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 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.     

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 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.     

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.     

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.     

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.     

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.     

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.     

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. © 2006 Wiley Periodicals, Inc. Dev Psyshobiol 48: 315–324, 2006.     

Expression of calcium-binding proteins in the chick auditory nuclei following prenatal auditory stimulation

Aim: Auditory stimulation during development influences the morphological and neurochemical substrate of chick brainstem auditory nuclei, nucleus magnocellularis (NM) and nucleus laminaris (NL). Calcium-binding proteins (CaBPs) - calretinin (CR), calbindin (CALB), and parvalbumin (PV) - are known to buffer cytosolic calcium transients that occur with activation of neurons. In the present study, we examined the expression of three CaBPs - CR, CALB, and PV - in the NM and NL at embryonic days E12, E16, E20, and posthatch dayl (PH1), following prenatal sound enrichment protocol. Materials and methods: The incubating eggs were exposed to species-specific sound or music (sitar) at 65 dB for 15 min/h over a day/night cycle from E10 to E14 (low frequency) and E15 till hatching (high frequency). Results: Calretinin and parvalbumin were present in the developing normal and stimulated auditory nuclei, while CALB was absent. Calretinin-immunoreactivity (CR-IR) was present from E12 onward in NM and NL neurons of all the groups. The auditory stimulated groups showed no change in the expression of CR-IR in NM and NL. During normal development, PV was restricted to the cochlear nerve fibers at E16, and appeared in their terminals on the NM somata at PH1. In both stimulated groups, however, PV appeared earlier at E12 in the cochlear fibers and was prominently visualized from E16 in the NM and E20 in the NL neurons. Conclusions: Thus, CR and PV but not CALB are present in chick brainstem auditory nuclei for mediating calcium signaling and homeostasis. Prenatal sound caused an early activity-dependent maturation of PV but not CR which is a constitutive protein.     

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.     

Visual stimulation enhances auditory processing in 3‐month‐old infants and adults

Behavioral work demonstrates human infants are sensitive to a host of intersensory properties and this sensitivity promotes early learning and memory. However, little is known regarding the neural basis of this ability in infants. Using event‐related potentials (ERPs) with infants and adults, we show that during passive viewing auditory evoked brain responses are increased with the presence of simultaneous visual stimulation. Results converge with previous adult neuroimaging studies, single‐cell recordings in nonhuman animals, and behavioral studies with human infants to provide evidence for an elevated status of multisensory stimulation in infancy. Furthermore, these results may provide a neural marker of multisensory audio‐visual processing in infants that can be used to test developmental theories of how information is integrated across the senses to form a unitary perception of the world. © 2009 Wiley Periodicals, Inc. Dev Psychobiol 52:181–189, 2010     

Effects of auditory stimulation on heart rate in premature infants as a function of level of arousal, probability of CNS damage, and conceptional age

In 2 experiments, heart rate responses of newborn infants to an auditory stimulus as a function of sleep vs wakefulness, probability of perinatal impairment of the central nervous system, and developmental level were compared. All subjects were studied under standard conditions, in their own incubators, using an 80 dB (re 0.02 dynes/cm²) low-frequency buzzer of 3-sec duration. Heart rate responses were averaged over 10 trials for each subject in each state. In the first study, which compared the responses of high- and low-risk subjects of 1800 gm or greater weight, it was found that there was no difference between the groups in the response during sleep; or greater weight, it was found that there was no difference between the groups in the response during sleep; during wakefulness, however, a significant difference in the direction of response was found. High-risk subjects accelerated, as in sleep, whereas low-risk subjects decelerated. In a developmental study of 4 small premature infants, it was found that the direction of the waking heart rate response changed from acceleration to deceleration at about 35 to 36 weeks conceptional age.     

Prenatal stimulation and postnatal testosterone affects infanticide in female rats

Prenatal handling, prenatal stress, and early postnatal exogeneous testosterone were examined in female rats for their effects on rat pup-killing and pup retrieval. During each of the last 5 days of pregnancy, Long-Evans rats received either 3 minutes of handling, 45 minutes of restraint and intense illumination or remained untouched. Half of the offspring of each group received testosterone from Day 1 after birth to Day 30. In adulthood, animals that received handling prenatally and testosterone postnatally killed pups more rapidly than any other group and a larger proportion did so than in the control groups. Animals not manipulated at any time retrieved pups more rapidly and a larger proportion did so than the combined other groups. The study suggests that prenatal handling interacts with testosterone presented immediately postnatally to increase infanticide in female rats. A variety of perinatal manipulations seem to suppress pup retrieval.     

Cross-species investigations of prenatal experience, hatching behavior, and postnatal behavioral laterality

Turning biases have been reported in some mammalian species, but less is known about such biases in nonmammalians. This study investigated turning biases in domestic chicks, bobwhite and Japanese quail, leopard geckos, and snapping turtles. Domestic chicks (white leghorn and bantam) and bobwhite quail demonstrate strong group laterality. Japanese quail chicks, snapping turtles, and leopard geckos demonstrate no significant group bias. Results are discussed with regard to differences in embryonic experience, hatching behavior, and postnatal environment.