Intersensory experience and early perceptual development: The role of spatial contiguity in bobwhite quail chicks' responsiveness to multimodal maternal cues

In contrast to the large body of work on young infants' capacity to perceive temporarilly based intersensory relations, little research has been done on the role of spatial contiguity in the development of audio-visual integration. This study examined the effects of early postnatal sensory experience on an avian neonate's responsiveness to the spatial contiguity between maternal auditory and visual cues. Specifically, we assessed whether a bobwhite quail chick's ability to respond to the correspondence between the location of auditory and visual events is affected by its sensory-stimulation history. Results revealed that chicks denied species-typical auditory or visual experience in the period immediately following hatching showed altered patterns of responsiveness to maternal auditory and visual cues. In particular, chicks that received modified postnatal sensory experience demonstrated a higher tolerance for audio-visual spatial discrepancy than did control chicks. These results provide evidence of the important role of sensory experience in the emergence of intersensory integration during the perinatal period and highlight the role of spatial information in early perceptual responsiveness to maternal cues. © 1996 John Wiley & Sons, Inc.     

The influence of prenatal tactile and vestibular stimulation on auditory and visual responsiveness in bobwhite quail: A matter of timing

The fact that the sensory systems do not become functional at the same time during prenatal development raises the question of how experience in a given modality can influence functioning in other sensory modalities. The present study exposed groups of bobwhite quail embryos to augmented tactile and vestibular stimulation at times that either coincided with or followed the period of onset of function in the later-developing auditory and visual modalities. Differences in the timing of augmented prenatal stimulation led to different patterns of subsequent auditory and visual responsiveness following hatching. No effect on normal visual responsiveness to species-typical maternal cues was found when exposure to tactile and vestibular stimulation coincided with the emergence of visual function (Days 14-19), but when exposure took place after the onset of visual functioning (Days 17-22), chicks displayed enhanced responsiveness to the same maternal visual cues. When augmented tactile and vestibular stimulation coincided with the onset of auditory function (Days 9-14), embryos subsequently failed to learn a species-typical maternal call prior to hatching. However, when given exposure to the same type and amount of augmented stimulation following the onset of auditory function (Days 14-19), embryos did learn the maternal call. These findings demonstrate that augmented stimulation to earlier-emerging sensory modalities can either facilitate or interfere with perceptual responsiveness in later-developing modalities, depending on when that stimulation takes place.     

Order-dependent timing of unimodal and multimodal stimulation affects prenatal auditory learning in bobwhite quail embryos

This study examined the relationship between unimodal and multimodal sensory stimulation and their effects on prenatal auditory learning in bobwhite quail embryos. Embryos exposed to a maternal call in the 24 hr prior to hatching (unimodal condition) significantly preferred this familiar call over an unfamiliar call in postnatal testing, but failed to demonstrate this preference when the maternal call was presented concurrently with non-synchronized patterned light (multimodal condition). To further explore this interference effect, we provided one group of embryos concurrent exposure to a maternal call and patterned light for 12 hr followed by 12 hr exposure to the call alone (multimodal-->unimodal call). This group failed to prefer the familiar call during postnatal testing. In contrast, reversing the order of presentation during prenatal exposure (unimodal call-->multimodal) led a second group of subjects to significantly prefer the familiar call, suggesting that the order-dependent timing of sensory stimulation can significantly impact prenatal auditory learning. Experiment 3 examined the influence of modality versus timing of sensory stimulation on prenatal auditory learning by providing three groups of embryos with exposure to a maternal call during the 12 hr prior to hatching and by varying the duration of visual stimulation. Results indicate that 12 hr unimodal exposure to patterned light does not support prenatal auditory learning when it is followed by 12 hr exposure to multimodal stimulation (light-->multimodal), but can facilitate prenatal auditory learning when it is followed by unimodal exposure to the call alone (light-->call). Results are discussed in terms of intersensory relationships during perinatal development.     

Contextual determinants of auditory learning in bobwhite quail embryos and hatchlings.

