eye and head movements of visually impaired children

EYE AND HEAD MOVEMENTS OF VISUALLY IMPAIRED CHILDREN

J. E. Jan K. Farrell P. K. Wong A . Q. McCormick

Eye and head movements are controlled by several supranuclear centres, resulting in one of the most complex systems in the body (Gay et al. 1974, Leigh and Zee 1982). However, visual input is needed to maintain the normal performance of all classes of eye movements (Leigh and Zee 1980, Lindstedt 1982). Furthermore, Wiesel (1982) concluded that ‘innate mechanisms endow the visual system with highly specific connections but visual experience early in life is necessary for their maintenance and full development. Deprivation experiments demonstrate that neural connections can be modulated by environmental influence during a critical period of post-natal development’.

In visually impaired children a certain relationship exists between eye and head movements on the one hand and the onset, type and severity of visual loss on the other. Because of this, their neurological examination can be most rewarding. Little attention has been paid to this relationship in the paediatric literature and often the opinions of physicians are conflicting. For example Moore and Taylor (1984) described three children with the diagnosis of congenital retinal dystrophy and saccade palsy. They considered this syndrome to be a subset of Leber’s amaurosis, but we believe that the oculomotor disorders in two of their

patients are similar to those seen in any child with marked congenital visual loss.

The purpose of this article is to describe fixation, nystagmus, pursuit, rapid voluntary and other types of eye movements, associated head movements and head position of visually impaired children with congenital and acquired visual loss due to disorders of the eye and visual cortex.

Patients and methods The prospective study included all children referred since 1980 to the Visually Impaired Program at the Children’s Hospital, Vancouver, B.C. The methods of referral and evaluation are reported elsewhere (Jan et al. 1973). 256 children with congenital visual impairment, 46 with acquired visual loss and 45 with permanent cortical visual impairment, were studied (Tables I to 111). Patients who had progressive ocular disorders were not included because the onset of visual loss could not be determined accurately. Children without ocular lesions who were diagnosed as having motor nystagmus were also excluded.

All children were fully evaluated by a multidisciplinary team including a paediatric neurologist and ophthalmologist. The parents were carefully interviewed regarding their children’s visual be-

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TABLE I Roving and nystagmus in congenital ocular visual impairment (N = 256)

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Roving and Sustained Roving sustained nystagmus No N Children

Visual loss only nystagmus only nystagmus examined

- 14 34

Severe - 32 34 - 66 20/200 - 2 66 - 68 20/200-20/70 - - 22 10 32 Better than 20/70 - - 2 40 42

- - Total blindness 14 - - - Light perception 34

haviour since birth. When children were able to co-operate, distance visual acuity was tested by the STYCAR Panda Test (Sheridan 1973). If they were too young or too handicapped, their vision was estimated by playing with them for 15 to 20 minutes and thereby obtaining an idea of how well they could see. All team members made observations which were then discussed.

The children were made to fixate for a few seconds on a colourful five- to six- inch toy, a light or a human face. When nystagmus was present its amplitude and frequency were noted in the null position. The children were also requested to follow an object moving slowly and smoothly across their visual field in different directions. The range and fluency of eye and associated head-pursuit movements were noted. The lateral conjugate eye- movements were considered normal when the limbus (the border of the cornea and the sclera) became hidden under the medial and lateral canthus. Vertical upward gaze was considered normal when it reached about 30" of elevation. Following this, the fast voluntary eye-movements (saccadic system) were tested. The older children were asked to look rapidly on command from one object to another, while the younger children were shown interesting toys in various positions. Again, the range and fluency of eye and associated head-movements were described. Fewer than one-quarter of these children were so developmentally delayed and or unco-operative that the examination was difficult.

noeuvre was done as children were focusing on an object and their heads were turned at various speeds, thus revealing the strength of fixation.

