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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.

Avian eggs contain maternally derived hormones, including testosterone and progesterone. Little is currently known about the effects of these hormones on early behavioral development. We assessed the effects of elevated levels of progesterone levels on prenatal perceptual learning and postnatal emotional reactivity in Northern bobwhite quail. Prior to incubation, eggs received an injection of either progesterone (P) or oil vehicle (V). In P eggs, levels of progesterone were elevated two standard deviations above the mean based on ELISA analysis of progesterone yolk concentrations from a previous study. A third group of eggs served as controls and received no injection (C). Chicks hatched from P eggs displayed elevated levels of emotional reactivity compared to V and C chicks in a tonic immobility task and a hole-in-the-wall emergence task. Chicks from P eggs also failed to demonstrate a preference for a familiarized bobwhite maternal call that had been presented prenatally. In contrast, the V and C chicks demonstrated a significant preference for the familiarized maternal call following hatching, indicating prenatal auditory learning. Our results are consistent with previous findings from precocial birds demonstrating that hormones of maternal origin can influence prenatal perceptual learning as well as emotional reactivity in the period following hatching. © 2015 Wiley Periodicals, Inc. Dev Psychobiol 57: 255–262, 2015.

Previous studies have established that yolk hormones of maternal origin can influence physiology and behavior in birds. However, few studies have examined the effects of maternal gestagens, like progesterone, on chick behavior and physiology. We tested the effects of experimentally elevated egg yolk progesterone on embryonic heart rate and postnatal auditory learning in bobwhite quail hatchlings. Quail chicks were passively exposed to an individual maternal assembly call for 10 min/hr during the 24 hr following hatching. Preference for the familiarized call was tested at 48 hr following hatching in three experimental groups: chicks that received artificially elevated yolk progesterone (P) prior to incubation, vehicle-only controls (V), and non-manipulated controls (C). Resting heart rate of P, V, and C embryos were also measured on prenatal day 17. The resting heart rate of P embryos was significantly higher than both the V and C embryos. Chicks from the P group also showed an enhanced preference for the familiarized bobwhite maternal call when compared to chicks from the C and V groups. Our results indicate that elevated yolk progesterone in pre-incubated bobwhite quail eggs can influence arousal level in bobwhite embryos and postnatal perceptual learning in bobwhite neonates.

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.

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. 2008 Wiley Periodicals, Inc. Dev Psychobiol 50: 460-472, 2008.

Rearing with enriched environmental complexity has been shown to enhance spatial exploration and spatial learning, among other benefits. Most studies examining enriched rearing effects have used extended periods of exposure in mammals; little is known about enrichment effects on avian species. We provided objects designed to encourage spatial exploration to socially raised northern bobwhite neonates; controls were socially raised without the enrichment devices. After 3-5 days of exposure, maze performance was assessed for 48 chicks. Chicks in the enriched group showed significantly more spatial activity in the maze than control chicks. These results extend the generality of spatial enrichment effects to birds and to a relatively short duration of enrichment exposure. 2007 Wiley Periodicals, Inc. Dev Psychobiol 49: 548-551, 2007.

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 naive embryos. In a subsequent experiment, naive 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. © 2006 Wiley Periodicals, Inc. Dev Psyshobiol 48: 315–324, 2006.

The effects of asymmetrical hatching behaviors on the development of turning bias and footedness in domestic chicks, bobwhite quail, and Japanese quail chicks were examined. Control tests with incubator reared domestic chicks and bobwhite quail revealed significant individual and population left-side turning bias and right footedness. When late stage hatching behaviors were disrupted, population laterality was not evident and individual laterality was reduced. By contrast, Japanese quail chicks demonstrated no population turning bias or footedness and only weak individual biases. Disruption of hatch behaviors further decreased laterality. Examination of discarded eggshells showed significant differences in the degree of rotation made to cut out of the egg by Japanese quail versus domestic chicks and bobwhite quail. Taken together these findings suggest that the counterclockwise hatching behaviors that are characteristic of many precocial bird species serve to facilitate the development of motor laterality at both the individual and population level.

