Subcortical Visual Function in the Newborn Russell D. Snyder, MD*, Steven K. Hata, MD*, Benjamin S. Brann, MD*, and Rose M. Mills~

Early behavioral visual function in infants may not depend upon the geniculocalcarine pathway but may be mediated through more primitive subcortical path- ways. This subcorticai visual system may exist in early life and be responsible for visual pursuit and perhaps fixation. In some infants with damage to the visual cortex, the subcortical pathway may persist beyond the neonatal period. Three infants with major defects in the visual cortex are reported. These infants displayed persistent preservation of visual pursuit movements without evidence of visual recognition. Limited behav- ioral expressions of vision in the infant with damage to the visual cortex may not always be an indicator of preserved function of the visual cortex.

Snyder RD, Hata SK, Brann BS, Mills RM. Subcortical visual function in the newborn. Pediatr Neurol 1990;6:

333-6.

Introduction

Early visual function in the term infant is generally considered to be a marker of the integrity of the primary visual cortex and a predictor of future neurologic develop- ment; however, it has been suggested that some visual behaviors in the human neonate are mediated through phy- Iogenetically older subcortical visual pathways [1 ]. A sub- cortical extrageniculocalcarine visual system may exist in early life before the geniculocalcarine pathway is fully functional. This subcortical system may function transi- ently in the newborn for visually guided behaviors, such as the following of large objects, which is replaced by the geniculocalcarine system in the early weeks of life [21. When the geniculocalcarine system has undergone major damage or abnormal development, the subcortical system may persist.

We present 3 infants with major defects in the region of the visual cortex but persistent evidence of visual pursuit. Conscious visual awareness was not demonstrated.

Case Reports

Patient 1. This male infant was born al home with meconium stain- ing at the time of membrane rupture, Birth weight was 3,530 gm and bead circumference 36 cm. He had no spontaneous respirations and required a ventilator. Pupillary light reflexes were normal, but eye movements were chaotic. He was hypoumic and had generalized myo- ckmic jerks several times daily.

Electroencephalography (EEG) was performed at I and 8 days of age and demonstrated no detectable cortical activity. Computed tomog- raphy {CT) was performed on day 6 and revealed diffuse, bilateral edema and hemorrhage (Fig IA), Visual pursuit was observed by 3 weeks of age and persisted thereafter. EEG was performed again at 6 weeks of age and disclosed periodic sharp waves. Cranial magnetic resonance imaging (MRI) was also performed and disclosed marked loss of hemispheric parenchyma (Fig 1B). At that time, the infant had normal suck. cry, and smile and the myoclonic jerks had ceased.

At 8 weeks of age, a brainstem auditory evoked response (BAER) study was perfm'med with a normal response: however, no response was obtained on visual evoked potential (VEP) testing.

One week later opticokinetic nystagnms (horizontal only) was present and he became more attentive to moving than to slationar} objects.

At 2% years of age, he lollowed moving objects but did not regard stationary objects. He exhibited no response to visual threat or any recognition. The optic discs were of normal color and the pupils responded to light. VEP studies revealed no response under transient or steady-state stimuli. BAERs were normal. He could roll fi'om front to back and hold an object placed in his hand but not exchange objects li'om hand to hand. He was unable to speak. VEP demonstrated no response under transient or steady-state stimuli. Head circunlferenee was consistently I S.D. below the mean.

Patient 2. Prenatal ultrasound revealed hydrocephalus. Spontaneous vaginal delivery occurred at 34 weeks gestation. Birth weight was 2.770 gm and head circumference 39.5 cm. Apgar scores were 4 at I min and 6 at 5 ram. The optic discs were of normal color and the pupils were reactive. He was hypotonic with poor" respiratory efton and cry. CT performed soon after birth demonstrated only a small amount of cortex in the occipital region with no other identifiable cortex and nonnal appearing brainstem, cerebellum, and thalamus. MRI perfbrmed at the same time demonstrated a markedly thin cortical mantle with massive hydrocephalus/bydranencephalus. The fimrth ventricle, thal- amus, brainstem, and cerebellum appeared normal. BAER studies dis- closed no response from the right ear with prolonged peak latencies on the left suggesting an upper medullary or pontine disturbance. No cor- tical response to flash VEP studies was observed. EEG revealed a bursl-suppression pattern. Karyotype was nonnal.

