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.     

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: XV. Individual auditory recognition

The present experiments examined the ability of domestic mallard ducklings (Anas platyrhynchos) to learn individual mallard maternal calls by either repetition-rate differences or spectral (Hz) differences, both of which are present in such calls recorded in nature. The ducklings could learn both kinds of differences within the first 24 hr after hatching, corresponding to the period prior to the exodus from the nest in nature. The hatchlings were able to learn these differences based upon only 12 min of exposure to the maternal calls during the first day after hatching. They were also able to retain (remember) the familiar call for an additional day after exposure. Embryos, on the other hand, could learn the spectral differences after either 12 or 24 min of exposure but could not retain the information under either exposure condition. An additional difference between the auditory learning competence of hatchlings and embryos was that the hatchlings were capable of learning the spectral features of a maternal call even if it was pulsed at different repetition rates during exposure (familiarization) and the subsequent test for recognition. The evolutionary significance of the results was discussed in terms of the general importance of familiarization as a basic behavioral mechanism underlying not only parental attachment but dietary and habitat preferences and the like.     

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.     

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.     

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.     

Prenatal exposure to temporal and spatial stimulus properties affects postnatal responsiveness to spatial contiguity in bobwhite quail chicks

Little is known about how experiential factors guide and organize the development of intersensory perception. This study manipulated the amount of late prenatal and early postnatal experience with the temporal synchrony and spatial contiguity of audio-visual stimulation available to bobwhite quail embryos and hatchlings to explore this question. Results revealed that only embryos exposed to temporally synchronous and spatially contiguous audio-visual stimulation prior to hatching subsequently preferred spatially contiguous audio-visual maternal information following hatching, despite being denied postnatal visual experience. In contrast, embryos that did not receive exposure to both temporal synchrony and spatial contiguity (and were also denied postnatal visual experience) failed to show a preference for the spatial contiguity of maternal auditory and visual information following hatching. These results suggest that prenatal exposure to the amodal properties of temporal synchrony and spatial contiguity facilitate chicks' emerging sensitivity to the spatial contiguity of audio-visual information in the period following hatching.     

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.     

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.     

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.     

Stimulus contingency and the malleability of species-typical auditory preferences in Northern bobwhite (Colinus virginianus) hatchlings

Precocial avian hatchlings are typically highly social and show strong species-typical preferences for the maternal calls of their own species. The influence of social contingencies on the acquisition of species-specific preferences has, however, largely been neglected. We found that exposing bobwhite (BW) quail chicks to a Japanese quail (JQ) call contingent on their own vocalizations for 5 min was sufficient to eliminate their species-typical preference for the BW maternal call. Yoked, noncontingent exposure had no such effect. The introduction of variability to the contingency, but not a lengthening of the training session, was found to engender even higher preferences for the JQ call. Chicks provided with contingent exposure to the JQ call on a variable ratio schedule showed a significant preference for the JQ over the BW maternal call, whereas chicks provided with equivalent fixed ratio exposure did not. These results highlight the role that social interaction and contingency can play in the acquisition and maintenance of species-specific auditory preferences in precocial avian species.     

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.     

Development of visually controlled maternal preferences in Peking ducklings

The interaction between natural visual and auditory stimulation in the control of filial behavior was studied in domestic mallard (Peking) ducklings during the first 3 days of postnatal life. Visual imprinting at 24 hr resulted in a visual preference for the familiar model over an unfamiliar model in each of two choice tests, one at 48 hr and one at 72 hr, but only if both models were silent. If both models emitted a recording of the mallard maternal call, the visual preference was found only in the later (72-hr) test. Visuomotor experience between training and testing was found to be essential for the development of the visual preference at 72 hr, but the required experience was of a very general nature. Either a choice test with silent models or a period of social rearing (between 24 and 72 hr) provided effective experience. Thus, the ability to show a visual preference in the presence of the maternal call at 72 hr depends on experience, but not necessarily on further exposure to the imprinting object or to any specific aspects of the test situation. These results demonstrate the importance of normal visual, motor and/or social experience to the development of the visual control of filial behavior in ducklings.     

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.     

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.     

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.     