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.

Avian eggs contain maternally derived hormones, including testosterone and progesterone. Little is currently known about the effects of these hormones on early behavioral development. We assessed the effects of elevated levels of progesterone levels on prenatal perceptual learning and postnatal emotional reactivity in Northern bobwhite quail. Prior to incubation, eggs received an injection of either progesterone (P) or oil vehicle (V). In P eggs, levels of progesterone were elevated two standard deviations above the mean based on ELISA analysis of progesterone yolk concentrations from a previous study. A third group of eggs served as controls and received no injection (C). Chicks hatched from P eggs displayed elevated levels of emotional reactivity compared to V and C chicks in a tonic immobility task and a hole-in-the-wall emergence task. Chicks from P eggs also failed to demonstrate a preference for a familiarized bobwhite maternal call that had been presented prenatally. In contrast, the V and C chicks demonstrated a significant preference for the familiarized maternal call following hatching, indicating prenatal auditory learning. Our results are consistent with previous findings from precocial birds demonstrating that hormones of maternal origin can influence prenatal perceptual learning as well as emotional reactivity in the period following hatching..

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.

This study examined the effects of prenatal sensory experience on the development of turning bias in a precocial avian species (bobwhite quail). Control tests with naive bobwhite quail chicks revealed a left-side turning bias in 85% of subjects. Such large population biases are considered unusual in nonhuman species. Experiments 1, 2, and 3 demonstrated that prenatal visual experience is a significant contributor to this population level left-side turning bias in bobwhite quail chicks. In contrast, prenatal auditory experience did not appear to significantly influence the development of postnatal turning bias. The findings of this study are discussed in terms of an epigenetic theory for the development of hemispheric specialization and behavioral asymmetry.

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.

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.

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. 2006 Wiley Periodicals, Inc. Dev Psychobiol 48: 233-242, 2006.

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 redun- dant 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 stimula- tion, 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. 2003 Wiley Periodicals, Inc. Dev Psychobiol 43: 304-310, 2003.

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. © 2003 Wiley Periodicals, Inc. Dev Psychobiol 43: 71–81, 2003.

This study examined the effects of prenatal sensory experience on the development of turning bias in a precocial avian species (bobwhite quail). Control tests with naive bobwhite quail chicks revealed a left-side turning bias in 85% of subjects. Such large population biases are considered unusual in nonhuman species. Experiments 1, 2, and 3 demonstrated that prenatal visual experience is a significant contributor to this population level left-side turning bias in bobwhite quail chicks. In contrast, prenatal auditory experience did not appear to significantly influence the development of postnatal turning bias. The findings of this study are discussed in terms of an epigenetic theory for the development of hemispheric specialization and behavioral asymmetry.

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 intersensory and intersensory interference.

In contrast to the large body of work on young infants' capacity to perceive temporally 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.

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. © 1992 Wiley & sons. Inc.

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.

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.

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.

The development of dustbathing components was investigated in Bobwhite and Japanese quail. The incidence and frequencies of components for both species increased with age, but dustbathing occurred earlier in Japanese quail. The dust toss, head rub, and side rub components invariably developed in the same order they occur during an adult bout. The topographies of many components changed systematically with a "rudimentary" form preceding the typical adult form. Large individual differences were observed in the development of the temporal relations among components, but these differences were unrelated to the relative frequencies of components.

The development of dustbathing was facilitated among groups of Bobwhite chicks allowed to peck into dust as compared to chicks allowed to peck at dust or those inexperienced with dust. A 2nd study found a consistent, but nonsignificant, facilitation among chicks pecking into dust on Days 1–3 as compared to Days 4–6. In Study 3, groups of chicks pecked into dust on Days 2, 4, or 6. Dustbathing development was facilitated among chicks pecking on Day 2, and inhibited among chicks pecking on Day 4, as compared to those pecking on Day 6. The only difference, however, between each of these groups and chicks with no pecking experience in dust (Study 1) was an inhibition of dustbathing among chicks pecking on Day 4.