The Fetus &&&&&&&&&&&&&& Atypical Perinatal Sensory Stimulation and Early Perceptual Development: Insights from Developmental Psychobiology

The Fetus &&&&&&&&&&&&&& Atypical Perinatal Sensory Stimulation and Early Perceptual Development: Insights From Developmental Psychobiology

Robert Lickliter, PhD infants.These advances in our understanding of the perinatal period have in large part come from work with animal subjects and have highlighted the dynamic, multiply determined nature of Comparative studies utilizing avian and mammalian embryos and early development.10 For example, psychobiological and develop- neonates have proven particularly useful in exploring how alterations in mental research with animal embryos and infants has repeatedly sensory experience during the perinatal period can affect subsequent shown that manipulating perinatal sensory experience (by either development.This article reviews research drawn from comparative enhancement or deprivation of sensory stimulation) can result in developmental psychobiology and concludes that the effects of modified several possible outcomes, ranging from facilitation to interference sensory stimulation on perceptual and behavioral development depend on with normal patterns of early perceptual and behavioral several related factors, including the timing of stimulation relative to the development.In light of this body of evidence, simple black and developmental stage of the young organism, the overall amount of sensory white predictions regarding the developmental effects of more or stimulation provided or denied, and the type of sensory stimulation less sensory stimulation on preterm infants seem suspect.Although presented.Directions for future research on the care of the high-risk infant it is certainly not always clear why manipulation of sensory are discussed. experience shows beneficial results under some conditions but Journal of Perinatology 2000; 20:S45±S54. detrimental effects under other conditions, such differences in outcome are beginning to be better understood, particularly in light of our growing appreciation of the dynamic nature of As many readers of this issue are aware, there is continuing neuroembryological development.How individual sensory mod- controversy regarding the potential benefits and hazards of providing alities relate to one another and how their functions are integrated supplemental sensory stimulation to preterm infants.1±9 This in the brain as a result of early experience have been the subjects controversy regarding the effects of infant stimulation has been of increasing research attention over the last decade.11 ± 19 In this fueled in part by historical swings in the prevailing view of what kind article I briefly review recent psychobiological research concerned of care is appropriate for preterm infants.These views have ranged with the roles of sensory experience on the emergence of early from the perceived importance of minimal handling and reduced perceptual organization and consider possible implications of this stimulation of preterms on one end of a continuum to the value of body of work for the care of the high-risk infant. providing supplemental tactile, vestibular, auditory, or visual stimulation (either alone or in combination) in promoting normal development at the other end of the continuum.The varied positions THE SEQUENCE OF SENSORY SYSTEM DEVELOPMENT regarding the hazards and benefits of the high-risk infant's All sensory systems begin to develop prenatally in birds and exposure to various amounts and types of sensory stimulation have, mammals and, in precocial species (including humans), are however, rarely been guided by either developmental theory or capable of functioning before birth.20,21 In addition, the prenatal empirical research. environment of avian and mammalian species is rich in tactile, In recent years, conceptual advances in our understanding of vestibular, chemical, and auditory sensory stimulation.22 ± 25 neural and behavioral development during the perinatal period However, as first pointed out by Gottlieb,21,26 onset of function within have provided new insights that can inform the issue of what kind the various sensory modalities does not occur simultaneously and how much sensory stimulation should be available for preterm during early development but rather proceeds in an invariant and sequential pattern (tactile!vestibular!chemical!auditory !visual), which appears to hold whether the young of a Department of Psychology, Virginia Polytechnic Institute and State University, Blacksburg, VA particular species are born in a precocial or altricial condition.Of 24061. course, in precocial infants the capacity for auditory and visual Address correspondence and reprint requests to Robert Lickliter, PhD, Department of Psychology, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061. function develops prenatally, whereas in altricial infants auditory and visual sensitivity does not emerge until after birth or The writing of this article was supported by grants RO1 - MH62225 and KO2 - MH01210 from the National Institute of Mental Health. hatching.27 As highlighted by Gottlieb, the fact that the sensory Journal of Perinatology 2000; 20:S45 ± S54 # 2000 Nature America Inc.All rights reserved.0743-8346/00 $15 www.nature.com/jp S45 Lickliter Perinatal Sensory Stimulation

