EARLY EXPERIENCE AND THE DEVELOPING VISUAL SYSTEM
The importance of normal development of the mammalian visual system to such diverse functions as negotiating space and conducting social interaction 1 becomes increasingly clear. It has long been established that early disruption of visual development has far-reaching consequences. Experimental studies since the 1960s have demonstrated in young mammals structural changes in the brain and altered behavior as a consequence of environmental conditions, such as total deprivation of light with occluding eye patches and absence of patterned input by suturing eyelids closed. 2 Furthermore, infant mammals reared under atypical visual conditions such as spots of light or black/white stripes showed increased brain responsiveness to the specific characteristics of the early environment. 3 The sensitive period, or period of susceptibility, for the animals studied corresponds to late prenatal and early postnatal life in the human infant.
In the human fetus and newborn, exuberant connections exist in the brain that are normally transient, but may persist if the sensory input is sufficiently altered by atypical environmental stimulation. Research with bobwhite quail and ducklings has also shown that precocious visual stimulation (light pulse or pattern) in early life can affect postnatal auditory dominance and interfere with the normal preference for species-specific sounds. 4,5 Furthermore, absence of an early visual motor milestone (hand regard) and relatively delayed visually directed reaching occurred among infants exposed to high levels of visual stimulation, compared to infants with more moderate or low levels of stimulation. 6 Together, these findings have major implications for the preterm infant.
Prenatal sensory environment
Throughout pregnancy, the sensory systems are normally exposed to a range of mechanical stimuli (sounds, vibration, vestibular changes, and even nonlabor contractions) and chemical stimuli (amniotic fluid bathes oral, nasal, and pharyngeal cavities stimulating senses of taste and smell). The womb is essentially dark, although a small amount of radiant energy (light) may also reach the fetus. With the exception of light, these stimuli are often structured or patterned, such as maternal speech, but not continuous or fixed (like a mechanical swing or clock). Even the maternal heart rate has a normal beat/beat variability. The prenatal stimulus may even be contingent on maternal or fetal behavior, such as variation in maternal heart rate with the mother's change in activity, or a change in a taste stimulus (amniotic fluid) as the fetus opens and closes its mouth. Of equal significance, a natural environmental stimulus often affects more than a single sense and in a contingent manner.
Visual system and sensory integration
During human fetal development, the sequential functional maturation of the tactile, auditory, and visual systems is modulated by this prenatal environment. At birth, vision is still the least functionally mature system relative to the other sensory systems. According to Turkewitz and Kenny 7 this functional immaturity of a given system is a necessary limitation during early development that effectively reduces available stimulation and thereby decreases competition between maturing sensory modalities. There is no evidence that accelerating development in a sensory system is advantageous, and it could be detrimental. 4
The normal full-term infant is auditory-dominant rather than visual-dominant at birth, but these two systems are coupled in a special way. A visually impaired newborn often has a heightened behavioral response to auditory stimuli; but in contrast, a hearing-impaired newborn has decreased attention to visual stimuli. At a more subtle level, a normal newborn looks in the direction of a sound presented laterally and responds differentially to sound of a given intensity according to the intensity of visual input (light level). 8 That is, the same sound may be responded to positively or negatively depending on whether the corresponding light level is low or high, respectively. It is also likely that a high-contrast visual pattern (eg, black/white/red) could have a similar negative effect on the auditory response.
What do we attend to?
Two different visual systems are present in primates. The magno system, or detection system (“where”), which responds to light, movement, edge, and large high-contrast form, functions even earlier than term birth. The parvo system (“what”) becomes activated around 2 months of age and is the essence of cortically mediated vision: sensitivity to finer detail, subtle contrast or shading, and ultimately processing and organizing those bits into meaningful information. In the normal infant, the “where” and “what” systems function together, but over-stimulation of the “where” system could, in effect, disrupt this balance and inappropriately heighten attention to motion and high-contrast form. Increased visual attending could also decrease responsivity to auditory input, which could impact language.