At 2 weeks of age, he was visually regarding and following objects and appeared to be a normal infant: however, at 21/2 months of age he was readmitted for rapidly increasing head circumt)rence. A shunt was placed from the large intracranial cavity into the peritoneum. After shunt placement he continued to follow moving objects and to fixate on stationary objects. His pupils reacted to light but he did not blink to threat.

At 3 months of age, VEP study disclosed prohmged latency poten- tials over the occipital area. He exhibited no cortical response during somatosensory evoked potentials (SSEPs) evaluation.

From the *Departments of Neurology and Pediatrics; University of New Mexico Medical Center: Albuquerque, New Mexico; '~Black Hills Neurology: Rapid City. South Dakota; TDepartment of Pediatrics; University of New Mexico Medical Center; ~Neurophysiology Laboratory: University of New Mexico Hospital; Albuquerque, New Mexico.

Communications should be addressed to: Dr. Snyder; Department of Neurology; University of New Mexico Medical Center; 2 South: Albuquerque, NM 87131. Received January 31, 1990; accepted May 16, 1990.

Snyder et al: Subcortical Visual Function 333

A B

Figure l. Patie~u /. fA) Cranial CT without ~ontr~st at 6 dav,s ~?f age, Diffuse edema ~?[" hemisphere's. ~Bt Cor~mal MR/c~['head, T/-weiehted at age 6 weeks. Marked loss i!f hemispheral parenchyma.

At 9 months or' age, CT demonstrated no change fiom earlier studies with cystic fluid collections in most of the supratentorial space (Fig 2i. At 18 months of age, pupillary reactivity, visual pursuit, and horizontal opticokinetic nystagmus persisted but recognition could not be demon- strated. He rolled from back to front and could raise his head and chest when prone. He blinked to loud noises and could be quieted by a whis- pered voice even when not held. Speech had not developed.

Patient 3. Seizures occurred shorlly after birth. Her early develop- ment was delayed. Microcephaly was present. The right ear was atretic. At 3 months of age, flash VEP studies revealed well-developed respon- ses over the occipital region. At 2 years ol' age, a gastrostomy was

required. At 4 years of age, CT revealed semilobar hotoprosencephaly with no

detectable occipital cortex (Fig 3). She exhibited conjugate visual fol- lowing without evidence of fixation or recognition. The pupils reacted to light and the optic discs were of normal color. EEG disclosed burst suppression and photic driving. Flash VEP revealed well-developed cortical responses, maximal over the midline parietal area CPz)~ No cor- tical response was present with SSEPs, She never developed self-help

skills.

Visual function in the human term newborn is assumed to require the visual cortex and has been considered to be an indication of the integrity of the cortex in general and a predictor of future neurologic outcome; however, vision in early life may be mediated by subcortical rather than

Discussion

Subcortical extrageniculocalcarine vision has been dem- onstrated in primates. The subcortical system in the mon- key is presumed to involve the retina, optic nerves and tract, pulvinar, and superior colliculus, with projections to the visual cortex and visual association cortex. In studies with monkeys, bilateral ablation of area 17 with preserva- tion of areas 18 and 19 results in loss of visual recognition of stationary objects, but preservation of awareness of moving objects. There also is preservation of visuospatial orientation [3]. In the primate the superior colliculus ap- pears to be involved in the immediate defense against a visual threat and in orienting responses [4]. This subcorti- cal system is sometimes referred to as the "collicular visual system" [5].

