Bobwhite Quail Embryos Research Articles

The intersensory redundancy hypothesis: Extending the principle of unimodal facilitation to prenatal development.

Selective attention to different properties of stimulation provides the foundation for perception, learning, and memory. The Intersensory Redundancy Hypothesis (IRH) proposes that early in development information presented redundantly across two or more modalities (multimodal) selectively recruits attention to and enhances perceptual learning of amodal properties, whereas information presented to a single sense modality (unimodal) enhances perceptual learning of modality-specific properties. The present study is the first to assess this principle of unimodal facilitation in non-human animals in prenatal development. We assessed bobwhite quail embryos' prenatal detection of pitch, a modality-specific property, under conditions of unimodal and bimodal (synchronous or asynchronous) exposure. Chicks exposed to prenatal unimodal auditory stimulation or asynchronous bimodal (audiovisual) stimulation preferred the familiarized maternal call over a novel pitch-modified maternal call following hatching, whereas chicks exposed to redundant (synchronous) audiovisual stimulation failed to prefer the familiar call over the pitch-modified call. These results provide further evidence that selective attention is recruited to specific stimulus properties of events in early development and that these biases are evident even during the prenatal period.

Simple Culture System for Bobwhite Quail and Japanese Quail Embryos from the Blastoderm Stage to Hatching using a Single Surrogate Eggshell

The ex vivo culture of avian embryos is a technique for the long-term culturing of embryos outside of their own shell and shell membrane. It allows easy access to the developing embryos and embryo manipulation. The two-step system is widely applied when the culture is performed after oviposition. Japanese quail as well as bobwhite quail are used as models for avian safety assessment as recommended by the Organisation for Economic Co-operation and Development (OECD) guidelines. However, biological studies on the bobwhite quail have been more limited than those on the Japanese quail. We have developed a more simplified ex vivo culture protocol for the two species of quail embryos from the blastoderm stage through to hatching using a single surrogate eggshell. Hatchabilities of 31% and 27% were obtained in bobwhite quail and Japanese quail embryos, respectively. The simple system described in the present study is an easy and acceptable procedure.

Culture System for Bobwhite Quail Embryos from the Blastoderm Stage to Hatching

Quail are divided phylogenetically into two groups, Old World quail and New World quail. Old World quail, such as the Japanese quail (Coturnix japonica), belong to the Phasianidae and distributed in the Palaearctic region (Europe, North Africa, and Asia), whereas New World quail, such as the bobwhite quail (Colinus virginianus), belong to the Odontophoridae and are restricted to North and South America. Both the bobwhite quail and the Japanese quail are used as models for avian safety assessment as recommended by the Organisation for Economic Co-operation and Development (OECD) guidelines. However, biological studies on the bobwhite quail have been limited compared with those on the Japanese quail. We have therefore now developed an ex vivo culture protocol for bobwhite quail embryos from the blastoderm stage through hatching. Of the various culture conditions examined in the present study, a good hatching rate (39%) was obtained when the embryos were cultured ex vivo in a two-step procedure. Unincubated embryos (with egg yolk) were first cultured inside the shell of a Japanese quail egg (11.5 to 13.0 g whole egg weight) together with chicken thin albumen for 63 to 65 h and were then transferred to the shell of a small-sized chicken egg (38 g whole egg weight) until hatching. This ex vivo culture system should provide to be widely applicable to the maintenance and generation of manipulated birds for basic and applied studies on the bobwhite quail.

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.

Intersensory redundancy educates selective attention in bobwhite quail embryos.

We assessed whether exposure to amodal properties in bimodal stimulation (e.g. rhythm, rate, duration) could educate attention to amodal properties in subsequent unimodal stimulation during prenatal development. Bobwhite quail embryos were exposed to an individual bobwhite maternal call under several experimental and control conditions during the day prior to hatching. Experimental groups received redundant auditory and visual exposure to the temporal features of an individual maternal call followed by unimodal auditory exposure to the same call immediately or after a 2-hr or 4-hr delay. Control groups received (1) the same exposure but in the reverse sequence (unimodal --> redundant bimodal), (2) asynchronous bimodal --> unimodal, (3) only unimodal exposure, or (4) only bimodal exposure. All experimental groups showed a significant preference for the familiar maternal call over a novel maternal call when tested 2 days after hatching, whereas none of the control groups showed a significant preference for the familiar call. These results indicate that intersensory redundancy can direct attention to amodal properties in bimodal stimulation and educate attention to the same amodal properties in subsequent unimodal stimulation where no intersensory redundancy is available.

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.

Effects of prenatal visual stimulation on growth and heart rate in bobwhite quail (Colinus virginianus)

This study examined the effects of prenatal visual stimulation on bobwhite quail embryos' growth and heart rate. No differences in growth rate were found between embryos exposed to visual stimulation during the late prenatal period and control embryos. Embryos exposed to visual stimulation throughout incubation maintained lower heart rates in response to visual stimulation than did naïve embryos. In a subsequent experiment, naïve embryos that underwent an egg-opening procedure exhibited heart rates that were lower than embryos measured in intact eggshells. Embryos in opened eggs maintained lower heart rates than comparison embryos across time; however, a less invasive egg-opening procedure led to a quicker heart rate recovery than did a more invasive egg-opening procedure. These findings indicate that prenatal heart rate responses may be mediated by multiple features of the organism's developmental context, including intensity and duration of sensory stimulation.

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 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.

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.