How do we see?
Light energy is transmitted through the cornea, pupil, lens, and optic media to the retinal layers where it bypasses blood vessels, ganglion cells, and bipolar cells before reaching the furthest tip of the photoreceptor cells (rods and cones). The actual amount of light energy necessary to stimulate a single photoreceptor cell is extremely small: 1 quantum. 9 A photochemical action then converts the radiant energy (light) into an electrical impulse that travels to the ganglion cells and from there to the optic nerve. The electrical signal from the optic nerve primarily transmits to the lateral geniculate nucleus and thence to the visual cortex (striate), located in the back portion of the brain.
Patterned information from the eye travels to the brain in a special way (Figure 1). Since the retina is a concave surface, like the bowl of a spoon, information from the left (or right) visual field falls on the opposite side of the retina and is upside down. In addition, fibers in the nasal (or inner) half of each retina divide at the optic chiasm and transmit to the opposite side of the brain (see figure), whereas fibers from the outer half of each retina do not divide. This means that information from the left visual field will fall on the right half of the retina and transmit to the right side of the brain. Likewise, the reverse holds for the right visual field to the left hemisphere. Representation in the visual cortex is topographic, although upside-down and reversed. This anatomic organization of the visual pathways also means that even with loss of vision in one eye, information is transmitted to both hemispheres of the brain. It also means that damage along the visual pathway past the optic chiasm can cause loss of vision in both eyes to the opposite visual field. Of note, the actual image from each retina is slightly different, so that a three-dimensional object in space, projecting as a two-dimensional retinal image, is transposed into three-dimensional information by the visual cortex providing one of the major clues for perception of depth.
Most higher-order visual processing (eg, pattern discrimination, visual recognition memory, visual-motor integration) takes place in the primary and association areas of the cortex, although subcortical structures and even the cerebellum are also involved. The highly complex task of reading involves interpretation of meaning from a finite set of visual elements (26 letters) that represent sounds arranged into words in order to convey meaning. Finally, the visual arts use form, dimension, color, light, space, and composition to convey an aesthetic experience.
Prenatal visual development
The eye is an outgrowth of the brain from the early embryonic period, thus the relative maturity of one generally reflects the other. At 23–24 weeks gestation, the lower limit viability for a preterm infant, major eye structures are in place and the visual pathway is complete to the level of the visual cortex. However, the extreme immaturity of the visual system at this age is signaled by the presence of fused eyelids, cloudy optic media, and remnants of an embryonic tissue (tunica vasculosa lentis) in the eye globe. Only a few immature photoreceptor cells are present in the retina at this stage. Blood supply to the retina depends on diffusion from the underlying choroid layer. Development of the retinal blood vessels, which will be needed to meet the increasing demand for nutrients, has begun in the posterior part of the retina near the optic nerve.
During the last trimester of pregnancy, the retina and visual cortex undergo extensive maturation, cell differentiation, and remodeling, while primitive visual function emerges. Underlying brain maturation is concurrently reflected in regulation of sleep/wake behavior. These events can be subdivided by conceptional age groups: 24–28 weeks, 30–34 weeks, and 36 weeks. 10
The eyelids are no longer fused. However, awake and sleep periods are not yet well differentiated, either behaviorally or by electroencephalogram (EEG) pattern. Immature visual response is present once the anatomic pathway from the retina to the visual cortex is complete. A primitive form of visual evoked response to light flashes can be recorded from the cortex. The pupillary reflex is absent, but a behavioral response (lid tightening) can be obtained to bright light, although the response readily fatigues. The refractive error is about -5 diopters, or extreme myopia.
Important functional changes begin. Sleep and wake states become differentiated by EEG pattern. The visual evoked response wave form is more complex and has a shorter latency. A (slow) pupillary reflex is now present. A bright light causes immediate lid closure, and the response sustains. The eyes may open spontaneously, and the infant may even briefly fixate. This first evidence of visual attention (32–34 weeks) may be elicited but requires a larger high-contrast form than at term; both occur under similar conditions of low illumination (5 footcandles).