Visually imprinted maternal preference in ducklings is redirected by social interaction with siblings

This study examined the influence of social interaction with broodmates on a visually imprinted maternal preference in domestic mallard ducklings (Anas platyrhynchos) during the first three days of postnatal life. Twenty-four-hour-old ducklings were allowed to follow a stuffed mallard hen for 30 min. This experience resulted in a visually imprinted preference for the familiar stuffed hen over 4 stuffed ducklings in simultaneous choice tests at 48 and 72 hr after hatching, but only if the imprinted birds were kept in social isolation. Imprinted ducklings reared in a social group containing either same-age siblings or the stuffed mallard hen and same-age siblings displayed a visual preference for the stuffed ducklings over the familiar mallard hen at 48 and 72 hr tests. As a first step in the analysis of the features of the social exposure to siblings that are necessary for the redirection of the visually imprinted maternal preference, it was found that direct social interaction is essential to establish the preference for ducklings, but even mere visual exposure to siblings does away with the imprinted maternal preference. These results provide striking evidence of the ready redirection of a species-specific maternal preference in otherwise imprinted ducklings.     

Maternal and peer imprinting in mallard ducklings under experimentally simulated natural social conditions

Previous studies revealed that if socially reared mallard ducklings actively follow a stuffed mallard (Anas platyrhynchos) hen, they later show a visual preference for the familiar mallard hen over an unfamiliar redhead (Aythya americana) hen. The present study determined that the experience of actively following the hen is essential to the induction of a visually controlled, species-typical, maternal preference. Domestic mallard ducklings that had not been given the opportunity to follow the mallard hen were "passively" reared in social groups consisting of a stuffed mallard hen and seven same-aged siblings for either 24, 48, or 72 hr after hatching. These birds were largely unresponsive to the hen in a later choice test, even when they were passively exposed to the mallard hen for as long as 72 hr prior to testing. The question arose as to whether passive exposure to the ducklings induced a preference for them that interfered with establishment of maternal imprinting under these simulated natural nest conditions. Results indicated that socially reared ducklings do prefer stuffed ducklings to a stuffed mallard hen in a simultaneous choice test even when the hen is present and vocalizing during social rearing. Further, even ducklings reared individually with the mallard hen were unresponsive to her in the later choice test. That there is something special about the stimulation provided by ducklings was further demonstrated by the finding that stuffed ducklings were preferred over the mallard hen (1) when the social rearing situation precluded active physical interaction with live ducklings and (2) when reared with inanimate stuffed ducklings. Thus, the ineffectiveness of the stuffed mallard hen in inducing visual imprinting under simulated nesting conditions cannot be attributed to the fact that she was not alive or reciprocally interactive. The present results suggest that mallard ducklings do not become visually imprinted to their hen until after departure from the nest, that the visual component of maternal imprinting likely involves active following subsequent to nest departure, and that early in postnatal development siblings are more visually attractive than is the hen.     

Social specificity: interaction with own species is necessary to foster species-specific maternal preference in ducklings

Previous studies have shown that if domestic mallard ducklings are allowed social interaction with broodmates after their initial exposure to a stuffed mallard (Anas platyrhynchos) hen, they later show a visual preference for the familiar mallard over an unfamiliar redhead (Aythya americana) hen. Birds kept in social isolation do not make this difficult discrimination. In the present study, we examined whether this social enhancement of imprintability to a natural maternal model is merely the result of social stimulation in its most general sense, or if its effects are specific to social interaction for 30 min (training). This experience resulted in visual preference for the familiar mallard hen over the unfamiliar redhead hen in simultaneous choices tests at 48 hr and 72 hr after hatching only if the birds were allowed social experience with a group of same-age undomesticated mallard hatchings. No visual preference for the familiar mallard hen was found if the ducklings were permitted social experience with a group of same-age chick (Gallus domesticus) hatchlings or muscovy (Cairina moschata) ducklings. Thus, it appears that for ducklings to show a visually imprinted preference for a natural maternal model, they must be allowed social interaction with broodmates of their own species. Social rearing with other precocial bird hatchlings, even other ducklings, is without apparent effect. These results provide further evidence of the importance of nonobvious experimental factors in the development of species-typical behavior. They also suggest that in the evolution of the species-specific learning underlying early species identification, natural selection has operated on the entire (organism-environment) developmental manifold and not merely on genetic, organic, or organismic aspects of that system.     

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.