in this article as they are basic to the understanding of the proposed new model.
In the essential alternators [Figure - 1], when the right eye fixated and left eye was occluded, the saccades of the occluded eye of both the horizontal recti showed underaction, whereas those of the fixating eye were of normal amplitude and velocity. The underactions completely reversed when the left eye fixated and the right eve was occluded. This has been described as alternate saccadic underaction, being of a reversible and reciprocal nature, such as alternate suppression seen in these cases.
In the case of unilateral (left, in this case) convergent squint [Figure - 2], the saccadic underactions were seen in the squinting (left) eye when the right eve fixated, whereas when the fixation was taken by the left eye, right eye being occluded there was no saccadic underaction of either eye. This suggests unilateral saccadic underaction of the squinting or nondominant eye.
This is in contrast to the observations of late onset paralytic convergent squint as in lateral rectus palsy (right, in the case) where there is always an underaction of the saccades by the paretic muscle (lateral rectus) irrespective of the change of fixation [Figure - 3]. The contralateral medial rectus shows overaction on fixation by paretic eye.
Similar observations of saccadic underactions have also been made by other investigators. ,
The Proposed Neurophysiologic Model of an Eye Movement
We propose that fundamentally any conjugate eye movement involves the yoking of two monocular reflex loops, each representing one eye. For example, a dextroversion movement entails a pairing of right abduction loop with left adduction loop [Figure - 4].
A reflex loop is initiated at the retina due to discrepancy of the retinal target. This stimulus travels to the ipsilateral cortex if initiated in the temporal retina and to the contralateral cortex if initiated in the nasal half of the retina due to the hemidecussation at chiasma. In effect, the impulse reaches the same side of the occipital cortex contralateral to the field of target in space. From here it travels to the frontomotor cortex and then down to the contralateral abducens nucleus subserving the lateral rectus to complete the abduction loop, or the contralateral internuclear neurons (para-abducens) which relate to the medial rectus of the opposite side through the medial longitudinal fasciculus (another hemidecussation) to complete the adduction loop. The monocular identity is thus maintained despite crossing of neural pathways from one side to the other, that is, an impulse initiated in the left eye culminates into the left extraocular muscles and that from the right eye culminates into the right extraocular muscles. The cortex directs the movement (saccades) to the opposite direction both in the ipsilateral and contralateral eye.
All horizontal eye movements are, in effect, a combination (yoking) of the basic four monocular reflex loops viz. (1) Right-Abduction reflex loop, (2) Right-Adduction reflex loop, (3) Left- Abduction reflex loop, (4) Left-Adduction reflex loop.
This "yoking" is flexible during the plastic stage of development of ocular motor reflexes. This is evident in the neonatal stage when the two eyes show incoordinated movements before the establishment of coordinated conjugate movements. These conjugate movements are 'conjugate' because the retinomotor value of the two loops in normal circumstances is the same. But in a hypothetical situation when the retinomotor value of the two loops is different for example, due to any sensory, optical, or motor obstacle, the two reflex loops will be coupled with unequal eye movements on the two sides. Thus, the eye movement though 'concomitant' would not be 'conjugate'; if such anomalies are repeated again and again, they get permanently yoked and would manifest permanently throughout life. This explains the saccadic underactions as observed by us , and others. ,
It is important to note that once coupled reflexes are not easily dissociated. Experiments with unequal stimuli to the two eyes could not dissociate the coupled reflexes as observed in four-prism diopter test. However, presumably a similar artifact during the formative plastic stage of development can effectively alter the retinomotor values and result in unequal saccadic movements on the two sides.
Evidence for the Model
(1) Double hemidecussation
The anatomical fact that hemidecussion occurs at the optic chiasma separating the nasal and temporal halves of one retina and blending them with temporal and nasal halves of the other to provide a unified right and left half of the visual field communicating with the contralateral sensory cortex, provides the substrate for binocular sensory correspondence.
The existence of internuclear neurons of the abducens indicates a similar hemidecussation in the motor pathways. This provides the substrate for binocular motor correspondence. The innervation from the contralateral frontomotor cortex gets segregated into two halves; one part going to the abducens motor neurons subserving the lateral rectus muscle to one side (contralateral to the cortex) and the other part going to the internuclear neurons of abducens (para-abducens) which relates through the medial longitudinal fasciculus to the medial rectus muscle of the opposite side (ipsilateral) to the cortex.
It has been observed that internuclear neurons do not receive any collaterals from the abducens motor neurons,  but instead from the frontomotor cortex in a manner similar to the abducens motor neurons. [12} Moreover, they are found to be excitatory and non-inhibitory in nature and therefore responsible for mediating the adduction of the contralateral eye in lateral gaze and also anterior internuclear ophthalmoplegia. It is apparently clear from these new findings that the nerve impulses from a motor cortex is channelised into contralateral lateral rectus (via the motor neurons) and the ipsilateral medial rectus(via the interneurons and medial longitudinal fasciculus).