By 36 weeks gestation, the electrophysiological and behavioral correlates of sleep are becoming organized into coherent patterns. The visual evoked response now resembles that of a full-term infant, but the latency is still longer for the preterm infant and generally remains so. The awake state is more sustained, although still shorter than at term. Behaviorally, the preterm infant shows spontaneous orientation toward a soft light and can track a slowly moving object along either a horizontal or vertical plane. The preterm infant, like the full-term infant, prefers a patterned to a nonpatterned surface. The earlier myopia is no longer evident, and the refractive error is near zero.
Visual development at term
The retina at term birth remains relatively underdeveloped. 11 The fovea, the region of the retina responsible for high acuity, is twice the width it will later become and contains relatively few cones, which are less maturely shaped (shorter) and less densely grouped than they will be. The process of cone migration from the periphery to the foveal region is not complete until 3–4 years of age. Color vision, the other primary property of the cone photoreceptors, is probably present in the newborn. However, blue cones may not be functional until about 1 month of age, and change in color perception is likely to occur during cone migration and maturation.
The optic media, the fluid filling the eye globe, is less dense and contains less macular pigment than an adult and therefore transmits more short-wavelength (blue to ultraviolet) light than an adult by a factor of four. 12 This may partially account for the relative photophobia of neonates and their more optimal visual behavior under low illumination (approximately 5 footcandles).
Infants at this age have more functional vision than their acuity estimates (20/400 Snellen equivalents) would suggest. The refractive error is slightly hyperopic (+1 diopters) or farsighted, and the accommodative, or focusing, properties of the lens are undeveloped. This means that the infant does not see “better” if an object is brought closer, it is just that the object occupies more area of the infant's visual field. The actual visual image is degraded, or blurry, but on a white board at a distance of 1 foot infants can see high-contrast black lines only 1/16″ wide. They can be “visually captured” by a slowing moving looming face/head of a person, light source, bright object, or high-contrast pattern, and will follow the movement horizontally across midline and, to a lesser extent, vertically. Eye movement is usually conjugate during tracking, even if the newborn is blind in one eye. Some dysconjugate eye movement may be observed in normal infants during the first month, particularly after the infant engages in imposed visual tasks.
Visual thinking during infancy
The visual image gradually sharpens with cortical maturation and as the lens begins its accommodative function. Early accommodation seems to be a cortical process, albeit an unconscious one. Increased cortical visual function becomes apparent with a shift from responding predominantly to light, movement, and simple brightness or high-contrast edges to more selective attending, organizing details into coherent patterns, and understanding the use of an object or what a picture represents. The maturational process is concurrent with change in synaptic density in the visual cortex, which is relatively constant from birth to 2 months of age, doubles by 8 months, then decreases to adult levels by age 10 years. 12 A shift from auditory to visual dominance along with an uncoupling or dissociation of the two systems occurs around 3 months of age, although auditory input continues to play a role in heightening and maintaining attention. Reintegration of the auditory and visual systems occurs through normal experience.
By 2 months of age, cortically mediated visual behavior can be reliably observed. The infant will look at the features of a human face, rather than just the edge, particularly when the face is accompanied by voice. Parents readily report that their infant by this age has begun to watch them at a distance. Attention now has a reflective quality as indicated by a deliberate shift of gaze between two people, objects, or patterns and by demonstration of simple visual preference for a particular member of a pair. The basis for visual-motor integration appears with the onset of hand regard.
By 3 months of age, the baby is more dominated by visual input, particularly social, than by auditory input. Visual attending has increased to the point where eye contact is coupled with increased limb movement to actively solicit attention from others. Objects are regarded with some interest but not in preference to people. A baby at this age will clasp a small rattle placed in one hand and bring it into the visual field.