systems of birds and mammals do not become functional at the In the ensuing years since the appearance of this novel view of same time in early development raises the interesting question of early perceptual development, researchers working with both altricial how sensory systems and their different stimulation histories might and precocial animal infants have provided a growing body of influence one another during the perinatal period.For example, it evidence in support of the importance of developmental sensory is possible that sensory deprivation (or sensory enhancement) limitations to early perceptual organization and behavioral within a late-developing sensory system (i.e., the visual system) development.31 ± 39 This body of comparative work has taken could result in either the acceleration or deceleration of the advantage of the benefits that animals provide for developmental development of behavior mediated by earlier developing sensory research, including precise experiential control and the ability to systems (i.e., olfactory, auditory). supplement behavioral measures with neurophysiological manip- ulations and measures.As reviewed below, animal research has provided several advances in our understanding the nature of early DEVELOPMENTAL LIMITATIONS OF SENSORY perceptual development, including the importance of the amount EXPERIENCE and type of sensory experience provided during perinatal Following Gottlieb's initial insight, several papers appeared over a development 32,33,39 ± 41 and the strong intermodal linkages of the decade ago outlining what was then a somewhat radical view of early sensory modalities during perinatal development.38,42 ± 44 We now know perceptual development.These papers were concerned with the that experiential input to one sensory modality cannot be examined amount and type of sensory stimulation present during various in isolation, as the effects of sensory experience not only influence the stages of early development.The authors of these papers were particular modality in question, but also other developing modalities developmental psychobiologists working with animal infants and as well, both before and after birth or hatching.45,46 they each explored implications of the notion that the relative immaturity of sensory during prenatal and early postnatal development and the resulting limitations of sensory input might be PERINATAL LINKAGES OF THE SENSORY SYSTEMS an important feature of subsequent perceptual and behavioral In both altricial and precocial animal infants the visual modality development.28 ± 30 For example, Turkewitz and Kenny 29 argued that does not normally become functional until after birth or hatching. sensory limitations associated with the perinatal period are likely Thus, unlike the other sensory modalities, under normal conditions adaptive for the young organism, because they serve to reduce the of development there is typically no prenatal visual stimulation of the amount and type of information embryos or infants have to deal visual system regardless of the organism's level of precocity (with the with.They suggested that during early development sensory exception of spontaneous neural firing, which is essential for normal limitations resulting from immature sensory systems both reduce neural development 47 ).As a result of this pattern of sensory system available stimulation and mediate the timing of the introduction of development, under normal conditions the earlier developing stimulation to the embryo or fetus, thereby reducing and regulating auditory system becomes functional and differentiates without the amount of competition between maturing sensory modalities.In prenatal competition from the later developing visual system. other words, the gradual and sequential onset of function within the Despite the unique developmental status of the precocial infant's modalities allows for the development of initial functioning in each visual system (i.e., the only system to become functional after birth sensory modality without competing stimulation from later or hatching), the various influences of emerging visual experience developing sensory systems. on postnatal perceptual organization remains unclear.Work with From this perspective, immature sensory systems are not animal subjects has shown, however, that unusually early handicaps that must be overcome but are adaptive and necessary for (prenatal) visual experience (and the resulting early onset of visual normal (i.e., species-typical) sensory development and perceptual stimulation) can alter the subsequent postnatal responsiveness of learning.29,30 Without the limited sensory functioning associated with both the visual system and the earlier developing olfactory and the perinatal period, a later developing system could potentially auditory systems, which normally function prenatally in the absence interfere with earlier