Figure 2. Patient 2. Cranial CT without contrast at age 9 months. Shunt tube in right posterior parietal region. Large ieystic fluid collec- tion in supratentorial region, Posterior septa probably representing de/~)rmed margins ~" tentorium ~md ,straight sinus. Hydroceph- ah~s/ hydraneneephalus.

334 PEDIATRIC NEUROLOGY Vol. 6 No. 5

Figure 3. Patient 3. Cranial CT at age 4 years without contrast. Holoprosencephaly without a detectable occipital cortex.

cortical structures. Premature infants with lesions in the thalami and basal ganglia were more likely to have prob- lems with visual behavior than those with extensive le- sions of the occipital cortex [1 ]. These functions may sub- sequently become cortical at about 48 weeks post concep- tion. At about the same time, binocular vision, which is regarded as a cortical function, appears and the visual evoked response undergoes a pronounced reduction in latency [6].

Two neonates and an older surviving infant with major brain abnormalities involving, but not restricted to, the visual cortex provide information regarding visual func- tion in infancy. Cognitive vision was absent in these in- fants, although normal optic discs, visual pursuit, and pu- pillary reactivity were present. The first infant had a mas- sive perinatal brain injury presumably related to hypoxia. The second had hydrocephalus/hydranencephalus 171. The third had a brain anomaly. Although cortically blind, each demonstrated some degree of visual behavior as mani- tested by visual pursuit movements when tested with a moving object. The findings in these infants suggest that the subcortical visual system is preserved or develops adaptively when a lesion, occurring prenatally or during early postnatal life, prevents normal development of the geniculocalcarine cortical visual system. These infants also corroborate the previous observation of the ability to track objects by an infant with hydranencephalus [81.

Alternative explanations for the visual difficulties in these infants have not been excluded. The infants did not have lesions isolated to the visual cortex. Plasticity within

the nervous system with rerouting of fibers from the visual cortex to areas of the cortex other than the primary visual cortex cannot be excluded; however, there was no sugges- tion of anterior displacement of VEP generators. Anatomic preservation of some functioning visual cortex is another possibility; these infants were all low-functioning individ- uals. Surviving infants with complete and isolated lesions of the visual cortex are exceedingly rare.

The human adult in the traditional concept does not appear to have an extrageniculocalcarine visual pathway [91; only cortical areas support behavioral vision. How- ever, it has long been known that humans with occipital lesions may manifest preservation of light discrimination and detection of moving but not stationary objects by a mechanism known as blindsight 1101. Blindsight is the ability to localize within a scotoma and is believed to demonstrate an extrageniculocalcarine visual pathway in adults [111. In addition, cortically blind adults with total destruction of the geniculocalcarine tract can retain pupil- lary reactivity to light and opticokinetic nystagmus I 12].

VEPs do not distinguish cortically blind from normal infants and abnormal responses are not incompatible with normal vision 113]. VEPs can be present in adults when subjective vision is absent and area 17 destroyed; VEPs are sometimes preserved with wide areas of cortical des- truction and cortical blindness. The responses are pro- longed and simplified. In these individuals, VEPs may be mediated at least in part by extrageniculocalcarine path- ways which are not capable of providing conscious vision in humans. Areas 18 and 19 do not receive input from the lateral geniculate body. Their input occurs from the cal- carine cortex and perhaps also from the superior colliculus. The collicular system appears to have input into VEPs, especially the components of long latency 114].

Positron emission tomography tPET) of infants has demonstrated low activity in the calcariue area until about age 3 months when an increase in activity occurs. PET activity increases even later in visual association areas 115] which provides additional indirect evidence that visual function in neonates may not be mediated by actively functioning cortical visual structures.

In early life there may be 2 visual pathways. The cortical visual pathway is used lk)r conscious visual analysis and the subcortical visual system subserves subconscious vis- ual guidance. An infant with a lesion of the visual cortex early in life or before birth may demonstrate visual phen- omena that can be explained by a subcortical visual sys- tem. Testing of vision in young infants by use of moving objects may be testing function of this subcortical visual system.

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