Embryonic Malpositions in Broiler Chickens and Bobwhite Quail

One of the factors contributing to failure of avian embryos to hatch is the positioning of the embryo at the end of incubation in such a manner that emergence from the egg is inhibited. Abnormal positions, or malpositions, may also be associated with other problems without directly affecting the ability of the chick to hatch. The effect of strain, breeder age, and gender of embryo on incidence of malpositions before hatching was determined in broiler embryos. The effect of strain, breeder age, pre-incubation egg storage, setting orientation, and turning during incubation on incidence of malpositions before hatching was determined in bobwhite quail embryos. Although there were variations among strains and between genders for incidence of malpositions, they were not statistically significant. Differences among settings and evaluators were as great as strain effects. No significant strain or breeder age effect on malposition incidence was found in quail. Long-term pre-incubation storage increased the incidence of quail embryos with head between the thighs, possibly related to delayed embryonic development. Setting quail eggs with the small end up resulted in 75% of the embryos with head in the small end of the egg. Eggs set normally but not turned had increased incidences of head in small end, beak away from air cell, and head over wing embryonic malpositions. Therefore, in these studies, the incidence of malpositions was affected by pre-incubation egg storage, egg orientation, and turning, whereas it was not affected by strain, embryo gender, and breeder age.

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.

Prenatal experience and postnatal perceptual preferences: evidence for attentional-bias in bobwhite quail embryos (Colinus virginianus).

Previous studies have indicated that concurrent multimodal sensory stimulation can interfere with prenatal perceptual learning. This study further examined this issue by exposing 3 groups of bobwhite quail embryos (Colinus virginianus) to (a) no supplemental stimulation, (b) a bobwhite maternal call, or (c) a maternal call paired with a pulsating light in the period prior to hatching. Experiments differed in terms of the types of stimuli presented during postnatal preference tests. Embryos receiving no supplemental stimulation showed no preference between stimulus events in all testing conditions. Embryos receiving exposure to the unimodal maternal call preferred the familiar call over an unfamiliar call regardless of the presence or absence of pulsating light during testing. Embryos exposed to the call-light compound preferred the familiar call only when it was paired with the light during testing. These results suggest that concurrent multimodal stimulation does not interfere with prenatal perceptual learning by overwhelming the young organism's limited attentional capacities. Rather, multimodal stimulation biases what information is attended to during exposure and subsequent testing.

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.

Timing of presentation of prenatal auditory stimulation alters auditory and visual responsiveness in bobwhite quail chicks (Colinus virginianus).

One group of bobwhite quail embryos (Colinus virginianus) was exposed to 10 min/hr of bobwhite chick contentment calls immediately followed by 10 min/hr of bobwhite chick distress calls. A 2nd group of embryos was exposed to the same auditory stimulation but in the opposite order of presentation. Postnatal testing revealed that chicks exposed prenatally to the bobwhite chick contentment call and distress call (in either order of presentation) continued to respond to maternal auditory cues into later stages of postnatal development compared with unmanipulated chicks. Chicks exposed prenatally to the contentment call followed by the distress call showed an accelerated pattern of visual responsiveness to maternal cues, whereas chicks exposed prenatally to the distress call followed by the contentment call showed deficits in the normal pattern of perceptual visual responsiveness, suggesting that the auditory stimulation precocial avian embryos encounter 1st is influential in directing early intersensory development.

Type and amount of prenatal stimulation alters perceptual responsiveness in bobwhite quail chicks

To explore the relationship between the type and amount of sensory stimulation provided prenatally and its impact on postnatal responsiveness to maternal cues, bobwhite quail embryos were exposed to 5 or 10 min/hour of either bobwhite chick contentment calls or bobwhite chick distress calls. Results revealed that embryos exposed to 5 or 10 min/hour of distress calls continued to respond to maternal auditory cues into later stages of postnatal development in comparison to controls and failed to demonstrate species-typical responsiveness to maternal visual cues. In contrast, embryos exposed to 5 min/hour of contentment calls continued to respond to maternal auditory cues into later stages of development and exhibited species-typical patterns of visual responsiveness (72 hour of age). Embryos exposed to 10 min/hour of contentment calls responded to maternal auditory cues into later stages of postnatal development but showed an accelerated responsiveness to maternal visual cues (48 hours of age). Taken together, these results suggest that the type and amount of sensory stimulation interact during the prenatal period to influence the course of perceptual development.

Prenatal visual experience alters postnatal sensory dominance hierarchy in bobwhite quail chicks

Work with a variety of precocial animal infants has demonstrated a hierarchy in the functional priority of the auditory and visual systems in the period following birth or hatching with infants initially utilizing auditory rather than visual cues to direct their early perceptual and social preferences. This experiment utilized bobwhite quail embryos and hatchlings to examine whether this pattern of early sensory dominance is influenced by the nature of prenatal sensory experience. Results revealed that bobwhite quail chicks that received unusually early (prenatal) visual experience demonstrate an altered pattern of postnatal sensory dominance but only under specific conditions. Whereas these chicks continued to prefer maternal auditory cues over visual cues when the maternal visual cues provided were motionless, chicks that received prenatal visual experience preferred maternal visual cues over auditory cues by 96 hours of postnatal age when the visual cues provided were kinetic. These results emphasize the importance of considering both extra- and intraorganismic variables when characterizing the nature of early perceptual organization.

Disruption of species-specific behavior in neonatal quail following chronic prenatal ethanol exposure

Bobwhite quail embryos were exposed to ethanol (5 mg every other day) from E5 to E21. Control embryos received comparable saline injections or were untreated. At 24 h posthatch, the neonates were tested in a single call approach test, using a Bobwhite maternal exodus call which had previously been shown to be a potent attractant to these animals. Almost all animals in all three groups approached the call, and latency of approach did not differ among the groups. The ethanol-treated animals, however, spent significantly less time within the approach area and exited the area significantly more often than did either the saline or untreated controls. Overall hyperactivity or loss of auditory acuity did not appear to account for the response deficits. These results suggest that species-specific behaviors might be a useful paradigm for the study of fetal alcohol effects.

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 maternal 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.

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.