At 4–6 months of age, babies are increasingly fascinated with other baby faces and with a mirror image. Visual recognition memory is present for both social and nonsocial stimuli. An infant recognizes a person on sight and smiles selectively in a discriminating sort of way. A bottle-fed baby may respond meaningfully to the sight of the formula bottle at a distance even without any contextual cues. Increased cognitive processing is also found in the ability to abstract relevant pattern information amidst change without being overly distracted by detail. Everything seen nearby is something to be touched and activates reaching. From this joint process, reaching/grasping become visually guided. Rather than just a sweeping or swatting action, the infant calibrates the reaching motion from the visual/proprioceptive feedback. Once a toy has been grasped, the infant will visually inspect and examine it while changing its spatial orientation, regard it with increased interest when it happens to make a noise, and then look for it when it falls from view.
From 6–12 months, visual information processing takes another major step. The infant learns to predict the reappearance of a toy that disappears in a playful way and to search under a cover for a toy that has disappeared. Thus objects continue to exist for the infant even when they are no longer in view. Understanding a picture as a representation of a real object also emerges. At first an infant will just look at a picture, then later touch it or attempt to pick the picture of a familiar object off a book page. By 12 months, a novel picture may be recognized as a representation of a familiar object, but the identity of unfamiliar objects is probably not learned through pictures until more language is available to support it.
The social/communication implications of normal vision also remain powerful during the second half of the first year. From the earlier roots of mutual gaze behavior in the form of a dyad, infants during this latter stage are able to look at what you are looking at by following the direction of your gaze. As the adult naturally and repeatedly labels what and who the baby is looking at, the baby then begins to direct his/her gaze toward those familiar people and objects in response to the word alone. Similarly, the baby looks at an object and then at the parent, to indicate wanting access to the object and/or seeking comment from the parent. Toward the end of this period, a baby shows a toy to a parent in a manner of sharing wonder and will modify approach to, or withdrawal from, a novel situation according to the positive (or negative) expression on their parent's face.
EFFECTS OF EARLY BIRTH
Susceptibility of preterm visual system
Preterm birth sets the stage for a cascade of events that potentially impact brain development; the visual system is particularly susceptible to insult. The most well-known problem is retinopathy of prematurity, but preterm infants are also at increased risk for ocular defects (refraction and eye alignment) and cortical visual deficits.
Retinopathy of prematurity
Retinopathy of prematurity (ROP) is a proliferative vascular disease of the immature retina affecting the majority of infants born prior to 28 weeks gestation. Severity of ROP is defined by disease progression (stages 1–4), retinal location (zones 1–3), and extent (number of clock hours affected). The more prematurely born an infant, the greater the probability of having ROP and the more severe disease.
Near the end of the second trimester, retinal blood vessels begin to develop in the most posterior region of the retina (zone 1) and progress anteriorly. This process is generally complete by term. In the healthy fetal retina the region between the newly developing blood vessels and the adjacent avascular region is normally indistinct, but if a thin line demarcating these two regions becomes apparent, then Stage 1 ROP is present. By Stage 2, the line has thickened into a ridge. Stage 3 defines qualitatively more severe disease with atypical proliferation of new blood vessels into the vitreous. This pathological process may lead to scarring and traction causing the retina to fold or even detach (Stage 4–5). The more posterior in the eye the disease occurs, the poorer the prognosis. This is because the damage may affect the macular region, the area of the retina densely populated with cones (photoreceptors responsible for high acuity).
Most cases of ROP do not progress beyond Stage 1 and have few sequelae. 13 Laser treatment is commonly applied in an attempt to halt Stage 3 disease and has significantly reduced the proportion of infants whose ROP reached Stage 4–5 and are functionally blind. Infants with ROP Stage 2 or greater have a higher probability of ocular disorders (see below).