This study examined the ability of bobwhite quail embryos and hatchlings to learn an individual bobwhite maternal call. Results revealed that embryos could learn an individual maternal call and remember that call for at least 24 hr following exposure. In contrast, hatchlings reared socially in groups of same-age chicks during postnatal exposure to a maternal call did not demonstrate a preference for that familiar call at 24 hr following exposure. However, individual auditory recognition was exhibited by hatchlings reared in social isolation, suggesting that the perceptual and social complexity of the postnatal situation can disrupt or interfere with early auditory learning. Additional support for this view was the finding that embryos exposed to unusually early visual stimulation during prenatal exposure to a maternal call also failed to prefer that familiar maternal call in subsequent choice tests. The idea that early auditory learning capacity is determined more by context and experience rather than the organism's specific age or stage of development is discussed.     

Augmented prenatal tactile and vestibular stimulation alters postnatal auditory and visual responsiveness in bobwhite quail chicks.

The fact that the sensory systems do not become functional at the same time during early development raises the question of how sensory systems and their respective stimulative histories might influence one another. Previous studies have shown that unusually early visual experience can alter subsequent responsiveness of both the visual system and the earlier developing olfactory and auditory systems. The question remains as to the extent which modified stimulation to an earlier developing system can also result in changes in responsiveness in later developing sensory systems. This study examined the effects of augmented prenatal tactile and vestibular stimulation on bobwhite quail chicks' postnatal visual and auditory responsiveness to maternal cues. Results indicate that augmented prenatal tactile and vestibular stimulation can alter postnatal perceptual responsivensss in the later developing auditory and visual sensory systems. Chicks exposed to augmented prenatal proximal stimulation continued to respond to maternal auditory cues into later stages of postnatal development and failed to demonstrate responsiveness to maternal visual cues in the days following hatching. However, augmented tactile and vestibular stimulation did not appear to affect prenatal auditory learning of an individual maternal call. These findings indicate a strong but selective pattern of influence between the sensory modalities during the prenatal period and support the view that substantially increased amounts of prenatal sensory stimulation can interfere with the emergence of species-typical perceptual functioning.     

Effects of redundant and nonredundant bimodal sensory stimulation on heart rate in bobwhite quail embryos

Research with both animal embryos and human infants has provided evidence that information presented redundantly and in temporal synchrony across sensory modalities (intersensory redundancy) can guide selective attention, perceptual learning, and memory during early development. How this facilitation is achieved remains relatively unexamined. This study examined the effects of redundant versus nonredundant bimodal stimulation on a measure of physiological arousal (heart rate) in bobwhite quail embryos. Results show that quail embryos exposed to concurrent but nonredundant auditory and visual stimulation during the late stages of incubation exhibit significantly elevated heart rates following stimulus exposure and during stimulus reexposure when compared to embryos exposed to redundant and synchronous audiovisual stimulation, unimodal auditory stimulation, or no supplemental prenatal sensory stimulation. These findings indicate a functional distinction between redundant and nonredundant bimodal stimulation during early development and suggest that nonredundant bimodal stimulation during the prenatal period can raise arousal levels, thereby potentially interfering with the attentional capacities and perceptual learning of bobwhite quail. In contrast, intersensory redundancy appears to foster arousal levels that facilitate selective attention and perceptual learning during prenatal development.     

Biased embryos: Prenatal experience alters the postnatal malleability of auditory preferences in bobwhite quail