Total blindness was defined as complete lack of sight. Light perception was diagnosed when a child could distinguish light from darkness but could not perceive shapes and could not reach for a visual cue. Profound visual impairment was defined as visual acuity better than light perception but worse than 201200 (6/60) vision in the better eye, even with correction (this is the definition of legal blindness in North America). Sensory nystagmus was diagnosed when conjugate oscillations of the eyes were seen, associated with visual loss and elicited by attempts at fixation. Nystagmus con- sisting of more than three or four beats was called sustained. Roving or drifting eye-movements were defined when the eyes shifted slowly and aimlessly back and forth, without attempts at fixation, usually horizontally. These movements were different from the normal but otherwise purposeless eye-movements of visually inattentive children. Oculomotor problems were diagnosed when the eye movements lacked smoothness and were poorly co-ordinated. 'Null position' indicated the position of gaze with least nystagmus.

Results Roving and sensory nystagmus Roving eye-movements were observed in children with vision worse than 20/200. Sensory systagmus was a sign of useful

286 The oculoceDhalic (doll's head) ma- vision and tended to be &resent when

distance visual acuity in the better eye was worse than 20170 (Table I). Sensory nystagmus developed when the visual loss occurred under 12 to 13 months of age. Furthermore, roving and sustained nystagmus were seen only in children with disorders of the anterior visual pathway. Occasional beats of nystagmus were observed in 12 of 45 patients with permanent cortical visual impairment. These children had co-existent damage to the anterior visual pathway since birth or acquired a visual loss under one year of age. Factors which influence sensory nystagmus are shown in Table IV.

Most parents of legally blind children were able to recall that their infants exhibited roving eye-movements within two to three weeks of birth, and sometimes even hours after birth. Roving gradually disappeared between two and 12 months of age in most children who developed useful vision, but it continued indefinitely in those with no vision or only light perception. The earlier roving subsided the more vision the children had. In many infants roving could be replaced temporarily with sustained coarse nystagmus when a colourful object was brought close enough to their eyes. New- borns’ roving was not always conjugate. Sensory nystagmus was never observed by the parents or by us during the first two weeks of life, but gradually appeared between one and 12 months of age. Earlier onset generally was indicative of more useful vision. The gradual dis- appearance of roving and the onset of sensory nystagmus were closely related to the development of visual acuity. Al- though the vast majority of infants were thought at first to be totally blind, 65 per cent of them eventually developed useful sight. Parent interviews and follow-up examinations indicated that the most marked improvement in visual function- ing was observed during the first 1 ?h years of life, although a lesser degree of improvement occurred through the pre- school years. Infants who were able to fixate even momentarily during the neonatal period or shortly afterwards always had enough vision to read print by the time they entered school. In infancy, fixation was better obtained by the human face than by a light source. When ocular