developing systems when the latter were still of patterned external input to the visual system.32 ± 34 For example, undergoing rapid development.This hypothesis suggests that precocial bird embryos exposed to unusually early visual experience premature or unusually early sensory experience in a later show accelerated onset of visual responsiveness to maternal cues, but developing system (e.g., vision) could serve to interfere with show a decline in auditory responsiveness to maternal cues.34,35 functioning of an earlier developing sensory system (e.g., olfactory Similarly, altricial rat pups provided unusually early visual or auditory).Spear 28 applied this notion to the early postnatal experience show accelerated visual responsiveness, but a decline in condition of altricial neonatal rats, arguing that ``if this animal olfactory responsiveness in the weeks following birth.33 These results could be made to see and hear, it seems at least as likely that severely suggest that specific limitations in the input to sensory systems maladaptive behavior would result due to distraction from the more during the perinatal period can serve to organize early perception conventional events (e.g., odors) upon which its survival depends'' and that prematurely introducing sensory input can, at least under (p.335). some conditions, interfere with the emergence of normal patterns of

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organization.These results highlight the dynamic nature of early manipulation of early sensory experience has focused on the perceptual organization and underscore the notion that when intramodal impact of postnatal sensory deprivation, in which sensory stimulation is provided can be as influential as what type of particular sensory experience is withheld at a time when it would stimulation is provided.48 ordinarily be available to the young organism.54 ± 57 In the general Research with human infants has tended to overlook the possible sense, this body of work has consistently demonstrated the negative influences of such timing issues on early perceptual development.In impact of dramatically reduced or attenuated sensory stimulation on particular, the dynamic nature of the relationship between the state normal or species-typical patterns of perceptual and behavioral of development of already functioning sensory systems and the development.In particular, the research on sensory deprivation has introduction of additional sensory input from newly emerging documented the negative intramodal consequences (both neural systems is poorly understood for human infants.Preterm infants are and behavioral) of a lack of normally occurring sensory routinely subjected to patterned light at a developmental age when stimulation.However, relatively little research attention has been they would not normally be exposed to such visual stimulation. paid to the intramodal or intermodal consequences of providing Likewise, preterm infants typically receive enhanced amounts and sensory experience earlier in development that when it would levels of auditory stimulation and reduced vestibular stimulation at a ordinarily be available (a topic of considerable relevance to the time in development when they would normally experience filtered preterm human newborn).Although there are a number of auditory stimulation and regular vestibular stimulation from the plausible reasons for this disparity, it is certainly the case that mother's movements.The intramodal and intermodal consequences experiments involving unusually early or augmented sensory of such altered patterns of sensory experience are only beginning to experience are often difficult to conduct, especially when prenatal be explored and comparative work with animal subjects can provide manipulations are involved. useful insights and guidelines in this regard. EARLY EXPOSURE STUDIES COMPARATIVE APPROACHES TO EARLY PERCEPTUAL In recent years, however, a number of studies have appeared utilizing DEVELOPMENT an ``early exposure'' paradigm to examine the role of enhanced The field of infant perceptual development has typically focused on perinatal sensory experience on subsequent perceptual and demonstrating the age at which babies manifest particular behavioral development.In a general sense, this research with both perceptual skills 15,17,49 and has only begun to focus on the altricial and precocial animal embryos and neonates has exposed the developmental background showing how such perceptual skills are young organism to unusually early or enhanced sensory experience achieved.This state of affairs is no doubt due in large part to the and then assessed the infant's subsequent perceptual and behavioral inherent limitations of research with humans.Experiential development.Results from this work have demonstrated that the manipulations of human fetuses and neonates are necessarily amount and type of sensory stimulation encountered during the limited in scope and duration, and traditional experimental prenatal period can actively shape infants' early perceptual manipulations used with animal subjects are generally prohibited. organization.More