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.     

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.     

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.     

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     

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.     

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 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.     

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.     

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.     

Audio-visual multisensory integration in superior parietal lobule revealed by human intracranial recordings

Intracranial recordings from three human subjects provide the first direct electrophysiological evidence for audio-visual multisensory processing in the human superior parietal lobule (SPL). Auditory and visual sensory inputs project to the same highly localized region of the parietal cortex with auditory inputs arriving considerably earlier (30 ms) than visual inputs (75 ms). Multisensory integration processes in this region were assessed by comparing the response to simultaneous audio-visual stimulation with the algebraic sum of responses to the constituent auditory and visual unisensory stimulus conditions. Significant integration effects were seen with almost identical morphology across the three subjects, beginning between 120 and 160 ms. These results are discussed in the context of the role of SPL in supramodal spatial attention and sensory-motor transformations.     

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.     

Neural mechanisms for synthesizing sensory information and producing adaptive behaviors

The ability to integrate information from different sensory systems is a fundamental characteristic of the brain. Because different bits of information are derived from different sensory channels, their synthesis markedly enhances the detection and identification of external stimuli. The neural substrate for such “multisensory” integration is provided by neurons that receive convergent input from two or more sensory modalities. Many such multisensory neurons are found in the superior colliculus (SC), a midbrain structure that plays a significant role in overt attentive and orientation behaviors. The various principles governing the integration of visual, auditory, and somatosensory inputs in SC neurons have been explored in several species. Thus far, the evidence suggests a remarkable conservation of integrative features during vertebrate evolution. One of the most robust of these principles is based on spatial relationships: a striking enhancement in activity is induced in a multisensory neuron when two different sensory stimuli (e.g., visual and auditory) are in spatial concordance, whereas a profound response depression can be induced when these cues are spatially discordant. The most extensive physiological observations have been made in cat, and in this species the same principles that have been shown to govern multisensory integration at the level of the individual SC neuron have also been shown to govern overt attentive and orientation responses to multisensory stimuli. Most surprising, however, is the critical role played by association (i.e. anterior ectosylvian) cortex in facilitating these midbrain processes. In the absence of the modulating corticotectal influences, multisensory SC neurons in cat are unable to integrate the different sensory cues converging upon them in an adult-like fashion, and are unable to mediate overt multisensory behaviors. This situation appears quite similar to that observed during early postnatal life. When multisensory SC neurons first appear, they are able to respond to multiple sensory inputs but are unable to synthesize these inputs to significantly enhance or degrade their responses. During ontogeny, individual multisensory neurons develop this capacity abruptly, but at very different ages, until the mature population condition is reached after several postnatal months. It appears likely that the abrupt onset of this capacity in any individual SC neuron reflects the maturation of inputs from anterior ectosylvian cortex. Presumably, the functional coupling of cortex with an individual SC neuron is essential to initiate and maintain that neuron’s capability for multisensory integration throughout its life.     

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.     

Spatial attention triggered by unimodal, crossmodal, and bimodal exogenous cues: a comparison of reflexive orienting mechanisms

The aim of this study was to establish whether spatial attention triggered by bimodal exogenous cues acts differently as compared to unimodal and crossmodal exogenous cues due to crossmodal integration. In order to investigate this issue, we examined cuing effects in discrimination tasks and compared these effects in a condition wherein a visual target was preceded by both visual and auditory exogenous cues delivered simultaneously at the same side (bimodal cue), with conditions wherein the visual target was preceded by either a visual (unimodal cue) or an auditory cue (crossmodal cue). The results of two experiments revealed that cuing effects on RTs in these three conditions with an SOA of 200 ms had comparable magnitudes. Differences at a longer SOA of 600 ms (inhibition of return for bimodal cues, Experiment 1) disappeared when catch trials were included (in Experiment 2). The current data do not support an additional influence of crossmodal integration on exogenous orienting, but are well in agreement with the existence of a supramodal spatial attention module that allocates attentional resources towards stimulated locations for different sensory modalities.     

Crossmodal Facilitation of Masked Visual Target Discrimination by Informative Auditory Cuing

Temporally synchronous, auditory cues can facilitate participants’ performance on dynamic visual search tasks. Making auditory cues spatially informative with regard to the target location can reduce search latencies still further. In the present study, we investigated how multisensory integration, and temporal and spatial attention, might conjointly influence participants’ performance on an elevation discrimination task for a masked visual target presented in a rapidly-changing sequence of masked visual distractors. Participants were presented with either spatially uninformative (centrally presented), spatially valid (with the target side), or spatially invalid tones that were synchronous with the presentation of the visual target. Participants responded significantly more accurately following the presentation of the spatially valid as compared to the uninformative or invalid auditory cues. Participants endogenously shifted their attention to the likely location of the target indicated by the valid spatial auditory cue (reflecting top-down, cognitive processing mechanisms), which facilitated their processing of the visual target over and above any bottom-up benefits associated solely with the synchronous presentation of the auditory and visual stimuli. The results of the present study therefore suggest that crossmodal attention (both spatial and temporal) and multisensory integration can work in parallel to facilitate people's ability to most efficiently respond to multisensory information.     

Anatomical traces of juvenile learning in the auditory system of adult barn owls

Early experience plays a powerful role in shaping adult neural circuitry and behavior. In barn owls, early experience markedly influences sound localization. Juvenile owls that learn new, abnormal associations between auditory cues and locations in visual space as a result of abnormal visual experience can readapt to the same abnormal experience in adulthood, when plasticity is otherwise limited. Here we show that abnormal anatomical projections acquired during early abnormal sensory experience persist long after normal experience has been restored. These persistent projections are perfectly situated to provide a physical framework for subsequent readaptation in adulthood to the abnormal sensory conditions experienced in early life. Our results show that anatomical changes that support strong learned neural connections early in life can persist even after they are no longer functionally expressed. This maintenance of silenced neural circuitry that was once adaptive may represent an important mechanism by which the brain preserves a record of early experience.     

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.     

Prenatal visual experience influences the development of turning bias in bobwhite quail chicks (Colinus virginianus)

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. © 1998 John Wiley & Sons, Inc. Dev Psychobiol 32: 327–338, 1998