Many precocial birds show a robust preference for the maternal call of their own species before and after hatching. This differential responsiveness to species-specific auditory stimuli by embryos and neonates has been the subject of study for more than four decades, but much remains unknown about the dynamics of this ability. Gottlieb [Gottlieb [1971]. Development of species identification in birds: An enquiry into the prenatal determinants of perception. Chicago/London: University of Chicago Press.] demonstrated that prenatal exposure to embryonic vocalizations serves to canalize the formation of species-specific preferences in ducklings. Apart from this, little is known about the features of the developmental system that serve to canalize such species-typical preferences, on the one hand, and generate novel behavioral phenotypes, on the other. In the current study, we show that briefly exposing bobwhite quail embryos to a heterospecific Japanese quail (JQ) maternal call significantly enhanced their acquisition of a preference for that call when chicks were provided with subsequent postnatal exposure to the same call. This was true whether postnatal exposure involved playback of the maternal call contingent upon chick contact vocalizations or yoked, non-contingent exposure to the call. Chicks that received both passive prenatal and contingent postnatal exposure to the JQ maternal call redirected their species-typical auditory preference, showing a significant preference for JQ call over the call of their own species. In contrast, chicks receiving only prenatal or only postnatal exposure to the JQ call did not show this redirection of their auditory preference. Our results indicate that prenatal sensory stimulation can significantly bias postnatal responsiveness to social stimuli, thereby altering the course of early learning and memory.     

Augmented prenatal visual stimulation alters postnatal auditory and visual responsiveness in bobwhite quail chicks

This study examined whether previously reported effects of altered prenatal sensory experience on subsequent acceleration of intersensory development in precocial birds are mediated by mechanisms sensitive to the overall amount of stimulation provided. Results revealed that bobwhite quail chicks exposed to substantially augmented amounts of prenatal visual stimulation show altered patterns of species-typical perceptual development. Specifically, chicks continued to respond to maternal auditory cues into later stages of postnatal development and failed to demonstrate responsiveness to maternal visual cues. Embryos also failed to demonstrate prenatal auditory learning of an individual maternal call, a behavior reliably seen in unmanipulated embryos. These findings suggest that substantially increased amounts of prenatal sensory stimulation can interfere with the emergence of species-typical patterns of postnatal intersensory functioning and lend support to the notion that sensory stimulation that falls within some optimal range maintains or facilitates normal patterns of perceptual development, whereas stimulation beyond the range of the species norm can result in intersensory interference. © 1995 John Wiley & Sons, Inc.     

Augmented prenatal auditory stimulation alters postnatal perception,arousal, and survival in bobwhite quail chicks

This study examined whether previously reported effects of altered prenatal sensory experience on subsequent acceleration of intersensory development in precocial birds are mediated by mechanisms sensitive to the overall amount of stimulation provided. Results revealed that bobwhite quail chicks exposed to substantially augmented amounts of prenatal auditory stimulation show altered patterns of species-typical perceptual development. Specifically, chicks continued to respond to maternal auditory cues into later stages of postnatal development and failed to demonstrate responsiveness to maternal visual cues. In addition, embryos exposed to substantially augmented amounts of prenatal auditory stimulation exhibited a higher level of behavioral arousal and higher mortality rates than embryos provided either moderately augmented amounts or no additional amount of prenatal auditory stimulation. These findings suggest that substantially increased amounts of prenatal sensory stimulation can interfere with the emergence of species-typical patterns of postnatal perceptual functioning and lend support to the notion that sensory stimulation that falls within some optimal range maintains or facilitates normal patterns of perceptual development, whereas stimulation beyond the range of the species norm can result in intrasensory and intersensory interference. © 1997 John Wiley & Sons, Inc. Dev Psychobiol 30: 201–212, 1997     

Premature visual stimulation accelerates intersensory functioning in bobwhite quail neonates

Recent evidence from both altricial and precocial neonates suggests that premature stimulation of a later developing sensory system may alter the functioning of earlier developing sensory systems. The present study examined the influence of prenatal visual stimulation on postnatal auditory functioning in precocial bobwhite quail chicks. Hatchlings that experienced patterned light during the 24-36 hr prior to hatching did not exhibit a naive auditory preference for their species-specific maternal call at 24 hr or 48 hr following hatching, a reliable phenomenon in chicks not receiving embryonic visual stimulation. To examine whether this lack of responsiveness resulted from enhanced intersensory functioning, hatchlings were tested for preference for both auditory and visual features of the bobwhite hen. Results indicate that prematurely stimulated chicks require species-typical auditory and visual stimulation earlier in postnatal development than do normally reared chicks to direct their filial behavior. These findings point to the importance of normally occurring developmental limitation of sensory input to early species-typical sensory/perceptual organization.     