specifically, early exposure studies with both Animal research can provide a useful avenue for asking questions avian and mammalian species have highlighted the importance of about the nature of early perceptual and behavioral development, as normal patterns (in terms of the type and amount of sensory they provide simpler and more experimentally accessible systems that stimulation) of prenatal sensory experience to several species-typical can be systematically probed to identify general principles and postnatal perceptual capabilities, including recognition and processes of development.50 ± 52 In addition, the study of a range of preference for maternal olfactory, auditory, and visual cues,33,34,58 the organisms can allow for the cataloguing and comparison of ability for prenatal and early postnatal auditory learning,32,37,59,60 and similarities and differences that can be highly informative for sensitivity to temporal and spatial features of sensory stimulation.61,62 understanding the development of infant perception and for Although space constraints prevent a detailed review of each of these generating specific developmental hypotheses that can then be tested individual studies and their results, it is clear that early sensory with humans.10,53 enhancement does not always lead to beneficial consequences on One obvious advantage of the use of animal subjects to study the early development.Sensory input introduced before the time that this specific effects of sensory experience during the perinatal period is the experience would normally occur can, in fact, interfere with the ability to readily alter both the timing and amount of particular young organism's perceptual and behavioral development. sensory stimulation available to the developing embryo or fetus. It is important to note that most of the research on the topic of Comparative developmental studies can employ sensory deprivation, the dynamic nature of early perceptual development has used sensory augmentation, or sensory substitution techniques during the precocial bird species, in large part because precocial avian embryos prenatal period to explore the specific experiential conditions show the same functional status of sensory systems as late-term necessary for the normal development of perception.To date, the human fetuses and because the procedure of providing unusually large majority of studies concerned with the experimental early or augmented sensory stimulation is relatively easy to

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accomplish with avian embryos.Because their prenatal development stimulation or unusually early visual stimulation show a decreased takes place in ovo rather than in utero, birds are much more sensitivity to maternal auditory cues and increased responsiveness to accessible to embryonic manipulations than are mammalian species. maternal visual cues following hatching when compared to For example, it is possible to give the avian embryo premature unmanipulated control birds.Lickliter 35 found that under normally exposure to patterned visual stimulation or enhanced auditory occurring perinatal conditions, the auditory modality of quail stimulation by the simple experimental procedure of removing the chicks has functional priority over the later developing visual shell and inner-shell membrane over the air space of the egg several modality.In a task where maternal auditory and visual days before hatching, thereby exposing the head of the embryo.This information was made to compete for the newly hatched chick's ready accessibility of the precocial avian embryo during the late attention, normally reared chicks consistently preferred maternal stages of prenatal development allows multiple experimental probes auditory cues over both static and moving maternal visual cues.In aimed at identifying the various features of perinatal sensory contrast, chicks that received unusually early visual experience as experience, which can facilitate or interfere with the emergence of embryos demonstrated an altered pattern of postnatal sensory normal patterns of early perceptual organization.36 salience, preferring maternal visual cues over auditory cues in the days following hatching.These results and those from related studies 33,44 suggest that species-typical patterns of prenatal sensory SENSORY EXPERIENCE AND STIMULUS SALIENCE experience is an important determinant of species-typical postnatal Comparative developmental research concerned with the organizing preferences.Animal infants that receive enhanced auditory or visual role of sensory experience has consistently revealed that the experience before birth or hatching are somehow ``reoriented'' in sequential and successive emergence of function across the various their responsiveness to auditory and visual stimulation when sensory systems can affect the salience of various types of sensory compared to normal controls.How this shift occurs remains poorly information by influencing the embryo and neonate's selective understood, but several related features of (1) sensory stimulation attention.32,35,37,39,52 Although