TABLE I1 Acquired visual impairment with known onset RJ - 46)*

~~~

Etiology -

N

Optic-nerve glioma Battering Shunt failure Craniopharyngioma Optic neuritis Uveitis Miscellaneous

*All but three children are legally blind.

TABLE 111 Permanent cortical visual impairment (N-45)

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Occasional

Onset Fundus nystagmus nystagmus No beats

- Congenital Normal 13 Abnormal 8 5

Under 1 yr Normal 5 Abnormal 1 I

Over 1 yr Normal 1 Abnormal 5 -

Total 33 12

-

-

visual loss was acquired under one year of age, nystagmus usually appeared two to four weeks later.

Pursuit movements The smoothness of pursuit movements of children with congenital visual impairment was related to the severity of visual loss. Pursuit became more clumsy and jerky with diminishing sight. Children with vision better than 20/200 followed mainly with their eyes. Those with 20/200 vision followed with both eye and head movements and those with severe visual impairment followed mainly by turning their heads, even struggling if restrained. Pursuit was not seen in patients with only light perception. Some children with more severe visual loss had difficulty in following an object upward but not downward or sideways. Children who became visually impaired after the age of one year had much less difficulty with pursuit,

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TABLE IV Factors influencing sensory nystagmus

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Age at visual loss

Age of child Severity of visual loss

Direction of gaze Type of visual loss Neurological state

Physiological status Drugs Attempts at fixation Emotional states Intelligence Tiredness Correction of refractory errors Ocular disorders

Not present when sudden visual loss occurs after 12-13 months of age. Con- genital and acquired visual impairment in early infancy causes more marked nystagmus than when loss of sight occurs later during the first year of life. Diminishes with age, rarely disappears. Not present in cases of total blindness, unilateral ocular disorders or when visual loss is minimal (<20/50-70). Severity of visual loss during the first year of life determines the degree of nystagmus. Onset of nystagmus is later when visual loss is severe. Decreases in null point (position of relative rest). Only central visual loss is associated with sensory nystagmus. Diminished or absent with associated cortical or cerebral blindness. May be absent in children with uncontrolled seizures, such as infantile spasms, or in coma. Absent in sleep, decreased with eyes closed. Diminished with phenobarbitol, sedatives, cycloplegics. Sustained nystagmus results from visual fixation. Increased by anxiety, happiness, excitement. Inquisitive infants fixate earlier than retarded children. Often increased. May increase or decrease nystagmus, depending on age of the child. Often more marked in children with photophobia.

TABLE V Voluntary upward gaze of children with congenital visual impairment (N = 165)

Minimal Marked Visual loss Normal limitation limitation N

Total blindness or light perception only - - 42 42

Severe 1 23 21 45 201200 12 33 3 48 Better than

30 - 201200 26 4

288

unless they had little or no useful vision. Those who acquired a visual impairment during the first six months had clumsier eye-movements than those who became blind during the second six months of life. Many children with cortical visual impairment paid little or no attention to visual stimuli, but when they had residual sight their pursuit movements tended to be smooth. They did not appear to be 'blind', so frequently the diagnosis was delayed.

Voluntary rapid eye-m o vemen ts Voluntary rapid (saccadic) eye-movements were affected by the severity of congenital ocular visual loss. Patients with total blindness were unable to move their eyes in any suggested direction. Those with severe congenital visual impairment moved their eyes in a jerky fashion horizontally and downward, but rarely more than a few degrees upwards (Table V). Occasionally one eye moved up slightly higher than the other (usually the better eye). Two congenitally visually impaired children had been investigated for a tumour before they were evaluated in our program because of their limited upward gaze. Associated head-movements were also seen, as described with pursuit. Children whose visual acuity was better than 20/70 had normal eye- movements. Patients who lost their sight after the age of one year had normal voluntary fast eye-movements, unless they had little or no useful sight. Those with permanent profound cortical blindness exhibited normal involuntary fast eye-movements. When they had useful sight, the voluntary fast saccades were also normal.

TABLE VI Head positions of visually impaired children (N = 296)’

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Congenital ocular Acquired ocular Cortical Little or Little or Little or no useful Useful no useful Useful no useful Useful

vision vision vision vision vision vision ~ ~~ ~

Head up 4 156 3 22 5 23 6 Head down 38 -

1 Variable 10 24 3 Total 52 180 12 22 6 24

- 1 - - -

*Excluding those who lacked head control.

00’ N

Head position The head positions of children with congenital and acquired ocular disturb- ance and permanent cortical visual impairment are shown in Table VI.

