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.     

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.     

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     

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.     

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.     

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.     

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.     

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.     

Species-specific auditory discrimination in bobtail quail neonates

Incubator-hatched bobwhite quail neonates were tested individually in a variety of single call and simultaneous auditory choice tests involving 6 adult quail vocalizations and a chicken exodus call. The quail showed a high degree of responsiveness (100%) to 3 adult quail vocalizations and significantly less responsiveness (40-50%) to 3 other quail calls and to the chicken exodus call in single call tests. In simultaneous choice tests, the quail were selectively responsive to a call of their own species over the chicken call, and they also showed certain intraspecific preferences. Because of their high degree of responsiveness, coupled with selectivity of their approach responses, bobwhite quail neonates are ideal for the laboratory investigation of the development of auditory perception.     

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.     

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.     

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.     

Development of species identification in ducklings. XIII: A comparison of malleable and critical periods of perceptual development

The present experiments sought to determine the relationship of the malleable period--when the mallard duck embryo is most susceptible to alien forms of maternal auditory stimulation--to the critical period, when the embryo must hear its own vocalizations in order to respond normally to the species-typical maternal call after hatching. It was found that a preference for either a wood duck or a chicken maternal call could be induced in devocalized mallard duck embryos by exposing them to either alien call some time between day 24, 0600 to day 26, 0600 hrs. Further experiments showed the height of the malleable period to be between day 24, 1400 hrs and day 25, 0800 hrs of embryonic development. Since the embryonic critical period for maintenance of the species-typical maternal auditory preference spans day 24, 0800 hrs to day 26, 0800 hrs, the malleable period for the induction of a preference for species-atypical maternal stimulation falls inside the critical period. While it is often assumed that malleable and critical periods overlap, this is the first behavioral study to actually demonstrate the temporal relationship of the two periods. It would seem important to further examine malleable and critical periods of development in a broader array of developmental contexts and species to determine whether malleable periods for atypical or abnormal development and critical periods for species-typical or normal development always coincide.     

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.     

Prenatal acoustic stimulation influences neuronal size and the expression of calcium-binding proteins (calbindin D-28K and parvalbumin) in chick hippocampus

Prenatal auditory enrichment by species-specific sounds and sitar music enhances the expression of immediate early genes, synaptic proteins and calcium binding proteins (CaBPs) as well as modifies the structural components of the brainstem auditory nuclei and auditory imprinting area in chicks. There is also facilitation of postnatal auditory preference of the chicks to maternal calls following both types of sound stimulation indicating prenatal perceptual learning. To examine whether the sound enrichment protocol also affects the areas related to learning and memory, we assessed morphological changes in the hippocampus at post-hatch day 1 of control and prenatally sound-stimulated chicks. Additionally, the proportions of neurons containing calbindin D-28K and parvalbumin immunoreactivity as well as their protein levels were determined. Fertilized eggs of domestic chick were incubated under normal conditions of temperature, humidity, forced draft of air as well as light and dark (12:12 h) photoperiods. They were exposed to patterned sounds of species-specific and sitar music at 65 dB for 15 min per hour over a day/night cycle from day 10 of incubation till hatching. The hippocampal volume, neuronal nuclear size and total number of neurons showed a significant increase in the music-stimulated group as compared to the species-specific sound-stimulated and control groups. However, in both the auditory-stimulated groups the protein levels of calbindin and parvalbumin as well as the percentage of the immunopositive neurons were increased. The enhanced proportion of CaBPs in the sound-enriched groups suggests greater Ca²⁺ influx, which may influence long-term potentiation and short-term memory.     

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.     

The dynamics of development and evolution: insights from behavioral embryology

The perspective that features of species-typical behavior could be traced to experience that occurred prenatally was raised by Zing-Yang Kuo [1921 Journal of Philosophy 18: 645-664] early in the last century and Gilbert Gottlieb subsequently elaborated on and provided empirical support for this idea over the course of more than four decades of innovative psychobiological research. Although we are still a long way from fully understanding the specific pathways and processes by which prenatal experience can influence postnatal development, Gottlieb's research with precocial birds provided significant insights into the conditions and experiences of prenatal development involved in the achievement of species-typical perception and behavior. In particular, his elegant series of studies on the development of species identification in ducklings documented how the features and patterns of recurring prenatal sensory experience (including self-stimulation) guide and constrain the young individual's selective attention, perception, learning, and memory during both prenatal and postnatal periods. I review how this body of research supports the view that the structure and functions of the developing organism and its developmental ecology together form a relationship of mutual influence on the emergence, maintenance, and transformation of species-typical behavior. I also explore how Gottlieb's empirical demonstrations of the prenatal roots of so-called "instinctive" behavior provided a foundation for his conceptual efforts to define the links between developmental and evolutionary change.     

Development of species identification in ducklings: X. Perceptual specificity in the wood duck embryo requires sib stimulation for maintenance

A critical acoustic feature of the wood duck maternal assembly call is the descending frequency modulation (FM) of its notes. To determine the role of exposure of wood ducklings to conspecific vocalizations in the development of selective responsiveness to the descending FM of the species maternal call, the behavioral response of embryos to synthetic descending and ascending maternal calls was examined. Previous work indicated that selective responsivenness of newly hatched wood ducklings to the descending FM of the maternal call is dependent upon prior exposure to descending FM calls of siblinngs. In advance of auditory experience the youngest embryos were responsive to both ascending and descending call notes, but older aurally isolated embryos became selectively responsive to the descending FM. However, even though the wood duck hatchling vocalizes considerably in aural isolation, self-stimulation is ineffective in maintaining the perceptual selectivity in the neonate. Unlike the mallard, in which self-stimulation is adequate, the wood duckling must be exposed to sib vocalizations in order to remain selectively responsive to the critical acoustic feature of the maternal call of its species.