Just as the right and left half of the visual fields relate to the contralateral sensory cortex, despite being received by the two eyes, the motor impulse from the motor cortex relates through contralateral abducens motor neurons and para-abducens internuclear neurons to the contralateral lateral rectus and ipsilateral medial rectus, respectively, to bring about a movement in the contralateral direction. The data being resifted in both situations by the two hemidecussations: optic chiasma for sensory impulses and internuclear neurons-medial longitudinal fasciculus for motor impulses. The two hemidecussations ensure the integrity of the monocular reflex loops.
(2) The evolution of binocularity
In the evolution of vision there has been a steady progression of events. The underlying neural apparatus being reorganised to meet the higher stereoptic visual need of a more highly evolved animal, the eyes for panoramic vision moved in toward the midline to provide for steropsis.  When the two eyes were located on the lateral sides, each functioned independently tQ the other indicating the possibility of a monocular neurophysiologic network. When the eyes moved in front they could no longer afford to be independent of each other because the stimuli for the two would have to be similar due to the overlap of visual fields. This provides the basis for the functional yoking of the adduction and abduction loops of the two sides. The reorganisation required in the evolutionary process is provided by the hemidecussation for it is a fact that animals with eyes on the lateral sides do not have chiasmatic hemidecussation but a total cross-over. On the evolutionary ladder there can be seen different grades of hemidecussation at the chiasma. A similar hemidecussation has come about at the abducens level in humans which has resulted in binocular motor correspondence. This finding has come to light only recently and comparative data in animals is not available to the best of our knowledge.
Development of Binocular Movements
The equal and symmetrical innervation of the paired extraocular muscles was a necessary outcome of the evolutionary progression of the eyes from the lateral sides to the front. Keiner  has mentioned about monocular adduction reflex and binocular abduction reflexes observed in neonates. Our understanding suggests the existence of monocular adduction as well as monocoular abduction reflexes. The combination of the four monocular adduction/abduction reflexes could result in the following horizontal binocular movements:
a. Dextroversion = right Abduction + left Adduction
b. Levoversion = left Abduction + right Adduction
c. Convergence = right Adduction + left Adduction
d. Asymmetric convergence of right side (b+c) (Right Adduction + right Adduction)+ (left Abduction + Left Adduction)
In the event of unequal retinomotor values of the two sides, unequal impulses in the two loops are expected to be coupled to give unequal but conjoined movements.
With our observations of alternate and unilateral saccadic underactions in alternators and unilateral convergent squints, experimental evidence of the existence of separate motor pathways through abducens motor neurons and internuclear neurons along with the observation of incoordinate movements in the neonates, we hypothesise the concept of monocular adduction and abduction reflex loops.
We further propose that yoking of adduction and abduction reflex loops with equal retinomotor values on the two sides result in concomitant movements, but when the retinomotor values are unequal, the two loops get yoked with unequal movements in the plastic stage of development and results in saccadic underactions.
| References|| |
Hering E. Theory of Binocular Vision, 1869, translated by Bridgeman B & Stark L, Plenum Press, New York, 1977.
Westheimer C. Pathological physiology of binocular parallelism. In The Functional Basis of Ocular Motility Disorders, Lennerstand C, Zee DS, and Keller EL (Eds). Pergamon Press, Oxford, 195-197, 1982.
Prakash P, Sharma P, Menon V, and Gahlot DK. The phenomenon of alternate saccadic underactions in essential alternating convergent squint. Trans Asia Pacific Acad Ophthalmol. (Hongkong), March. 774-782, 1983.
Sharma P, Prakash P, Menon V, and Gahlot DK, Saccadic underactions in concomitant convergent squint. Ind Jour Ophthal, 34: 461-466, 1984.
Mitsui Y, Hirai K, Takashima 1, and Masuda K.EOG of squint and its relation to the etiology of squint. Acta Soc Ophthalmol Jpn. 81(11): 1987-94, 1977.
Qure MA. La dominance anormale de loeil fixatour dons les exotropics functionalles. Arch Ophthalmol.(Paris): 32: 382-392, 1972.
Ono H. The combination of version and vergence in Vergence Eye Movements: Basic and Clinical Aspects.Scher CM, and Ciuffreda KH (eds). Butterworths, Lon don. 373-400, 1983.
Rashbass C, and Westheimer G. Independence of conjugate and disjunctive eye movements J Physiol. 159: 361 364, 1961.
Metz HS, Scott AB, and Omeara D.Ocular Saccades inlateral rectus palsy, Arch. Ophthalmol,84: 453-400,1984.
Prakash P, Sharma P, and Menon V, A Study of saccadic eye velocity, Afro Asian J Ophthalmol. 9: 54-57, 1990.
Baker R, and Highstein SM. Physiological identification of interneurons and motorneurons in the abducens nucleus. Brain Res, 91: 292-298, 1975.
Cohen B. The vestibulo ocular relations. In The Control of Eye Movements. Bach-y-Rita. P and Collins CC (eds). Academic Press, New York. 105-148, 1971.
Duke-Elder S. The Eye in Evolution. Vol.1, System of Ophthalmology. Henry Kimpton, London, 698-700 1958.
Keiner BJ. New Viewpoints on the Origin of Squint. Martinus Nizhoff, The Hague, 1951.
[Figure - 1], [Figure - 2], [Figure - 3], [Figure - 4]