Oculocephalic (doll’s head) manoeuvre As children wzre looking at an object, their heads were moved sideways by the examiner at varying speeds. When the visual impairment was severe, even gentle slow turns broke the fixation. As vision improved, brisker head turns were necessary to dislodge fixation. When distance visual acuity was 20/70 or better, fixation was not interrupted. This was sometimes a difficult test to do in children with severe mental retardation or with cortical visual impairment, because their attention span was so short that they rarely fixated on objects for long enough.

Discussion Visual maturation is an important factor in understanding the eye and head movements of visually impaired children. Dobson and Teller (1978) concluded that the increase in visual acuity in postnatal life, as demonstrated by clinical observations, optokinetic nystagmus, preferen- tial looking and visual evoked potentials, probably reflects the neuronal maturation of the visual pathway. The vision of normal neonates who lack visual experience is so impaired that it is close to legal blindness. In fact it has been postulated that the visual performance of newborn infants depends on peripheral rather than central vision (Bronson 1974). PeriDheral acuitv develoDs dramaticallv in

the first months of life and reaches a plateau at about four months (Sireteanu et al. 1984). In contrast, adult acuity is reached by 1% years of age, or earlier. Therefore a ‘double’ visual impairment exists in infants with congenital and early- acquired ocular disorders. As a result, most of them initially are thought to have little or no vision. As the ‘psychological visual impairment’ disappears, however, a majority will develop useful sight. Indeed, the future visual function of most of our infants was underestimated at the time of diagnosis. Unless physicians keep this process in mind, their prognoses will be unduly pessimistic.

Frequently the parents could not determine accurately the onset of roving because newborns sleep most of the time. Furthermore, often they did not know what normal eye-movements should be at this age. Nevertheless, it appears from our study that most legally blind children exhibited roving movements immediately after birth or within a couple of weeks. It needs to be emphasized again that roving is a slowly drifting movement and it is different from the aimless eye-movements of visually inattentive children, and from nystagmus, which is best conceptualized as a ‘tremor’. Roving is not ‘searching nystagmus’, a vague term which probably should be discarded.

Without fixation, which is an ‘anchor’, the globes move slowly back and forth, probably because in the absence of vision, perception of eye position is very poor (Brindley and Merton 1960, Gauthier and Hofferer 1976). Roving therefore implies lack of fixation. Infants with comdete 289

blindness or only light perception exhibited roving indefinitely. Otherwise at a certain stage of visual maturation they developed enough vision for fixation, which initiated sensory nystagmus. Roving could be interrupted if a face or object was brought close enough to the child's eyes. Thus roving and nystagmus did not exist simultaneously, but replaced each other.

In infants with residual sight, nystagmus gradually appeared and roving then faded away. First they fixated only occasionally on objects, later more often and longer, and eventually the nystagmus became more sustained. Nystagmus lasted as long as the children attempted to fixate, and sustained nystagmus was observed at one time and only a few beats at another. Infants with 20/200 acuity frequently began to exhibit nystagmus at two to three months, while roving gradually faded away after four to six months of age. Children with worse vision developed nystagmus later and also exhibited roving longer. Therefore it is our clinical impression that early onset nystagmus implied better visual acuity.

When the posterior visual pathways were destroyed in our patients, nystagmus did not develop or it was abolished. Therefore roving and sustained sensory nystagmus were the hallmarks of ocular or anteriorpath way disorders. Nystagmus in our children was never congenital, but acquired during the first year of life in response to poor central vision and not to abnormal peripheral retinal function. Sensory nystagmus was the result and not the cause of visual impairment. Further- more, it appeared that the severity of the combined 'physiological' and ocular visual impairment during the first year of life determined the presence and quality of nystagmus. Infants whose acuity improved to 20170 or better did not develop nystagmus because their visual systems were exposed to adequate visual input, unless they had an uncorrected refractive error, during the first year of life. Therefore during that critical early period their vision was worse than the later 20/70 corrected acuity would suggest. Nystagmus resulting from congenital or acquired visual impairment

290 under six months of age was often intense

(slow, with large amplitude), while visual loss acquired in the second half of the first year was associated with finer nystagmus (fast and small amplitude). Nystagmus tended to appear two to four weeks after sudden severe visual loss under the age of one year only.

The severity of visual loss clearly affected the strength of fixation, and as vision diminished it was easier to break fixation by the oculocephalic manoeuvre. As vision improved with age, the nystagmus diminished. Initially it tended to be coarse, then later finer. When refractive error was corrected in an infant with roving movements, the improved acuity occasionally precipitated nystagmus, but prescribing glasses for older children sometimes made the nystagmus less marked. Sensory nystagmus was ex- tremely variable because it was influenced by many dynamic factors (see Table IV). Nevertheless, it did reflect the onset and severity of visual loss.