precocial infants are born or hatched with and (2) organismic variables such as state and arousal level seem relatively well-developed sensory capacities, all have had limited to be involved, as briefly reviewed below. sensory functioning at some stages of their prenatal development and these developmental limitations appear to play an important role in how the young organism responds to perceptual input during the STIMULATIVE FEATURES CONTRIBUTING TO DEVELOPMENTAL OUTCOME perinatal period.29,30,63 As a case in point, responsiveness to auditory information has Taken together, the varied results from animal experimentation been shown to have functional priority over responsiveness to visual suggest that the effect(s) that manipulations or alterations of information during the early stages of the postnatal period in a perinatal sensory stimulation have on early perceptual and number of precocial animal species.These findings conform to what behavioral development range from facilitation of normal outcomes is known about the neuroembryological development of the sensory to interference with these same outcomes.These different endpoints systems, in that the auditory system develops prenatally in advance of seem to depend on a number of related factors, including (1) the the visual system in both precocial birds and mammals, including amount of stimulation provided or denied the young organism, (2) humans.21,64 As a result, at the time of birth or hatching these two the type of sensory stimulation presented, and (3) the timing of the sensory systems have had different amounts of prenatal experience. presentation of stimulation relative to the stage of the The precedence of auditory over visual experience may explain why organism.38,40,76 ± 78 These stimulative factors and their influences precocial infants typically utilize auditory over visual information to appear to interact and to change with the organism's context, initially direct their perceptual and social preferences.Because of its behavioral state, and developmental history.43,79 ± 81 earlier development, the auditory system is more structurally and Although this developmental scenario may sound overwhelmingly functionally differentiated and thus has an advantage when auditory complex and inaccessible to empirical study, such complexity can be and visual input compete for the infant's attention.35 For example, experimentally unraveled with an explicit focus on the nature of the the bobwhite quail maternal call is an extremely compelling relationships within and between internal and external variables.82,83 stimulus for young quail hatchlings, easily outweighing the effects of The idea that control for developmental outcomes resides in the species-typical maternal visual cues during early postnatal nature of the relationships within and between internal and external development.65 A similar pattern of the initial salience of auditory variables (rather than in any one individual factor) is still not over visual information has also been reported for domestic chicks,66 widely appreciated in the behavioral sciences, but has important ducklings,67 ± 69 rats,70 lambs,71 and human infants.72 ± 74 implications for the study and care of the high-risk infant.These Several studies manipulating either prenatal auditory or considerations include (1) a deeper appreciation that perceptual prenatal visual experience 34,35,44,75 have indicated that this typical and behavioral development is a process that is ``situated'' (i.e., pattern of the initial salience of auditory over visual information takes place in a context) and (2) a need for experimentally can be redirected.Quail embryos provided augmented auditory specifying how external stimulative events coact with organismic

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factors to exert particular effects on specific traits or characteristics at stimulation and patterned visual stimulation).Although important particular times in development. advances are being made,23,87 we currently know little about what As a case in point, based on their findings from enhanced constitutes the normal or typical range of stimulation optimal for the prenatal vestibular stimulation in duck embryos, Radell and human infant's perceptual and behavioral development.As a result, Gottlieb 38 have argued that the amount of stimulation an organism we also know little about what constitutes appropriate ranges or encounters in its typical developmental context may be optimal for thresholds of stimulation (be it tactile, vestibular, auditory or its species-specific perceptual development.In other words, sensory visual) for the high-risk infant.More normative research is clearly experience that falls within a range of stimulation typical for that needed in this important area. species should not interfere with intersensory development, and mildly enhanced levels of stimulation may maintain or even facilitate typical perceptual development.This hypothesis would ORGANISM-BASED FEATURES CONTRIBUTING TO DEVELOPMENTAL OUTCOME account for the findings of Lickliter,34 in which moderately enhanced prenatal