Development of species identification in ducklings: IX. The necessity of experiencing normal variations in embryonic auditory stimulation

The domestic mallard duck embryo must be exposed to its embryonic contact-contentment call at a repetition rate of 4 notes/sec if the neonate is to show the species-typical preference for the maternal call at its normal rate (3.7 notes/sec) after hatching. Exposing the embryo to the contact call at either 2.1 notes/sec or 5.8 notes/sec is no more effective than no auditory experience at all. To determine if there is a critical period for exposure, embryos were exposed to the 4 notes/sec call either before or after hatching. Both periods proved equally effective provided only that a 48-hr “consolidation” period was allowed to intervene between stimulation and testing. That is, the birds tested 24 hr after prenatal or postnatal stimulation behaved as if they were not stimulated at all. The present study was undertaken to determine whether the curious requirement for a consolidation period is a normal developmental phenomenon or a consequence of limiting the birds to exposure to a call with an abnormally invariant repetition rate of 4 notes/sec. To that end, embryos were stimulated with the same call as before but at variable rates of 2.1, 4, and 5.8 notes/sec, as happens under normal conditions of development. In this case, the neonates had no need for a consolidation period and showed the species-typical preference at 24 hr after hatching. Thus the previous results were a consequence of an abnormally narrow range of embryonic auditory stimulation. A 2nd experiment showed that, if the birds' postnatal perception was to be normal, the embryos could not be merely exposed to the rhythmic component of the contact call, but had to experience the characteristic frequency modulation of the call as well. These results indicate that we require surprisingly detailed information about the sensory stimulation present during the usual course of development of our subject species if we are to give an appropriate interpretation to the results of early experiential and critical period manipulations. Knowledge of usual sensory-stimulative variations has not been a conspicuous feature of developmental psychobiological studies in the past.     

Effects of early and delayed visual experience on intersensory development in bobwhite quail chicks

The relative impact of early versus delayed visual experience on intersensory development was studied by manipulating the timing of visual experience of bobwhite quail (Colinus virginianus) embryos and hatchlings. Previous studies with quail chicks have revealed that: (1) Socially reared chicks require only maternal auditory cues to direct their social preferences in the first 2 days following hatching; (2) by 3 days following hatching chicks require both auditory and visual maternal cues to direct their social preferences; (3) chicks which have received unusually early visual experience as embryos require both auditory and visual cues by 24 hr following hatching, indicating an accelerated pattern of the emergence of intersensory functioning; and (4) chicks reared under conditions of attenuated social and visual experience continue to rely on matenal auditory cues alone at 4 days following hatching, indicating a decelerated pattern of early intersensory functioning. In the present study, quail chicks that received both early visual experience as embryos and delayed visual experience as hatchlings exhibited a pattern of both auditory and visual responsiveness like that seen in normally reared chicks. These results indicate that, at least under the present experimental conditions, the influence of early and delayed visual experience on perinatal perceptual development appears to be relatively comparable in effect © 1993 John Wiley & Sons, Inc.     

Effects of prenatal sensory stimulation on heart rate and behavioral measures of arousal in bobwhite quail embryos

Although a number of studies have demonstrated the effects of altered prenatal experience on subsequent behavioral development, how these effects are achieved remains a topic of enduring interest. The present study examined the immediate effects of unimodal and multimodal prenatal sensory stimulation on physiological and behavioral arousal in bobwhite quail embryos. Embryos were videotaped and their heart rate was monitored during a 4-min exposure period to (a) no supplemental sensory stimulation, (b) unimodal auditory stimulation, (c) unimodal visual stimulation, (d) two sources of concurrent auditory stimulation, or (e) concurrent auditory/visual stimulation. Results indicated that quail embryos' overall activity levels and heart rate can be significantly affected by the type of prenatal sensory stimulation provided during the period prior to hatching. In particular, multimodal stimulation increased both behavioral activity levels and heart rate compared to controls. Across the unimodal and intramodal groups, however, behavioral and physiological measures revealed different patterns of activity in response to supplemental sensory stimulation, highlighting the value of using multiple levels of analysis in exploring arousal mechanisms involved in prenatal perceptual responsiveness.     