On rare occasions sensory nystagmus completely disappeared because a signifi- cant refractive error was corrected, gradually all vision was lost, or super- imposed cortical blindness abolished it. The last occurred in one of our patients with adrenoleukodystrophy.

Individuals with nystagmus may have certain positions of gaze in which vision is better and the nystagmus is less intense and pendular. These positions frequently do not coincide with normal frontal gaze but are displaced to an eccentric position. As a result, when concentrating on seeing, these children learn to hold their heads at abnormal angles. This tended to happen during the first year of life in our patients. Outside this position of relative rest the nystagmus becomes jerky and no longer consists entirely of slow eye-movements. This is of marked importance physio- logically because during fast saccades the vision is inhibited, while during slow movements it is not. This may explain why vision is better in the null position.

Traditionally sensory nystagmus has been interpreted as an undesirable con- sequence of visual dysfunction. On the contrary, however, the dynamic nature of sensory nystagmus suggests that it may be a physiological rather than a pathological process. The reason why steady visual

scenes do not fade away is that micro- saccadic eye- and head-movements exist to produce fluctuation continually in the local stimulation of retinal receptors. The ever-changing retinal stimulation is necessary for the proper maintenance of vision. By being a scanning device during fixation, nystagmus thus may be advan- tageous to visually impaired children, who may require more movement for stimulation.

Normal infants exhibit poorly co- ordinated eye-movements which then improve (Dayton et al. 1964). In our children with congenital or acquired visual impairment under the age of one year, the oculomotor problems persisted. Those with acuity of 20/100 or better generally followed moving objects with good fluency and minimal associated head-movements. Their voluntary upward gaze was normal, fixation was strong and they kept their heads erect. When vision in the better eye was close to 20/200, the associated head-movements during pursuit and looking on command were noticeably increased and the eye movements became jerky and clumsy. They still kept their heads erect but their voluntary upward gaze tended to be limited and fast, passive head-movements could dislodge their fixation. When vision was severely impaired, oculomotor diffi- culties also were more severe. These children lacked fluent eye-movements and frequently were unable to look up voluntarily. Even slow, passive head- movements broke their fixation, and when not looking their heads often hung down. During pursuit and looking on command they mainly moved their heads rather than their eyes. With total loss of vision there was no pursuit and voluntary eye-movements were absent. These children kept their heads erect only when taught to do so.

We observed that intelligent children and those who were encouraged to use their vision often seemed to have fewer than expected oculomotor problems. Further research is indicated to substan- tiate this clinical impression.

We believe that the restriction of voluntary upward gaze exists in some visually impaired children because they rarely look up. Children who can see only

m one foot away see nothing if they look up, but see much more sideways or downward. Similar restriction of upward gaze has been noted more commonly in old people and in tall rather than short individuals, and less commonly in patients with severe kyphosis (Chamberlain 1971).

When there is marked loss of vision due to ocular causes the head tended to hang down. In contrast, patients with cortical visual-loss, regardless of the degree of sight, kept their heads erect when they had good neck control. A small group of patients with total or severe ocular visual- loss held their heads erect only at certain times; generally they were encouraged to do this because it was more socially E

acceptable. Many of them temporarily lifted their heads when they saw 2

2 d something, so it seems that visual contact

with the environment is the main stimulus for individuals to keep their heads erect. It has been postulated that balance improves when the head is tilted forward and the horizontal semicircular canals become entirely horizontal, but there is no scientific evidence for this. However, when some of our severely visually impaired children closed their eyes their static balance improved, suggesting that at times the use of minimal vision may interfere with the efficiency of other senses.

Cortical blindness is defined in the literature as complete loss of vision with preservation of pupillary reflexes, normal eye-movements and a normal-appearing fundus (Marquis 1934). However, this definition is too restrictive and often leads to a delay in the diagnosis of permanent cortical visual impairment. Damage to the occipital lobes or post-geniculate visual pathways rarely caused total destruction in our patients, so most of them had some residual sight. Furthermore, the existence of extra-geniculo-striate visual systems is now well accepted. These probably pro- ject from the retina via the superior colliculus and the pulvinar to the secondary visual cortical areas and other regions (Perenin et al. 1980, Zihl 1980). Therefore even when the visual cortex is completely destroyed, visual input to the brain is not totally abolished. For these reasons cortical visual impairment is a better term than cortical blindness. This