visual stimulation (e.g., 10 min/hr) led to How does altering the amount of sensory stimulation provided the accelerated visual responsiveness in quail chicks.However, if some neonate result in increased or decreased sensitivity to specific sensory optimal range of stimulation exists, then stimulation that exceeds input? One underlying variable that likely mediates the observed the optimal range should potentially cause functional deficits in differences in the embryo or infant's sensitivity to specific sensory normal patterns of perceptual functioning.Indeed, Sleigh and input is the overall arousal level of the developing organism.Based Lickliter 84 demonstrated that quail embryos exposed to substantially on his work with domestic chicks, Gray 88 argued that responsiveness increased amounts of prenatal visual stimulation (e.g., 40 min/hr) to experimental manipulations of sensory experience is directly show significant delays in postnatal visual functioning. influenced by the arousal level of the organism.Excessive or reduced Similar work concerned with auditory responsiveness in precocial arousal levels are generally found to be associated with poor auditory birds lends further support to the existence of some optimal range of perceptual performance, whereas a moderate level of arousal is perinatal stimulation necessary for species-typical perceptual associated with peak performance on auditory tasks.Efforts toward development.32,41,43 For example, Lickliter and Hellewell 37 found that uncovering how the arousal level of the organism may alter bobwhite embryos exposed to an individual bobwhite maternal call sensitivity or attention to specific sensory inputs have been provided readily learn this call when the call is presented nonconcurrently by work with both animal and human infants.For example, with 10 min/hr of patterned light.In contrast, embryos do not Lewkowicz and Turkewitz 81 found that prestimulation of human exhibit prenatal auditory learning when the maternal call is newborns with a pulse of white noise resulted in infants' increased presented concurrently with visual experience.In this example, the looking at a dimmer light and decreased looking at a brighter light effectiveness of the embryo's prenatal exposure to an individual in comparison to unstimulated infants.In a subsequent experiment, maternal call was dependent on the absence of exposure to infants exposed to auditory stimulation immediately preceding or concurrent visual input (for a parallel example with ducklings, see presented concurrently with visual stimuli significantly preferred less Ref. 3 ).Similarly, Radell and Gottlieb 38 demonstrated that duckling intense visual stimulation when compared to controls.89 Parallel embryos failed to learn an individual maternal call when exposed results have been obtained utilizing either auditory or visual concurrently to augmented vestibular stimulation, but demonstrate stimulation before testing.80 auditory learning when the amount of vestibular stimulation In a similar vein, Gottlieb 59 found that ducklings' arousal level provided embryos was reduced to more closely approximate their and sensitivity to specific auditory stimulation presented in the period normal range of prenatal vestibular stimulation.Taken together, following hatching was dramatically affected by the presence or these findings suggest that when overall amounts of stimulation absence of tactile stimulation.Ducklings denied tactile stimulation exceed a certain threshold level, prenatal auditory learning capacity from broodmates did not learn an individual maternal call, whereas can be compromised.Deviations either above or below the normal or control subjects allowed normal levels of tactile experience readily typical range of sensory stimulation (either within or across learned the maternal call.Importantly, ducklings deprived of tactile modalities) apparently negatively impact the young organism's contact demonstrated higher levels of arousal (as measured by ability to attend to available information in the perinatal distress vocalizations and time spent awake) than control ducklings. environment.41 Parallel studies with bobwhite quail chicks examining the effects of This insight raises obvious questions regarding the design of care increased amounts of sensory stimulation have reported similar environments for high-risk, preterm human infants,85,86 in that the negative outcomes.41,42 Taken together, these studies of human and premature infant typically receives decreased amounts of some types animal infants suggest that changing the arousal level of infants of sensory stimulation normally present in the intrauterine through (1) substantially enhanced vestibular, auditory, or visual environment (vestibular stimulation from maternal movements) stimulation or (2) attenuated tactile and vestibular stimulation can and increased amounts of other types of stimulation not normally alter their subsequent perceptual preferences.These results again present until later stages of development (unfiltered auditory emphasize that early perceptual organization is ``context sensitive.''