Specific postnatal auditory stimulation interferes with species-typical visual responsiveness in bobwhite quail chicks

The effects that a manipulation of sensory experience may have on perceptual development are likely to depend on a number of factors, including the amount and the type of stimulation provided. To examine the relative influence of these stimulation factors on early perceptual organization, this study exposed bobwhite quail hatchlings to augmented amounts of bobwhite chick distress calls, bobwhite chick contentment calls, domestic chicken distress calls, or no additional auditory stimulation during the first 72 hr following hatching. Results showed that bobwhite hatchlings exposed to bobwhite chick distress calls do not exhibit species-typical visual responsiveness to maternal cues. In contrast, bobwhite hatchlings exposed to bobwhite chick contentment calls, domestic chicken hatchling distress calls, or no agumented auditory stimulation exhibited species-typical auditory and visual responsiveness to maternal cues. These results demonstrate intermodal effects of postnatal sensory stimulation and suggest that specific types of postnatal auditory stimulation, rather than simply increased amount of stimulation, are necessary to interfere with species-typical intersensory functioning.© 1994 John Wiley & Sons, Inc.     

Alarm call responsivity of mallard ducklings: VII. Auditory experience maintains freezing

Mallard ducklings (Anas platyrhynchos) freeze upon hearing the maternal alarm call, which the hen issues when there are disturbances (e.g., potential predators) near the nest. Our previous work indicates that ducklings that have been devocalized embryonically and reared in auditory isolation exhibit a significant reduction in the incidence of freezing, as compared to vocal ducklings or to devocal ducklings that have been exposed to duckling sounds throughout the perinatal period up to the time of testing at 12 hr posthatch. The main purpose of this paper is to assess whether there is a prenatal or postnatal sensitive period for such auditory experience. Two groups of 30 devocalized ducklings were either (a) stimulated with duckling sounds prenatally and tested to the alarm call at 12 hr posthatch (Expt. 1), or (b) stimulated from the time of hatching to the time of testing at 12 hr (Expt. 2). These experiments rendered no conclusive evidence of either a prenatal or postnatal sensitive period, but they suggested that auditory experience might be important in maintaining freezing. To test this hypothesis, a third group of 30 ducklings was stimulated from hatching to 12 hr and tested at 24 hr (Expt. 3). Only those ducklings receiving auditory experience contiguous with the time of testing (Expt. 2) showed high levels of freezing. Whenever a gap occurred between the offset of stimulation and the onset of testing (Expts. 1 and 3), the incidence of freezing dropped. Thus, auditory experience is important in maintaining the freezing response. This effect contrasts markedly with traditional conceptions of sensitive periods.     

Prenatally elevated physiological arousal interferes with perceptual learning in bobwhite quail (Colinus virginianus) embryos

Neonatal studies suggest elevated arousal can negatively influence perceptual and cognitive processes during early development. The authors explored this issue during the prenatal period by pharmacologically elevating physiological arousal in bobwhite quail (Colinus virginianus) embryos during exposure to a maternal call, then assessing preference for the familiar call following hatching. Embryos receiving norepinephrine showed a prenatal elevation in heart rate and failed to demonstrate a preference for the familiar call following hatching. Embryos not receiving norepinephrine showed no elevation in heart rate and demonstrated a preference for the familiar call. These results indicate elevated arousal can interfere with perceptual learning during the prenatal period and provide additional evidence for an optimal window of arousal necessary to foster species-typical perceptual functioning during early development.     