The more common ocular defects affecting infant visual development include significant refractive error and defects of eye alignment. Common refractive errors are myopia (nearsightedness) and hyperopia (farsightedness). Significant myopia would affect a baby's ability to see at a distance details of objects or a person's features. In cases of extreme myopia even mid-range would be affected. Significant hyperopia can affect a baby's interest in attending to near objects, such as pictures in a book and objects in their hands or on a table surface. With hyperopia, the baby's lens attempts to bring the near object into focus, but the sustained effort may cause some discomfort and the baby naturally looks away. Astigmatism is another common refractive problem, whereby the surface of the cornea lacks its normal spherical shape so the light rays entering the eye are distorted and the image is not well focused. Refractive errors are usually well corrected with appropriate glasses, but glasses are often not tolerated by infants until they become more cognitively aware of the advantage.
Problems with eye alignment are referred to as strabismus. One or both eyes may turn inward (esotropia) or outward (exotropia). Abnormal eye alignment will cause diplopia (double vision). The brain responds to this double image by suppressing the information from one or the other eye which may cause a condition known as amblyopia, or “lazy eye.” If untreated, amblyopia can lead to permanent loss of vision that is not correctable with glasses.
Cortical visual impairment
Cortical visual impairment (CVI), as the name implies, involves injury to or malfunction in the brain. The general appearance of the retina is normal, although the optic nerve may be less developed. CVI has also been referred to as cortical blindness, but the degree of deficit varies and young infants generally show some improvement over time. It is common among infants with global brain damage associated with severe hypoxic-ischemic events and among those preterm infants who have significant loss of brain tissue in the region of the ventricles (eg, periventricular leukomalacia). 30 The severity of CVI generally corresponds to the degree of brain injury. Initially, fixation and tracking may be absent or limited to light and movement of large looming forms. The ability to visually recognize an object may never develop.
Visual processing deficits
Visual processing deficits represent a milder form of cortical visual deficit, which occurs more commonly among infants and children born prematurely, particularly those who had some degree of brain injury. The deficits include problems in attention, pattern discrimination, visual recognition memory, and visual-motor integration.
Attention is basic to visual information processing, but defining an optimal response is problematic. Obviously, looking times that are too short may reflect deficits in attention. However, longer looking times are defined as less mature responses because for a given stimulus younger infants take longer to process the information and tend to look at it longer than do older infants. Longer looking time to an unchanging pattern, or slower rate of processing, is also characteristic of preterm infants compared to full-term infants. 14 Of particular relevance, longer attention to a black/white checkerboard pattern at term is associated with a lower IQ in childhood. 15
Unlike full-term infants at the same conceptional age, preterm infants fail to demonstrate a response to novel pattern 16 or visually recognize an object that was handled. 17 In addition, preterm infants show a relatively longer latency to reach for a toy, less interest in novel toys, and lesser degree of exploration of objects. Studies of older preterm children indicate the problem may persist, even if the comparison is limited to children who have a normal IQ score. 18 The range of tasks studied included visual discrimination by match to sample, selection of one visual pattern that does not belong to the group, and visual-motor integration (reproducing a visual pattern with pencil and paper).
Potential impact of the neonatal intensive care unit (NICU) environment
During the third trimester of pregnancy, extensive maturation of the visual system ordinarily takes place within a dark womb, which differs markedly from the NICU environment. A small amount of light (probably less than 2%) can reach the fetus, but in the latter stages of pregnancy even the normal position of the fetus (face posterior) limits light exposure. Thus, it is highly unlikely that light exposure is a necessary condition for normal development of the fetal visual system. Periodic exposure to low levels of long-wavelength light is probably not harmful. However, common light levels in the NICU are in the range that produce phototoxic effects in animals 20 and potentially affect the preterm infant. 11,21 Converging evidence supports an association between NICU light exposure and ROP, 22–25 although a separate study found no significant protective effect for preterm infants whose eyes were patched until 31 weeks gestation. 26
There is no evidence light is a necessary condition for ROP to occur or that maintaining a preterm infant in the dark will completely prevent it. NICU light levels may also have behavioral effects. Lower ambient light is associated with more quiet sleep, 28 during which period growth hormone secretion and tissue healing occur. Lower light is also associated with increased awake/alert periods and with more optimal responding to auditory stimuli. 8
DEVELOPMENTAL INTERVENTION DURING EARLY INFANCY
Developmental interventions affecting the visual system include manipulation of light levels and patterned input. These manipulations are often initiated in the NICU but extend beyond the period of term birth into the home and also include healthy infants. However, even the most well-intended interventions, whether for preterm infants or otherwise normally developing infants, may have unexpected consequences beyond an immediate goal of enhancing visual attention.