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That is, emerging perceptual capacities and preferences can be the parental call or voice, they appear unable to learn the parental strongly influenced or modified by specific stimulative features of the vocalization.When visual or vestibular experience is made to infant's immediate surround.These features include the overall alternate with exposure to the parental vocalization (that is, amount of stimulation provided to the young organism, as well as presented unimodally and nonconcurrently), embryos learn an the type of sensory stimulation and its influence on the infant's state individual call and prefer that familiar call over another unfamiliar of arousal. maternal call for at least 24 hours following exposure.32,37,38 Although more research is needed to better understand and predict such an ``interference effect'' of bimodal prenatal sensory DIFFERENTIAL EFFECTS OF UNIMODAL VERSUS stimulation on normal patterns of perceptual responsiveness and MULTIMODAL SENSORY STIMULATION learning abilities, these results suggest that whereas chicks In keeping with the theme of the importance of the type of sensory apparently require postnatal bimodal sensory stimulation for the stimulation present in the perinatal environment, a potentially emergence of normal patterns of perceptual responsiveness,90,94 such important feature of early sensory experience is that it can be bimodal stimulation can lead to detrimental effects earlier in multisensory in nature.That is, the fetus or neonate may experience development.Once again, this raises important questions regarding sensory stimulation of the vestibular, somesthetic, chemical, or the care environment of the high-risk infant, especially in regards to auditory (and the visual following birth) modalities either the specific combinations and timing of sensory stimulation provided simultaneously or sequentially.Recent evidence from animal or denied. experimentation at both the neural and behavioral level of analysis The view that unimodal and multimodal stimulation are suggests that there is a functional distinction between unimodal functionally distinct during the perinatal period is in keeping with a (stimulation presented to one modality) and multimodal theme that runs throughout this article, namely that the perinatal (stimulation presented to two or more modalities) exposure during period is a unique period of development.Before birth or hatching, early development.For example, a recent study assessed the effects of the embryo or fetus does not appear to be particularly competent at postnatal unimodal versus bimodal sensory stimulation on quail attending to simultaneous sensory stimulation from two or more chicks' responsiveness to maternal auditory and visual information.90 modalities.Of course, by the very design of the egg or uterus, the The results indicated that concurrent postnatal auditory and visual developing embryo or fetus resides in a relatively sequestered and sensory experience appears to underlie the emergence of early simplified environment.Our present knowledge suggests that both intersensory integration.Chicks provided only unimodal maternal the limited sensory capacities of the young organism and its experience (either auditory or visual) following hatching showed constrained developmental context combine to minimize simulta- delayed patterns of responsiveness to maternal cues when compared neous or concurrent presentation of multiple sources of information. to chicks receiving integrated audio/visual experience.Chicks that Said another way, the order and constraint typically provided by the received temporally disparate maternal auditory and visual cues sequential onset of sensory function prenatally and the simplified (presented at different times) also failed to show normal perceptual nature of the prenatal environment combine to effectively reduce the preferences, indicating an apparent need for concurrent auditory and amount and timing of competition between rapidly maturing visual experience in the days following hatching.These behavioral sensory systems.This scenario is in keeping with Turkewitz and findings, coupled with similar results from the neurophysiological Kenny's 29 theory of early perceptual development discussed earlier level of analysis 19,91 ± 93 suggest that postnatal sensory information that centers around the role of developmental limitations of sensory presented concurrently in two modalities is functionally distinct from experience during sensitive stages of the perinatal period.In the same information presented unimodally. particular, limitations of sensory input appear to be a key In contrast, the nature of the relationship between unimodal and mechanism by which the quantity and/or quality of sensory multimodal stimulation during the prenatal period has received little stimulation available to the young organism is regulated, thereby research attention and remains poorly understood.Typically, reducing competition between maturing sensory modalities. auditory experience is available prenatally for both precocial birds The emergence of visual functioning and the increasingly and mammals, but visual experience is not available until after birth multimodal nature of sensory stimulation following birth signal