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may also explain why roving movements were absent in our patients with cortical visual impairment.

The main causes of permanent cortical visual impairment in these children were asphyxia, ventricular shunt failure, mas- sive brain swelling, congenital anomalies of the brain and infections. In some patients both pre- and post-geniculate pathways were damaged simultaneously (Whiting et al. 1985). While ocular and anterior visual-pathway disorders in congenital or early-onset blindness predis- posed to nystagmus, damage to the occipital lobes and to the posterior visual pathways diminished it. Therefore the presence or absence of nystagmus and roving movements were important clinical clues. When congenital or early-onset blindness was not associated with roving movements and/or sustained nystagmus, damage to the visual cortex or post- geniculate pathways was suspected. Our patients with co-existing defects of anterior and posterior pathways occasionally exhibited a couple of beats, but not sustained nystagmus. Again, the ‘tra- ditional’ definition of cortical blindness is too restrictive, since the eye movements of children with permanent cortical visual loss may not always be normal.

Children with cortical visual impairment often paid little or no attention to their visual environment, had fast, fluent eye-movements and tended to keep their heads erect. Because they did not appear to be ‘blind’, the diagnosis was frequently delayed. Again, the existence of extra- geniculo-striate visual pathways may explain both the lack of poorly co-ordinated eye-movements and the presence of erect head posture. Three children with congenital cortical visual loss due to neonatal asphyxia were blind for six to 11 months

and then rapidly recovered, two of them completely. Their eye movements when they were older were normal. The analysis of our patients with cortical visual loss strengthens the observation that nystagmus develops and apraxic eye-movements occur because of visual deprivation rather than the lack of visual interpretation.

Evaluation of vision is a difficult task with the young and the handicapped, since most tests require co-operation b j the patient. However, it is the amount of time the examiner is prepared to spend that determines the accuracy of the assessment (Taylor 1978). Our studies indicate that the appearance and the eye and head movements of the visually impaired reflect the severity and onset of their visual loss and offer valuable clues, especially in the evaluation of preverbal and handicapped children, who most frequently fail to co-operate.

Accepted for publication 10th September 1985.

Acknowledgement The authors thank Dr. C. S. Hoyt for his comments.

Authors’ Appointments *James E. Jan, M.D., F.R.C.P.(C), Professor, Division of Paediatric Neurology, Department of Paediatrics, University of British Columbia. Cf. ordinator of Visually Impaired Program, B.C. s Children’s Hospital, 4480 Oak St., Vancouver, British Columbia V6H 3V4. Kevin Farrell, M.B., Ch.B., D.C.H., M.R.C.P.(UK), F.R.C.P.(C). Assistant Professor, Division of Paediatric Neurology, Department of Paediatrics, University of British Columbia. Director of Seizure Clinic, B.C.’s Children’s Hospital, Vancouver. Peter K. Wong, M.D., F.R.C.P.(C), Assistant Professor. Division of Paediatric Neurologv. University of British Columbia. Director, Divisi’Gn of Diagnostic Neurophysiology, B.C.’s Children’s Hospital, Vancouver. Andrew Q. McCormick, M.D., C.M., F.R.C.S.(C), Clinical Associate Professor, Department of Oph- thalmology and Associate, Department of Paedi- atrics, University of British Columbia, Vancouver.

*Correspondence to first author.

SUMMARY Fixation, nystagmus, pursuit, rapid voluntary, other types of eye movements and associated head movements of visually impaired children were studied. It was concluded that their eye and head movements reflect the severity and onset of their visual loss.

R ~ S U M ~ Mouvements des yeux et de la t2te chez des enfants prksentant des dkfauts visuels La fixation, le nystagmus, la poursuite oculaire, les mouvements des yeux volontaires rapides et d’autres types, les mouvements de t&te associes ont CtC ttudies chez des enfants presentant des defauts de vision. Les auteurs concluent que les mouvements des yeux et de la t@te traduisent la gravitt et le moment du debut de la Derte visuelle.

ZUSAMMENFASSUNG Augen- und Kopfbewegungen bei visuell geschadigten Kindern Bei visuell geschadigten Kindern wurden Fixation, Nystagmus, Folgebewegungen, schnelle willkiirliche Augenbewegungen und andere Augenbewegungen sowie die entsprechenden Kopfbewegungen untersucht. Die Autoren haben gefunden, daR ihre Augen- und Kopfbewegungen den Schweregrad und den Beginn ihres Sehverlustes widerspiegeln.

RESUMEN Movimientos de ojo y cabeza en niflos con dificultad visual Se estudiaron 10s movimientos de fijacion, nistagmus, seguimiento, movimientos voluntarios y de otros tipos, asi como 10s movimientos asociados de cabeza en niflos con dificultad visual. Se concluye que sus movimientos oculares y de cabeza reflejan la gravedad y el inicio de su perdida visual.

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