High levels of ambient light in the NICU, as might emanate from overhead fluorescent tubes or from nearby windows, are unnecessary and potentially detrimental. A prudent approach in the NICU is to shield the infant's eyes from ambient and supplementary light sources. Shielding does not mean occluding the eyes. No evidence supports the use of patching beyond what is necessary for phototherapy. Prolonged patching may be detrimental in terms of both stimulus deprivation and possible effects on corneal growth. The light beam that emanates from some bili-lites is quite intense (>10,000 footcandles), should only be used with opaque patches, and should never be directed at an infant's head.
Cycled light (dim/dark) is logistically difficult to manage in an environment caring for critically ill neonates, but it may be feasible when the infant is more medically stable and occurs naturally at home. Animals that have sustained photic damage show recovery when returned to normal light-dark environments. 20 Beneficial effects on preterm infant behavior have been reported. 29
Dim light (5 footcandles) enhances spontaneous eye opening in the preterm and full term newborn, which is particularly compelling when a caregiver is present. Effective use of available room light during early infancy for any baby would involve positioning so that the light source is behind the baby's head, which then allows the light to softly illuminate the adult's facial features. This same technique is later extended for use with visually impaired infants and young children who may require use of more intense directed light.
Black/white pattern as a form of visual stimulation in early infancy is inappropriate on a number of levels. Its popular use stems from the well known observation that neonates attend to black/white pattern in preference to a grey unpatterned surface, but an infant's ability to respond to a type of stimulation does not necessarily mean that he or she should be stimulated in that manner (eg, young infants will even stare at light bulbs). Since the immature brain becomes increasingly responsive to specific characteristics of the visual environment, 3 the consequence of exposure to black/white pattern—increased attention—is actually a less mature response and is even associated with lower IQ in childhood. 15 Furthermore, precocious visual stimulation interferes with the normal auditory dominance in the newborn period 4,5 and could have the unexpected consequence of decreased attention to normal auditory input (speech). Finally, high levels of visual stimulation in early infancy disrupt the emergence of hand regard and visually directed reaching, 6 both important milestones.
Mechanistic approaches to enhance infant visual development have significant shortcomings, with the exception of a simple, pastel mobile. An abundance of brightly colored toys with flashing lights is visually over-stimulating and promotes simple arousal, than rather relational play. The more important form or function of an object is most likely to be lost. Swings create a fixed motion that produces a constantly shifting visual image, particularly in the retinal periphery. Television is equivalent to staring at multicolored moving lights; videotapes should be avoided entirely, since they provide a stereotyped repetitiveness on multiple viewing not reproducible in nature.
Basic principles can effectively guide developmental intervention in the early months. In the transition from prenatal to postnatal life, the infant's mother is the optimal source of stimulation, providing familiar smell, taste, rhythms, and even voice. The innate predisposition of the infant to attend to features of a face 16 emerges in this familiar and contingent social context. The visual system is the least mature at birth, so given the hierarchical organization of the sensory systems, 7 direct visual stimulation would be emphasized the least. Early tactile stimulation (stroking/massage) in the preterm infant can enhance later visual information processing. 17 Soft, rhythmic talking to a baby brings about and sustains a quiet/alert state, which in turn invites a response (voice, touch). This type of contingent response by a person to the baby's early efforts is the hallmark of successful early intervention.
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