a or hatching.Might there be some necessary level of unimodal major shift forward in the nature of the young organism's capacity auditory stimulation in the period before birth or hatching (and the and experiential milieu.We currently know relatively little about the onset of visual experience) for the emergence of normal patterns of specifics of the intricate relationship between prenatal and postnatal postnatal perceptual functioning? This question remains relatively periods of development for human neonates and a core of basic unexplored for both animal and human infants, but the few existing behavioral and physiological data on the attentional, sensory, motor, comparative findings reviewed earlier do raise questions and possible and social factors associated with this shift are needed to better guide directions for future research.For example, if avian embryos are our views and policies regarding the care of the high-risk infant. exposed to bimodal stimulation (i.e., the addition of visual Does the fact that the developing auditory system of the preterm has stimulation or vestibular stimulation) during prenatal exposure to less time to function without competition from the visual system

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have implications for subsequent perceptual and behavioral the environment and the structure of the organism coact to organization? The animal literature reviewed in this article suggests determine behavioral outcome. that this could be the case.Can the unusually early bimodal Given that perceptual and behavioral development always (auditory-visual) stimulation experienced by the premature infant depends on coactions involving the organism and its context, the shift the infant's attention to more abstract, amodal properties of task of defining the relevant developmental resources of the sensory stimulation (including temporal and spatial features of organism's internal and external milieu becomes the necessary stimulation) and away from more modality-specific features (like foundation of any systematic analysis of behavioral capacity.It is the pitch and timbre of auditory stimulation) in the period following important to acknowledge that only first steps have been made in birth? These and other potential consequences of the premature this difficult and often tedious task and much work remains to be infant's reduced experience with unimodal stimulation during early done in this quest, both for full-term and premature infants.For development remain to be explored. example, precise and detailed information about the experiential stimulation present during the perinatal period is needed if we are to begin to understand what features of experience are most likely IMPLICATIONS AND APPLICATIONS OF COMPARATIVE to facilitate or interfere with normal patterns of early development. RESEARCH Contributions from developmental psychobiology, physiology, Although it is certainly clear that more sensory stimulation is not neurobiology, fetal medicine, and neonatology can be integrated to necessarily better, at present we remain relatively uninformed in provide more fruitful questions, methods, and answers regarding: terms of when, how much, and what type of stimulation regimes are (1) what is the nature and range of sensory stimulation patterns best suited to promote optimal outcomes during the various present for the fetus prenatally, (2) what happens to these developmental stages associated with the perinatal period.More stimulation patterns after birth, and (3) what happens to the extensive and focused research with both animal and human nature and range of sensory stimulation when birth occurs early? subjects is needed to successfully achieve such a specific level of This much needed knowledge base will enrich our understanding of insight and understanding.Nonetheless, several general insights can how behavioral capacity emerges through dynamic transactions be gleaned from the body of psychobiological work briefly reviewed in occurring within the organism±environment system and can this article and applied to the issue of the care of the high-risk provide important avenues of insight and guidance in our care of infant.These include: (1) early development is coactional or the high-risk infant. multidimensionl, that is, no individual level, component, or experience necessarily has causal priority or acts in isolation in influencing developmental outcome; (2) early development is Acknowledgements nonlinear, that is, the intricacies of developmental causal networks I thank Lorraine Bahrick and Gilbert Gottlieb for their constructive comments on the are not typically unidirectional and patterns of influence are not manuscript. always obvious or straightforward; (3) early development is experience-dependent, that is, outcomes and abilities emerge from References the young organism's ongoing encounters with its world; and (d) 1.Avery GB, Glass P.Thegentle nursery: developmental intervention in the early development is context-sensitive, that is, the fetus or infant's NICU.J Perinatol 1989;9:204±206. emerging capacities are strongly influenced or modified by specific 2.Blackburn S.Fosteringbehavioral development of high-risk infants.JObstet features of its immediate surround. 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