Effects of prenatal cocaine and heroin exposure on neuronal dendrite morphogenesis and spatial recognition memory in mice

Cocaine and heroin are psychoactive substances frequently used by woman abusers of childbearing age. In this study, we used in utero electroporation labeling technique and novelty recognition models to evaluate the effects of prenatal exposure of mice to cocaine or heroin on the morphological development of cortical neurons and postnatal cognitive functions. Our results showed that prenatal cocaine exposure increased dendrite outgrowth, and prenatal heroin exposure decreased dendrite length and branch number in pyramidal neurons in the somatosensory cortex. Furthermore, although no effects of prenatal cocaine or heroin exposure on novel object recognition were observed, offspring prenatally exposed to cocaine exhibited no exploration preference for objects placed in novel locations, and mice prenatally exposed to heroin showed a reduced tendency of exploration for objects in novel locations. These data demonstrate that maternal cocaine or heroin administration during pregnancy causes morphological alterations in pyramidal neurons in the somatosensory cortex and suggest that prenatal administration of addictive substances may impair short-term spatial memory in adult offspring.     

Effects of social experience on visually imprinted maternal preferences in Peking ducklings

If Peking ducklings are given social experience with agemates after their initial exposure to a maternal imprinting model (a stuffed mallard hen) their subsequent maternal preferences in simultaneous choice tests are different from those of isolate-reared ducklings. Early in development (at 48 hr after hatching), they show a visual preference for the mallard over a redhead model, a difficult discrimination that isolated birds do not make (Experiment I). However, later in development (at 72 hr after hatching) the social experience interferes with the birds' maternal preferences, in that socially reared birds do not show a visual preference for the mallard over a pintail model, a preference that isolated birds do show at that age (Experiment II). It was found that it is the later social experience with agemates (between 48 and 72 hr) that actively interferes with the preference for the mallard model, because birds that have had only early social experience with agemates (between 24 and 48 hr) prefer the familiar mallard to the pintail model at both 48 and 72 hr (Experiment III). The conventional view of visual imprinting is that it serves to establish a maternal bond that does not require further experience with the mother to be maintained. Our results suggest that in the natural situation, where potentially interfering social stimulation is provided by siblings, continual exposure to the mother may be necessary to maintain the maternal bond even after it has been established.     

Temporal frequency characteristics of synchrony–asynchrony discrimination of audio-visual signals

Temporal synchrony is a critical condition for integrating information presented in different sensory modalities. To gain insight into the mechanism underlying synchrony perception of audio-visual signals we examined temporal limits for human participants to detect synchronous audio-visual stimuli. Specifically, we measured the percentage correctness of synchrony-asynchrony discrimination as a function of audio-visual lag while changing the temporal frequency and/or modulation waveforms. Audio-visual stimuli were a luminance-modulated Gaussian blob and amplitude-modulated white noise. The results indicated that synchrony-asynchrony discrimination became nearly impossible for periodic pulse trains at temporal frequencies higher than 4 Hz, even when the lag was large enough for discrimination with single pulses (Experiment 1). This temporal limitation cannot be ascribed to peripheral low-pass filters in either vision or audition (Experiment 2), which suggests that the temporal limit reflects a property of a more central mechanism located at or before cross-modal signal comparison. We also found that the functional behaviour of this central mechanism could not be approximated by a linear low-pass filter (Experiment 3). These results are consistent with a hypothesis that the perception of audio-visual synchrony is based on comparison of salient temporal features individuated from within-modal signal streams.     

Intersensory functioning in bobwhite quail chicks: early sensory dominance

Two sensory systems known to be important for the control of early filial behavior in precocial avian neonates are the auditory and visual modalities. This study examined the interaction between naturally occurring auditory and visual stimulation in the control of filial behavior in bobwhite quail (Colinus virginianus) during the first four days of postnatal development. Results revealed a hierarchy in the functional priority of the auditory and visual systems in the days immediately following hatchling. At one and two days of age, species identification in quail hatchlings was found to depend on the auditory component of maternal stimulation. Later in development (at three and four days of age), combined auditory-visual stimulation was necessary to control species-specific filial behavior. Even at these later stages of development, however, the auditory modality remained dominant over the visual in eliciting responsiveness to the maternal hen. These findings conform well to what is known about the neuroembryological development of the sensory systems, in that the auditory system of birds (and mammals) develops in advance of the visual system. This prenatal sequence of sensory system development appears to influence the nature of early postnatal perceptual preferences and serves to question several traditional assumptions regarding the imprinting process.