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.     

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     

Premature visual stimulation accelerates intersensory functioning in bobwhite quail neonates

Recent evidence from both altricial and precocial neonates suggests that premature stimulation of a later developing sensory system may alter the functioning of earlier developing sensory systems. The present study examined the influence of prenatal visual stimulation on postnatal auditory functioning in precocial bobwhite quail chicks. Hatchlings that experienced patterned light during the 24-36 hr prior to hatching did not exhibit a naive auditory preference for their species-specific maternal call at 24 hr or 48 hr following hatching, a reliable phenomenon in chicks not receiving embryonic visual stimulation. To examine whether this lack of responsiveness resulted from enhanced intersensory functioning, hatchlings were tested for preference for both auditory and visual features of the bobwhite hen. Results indicate that prematurely stimulated chicks require species-typical auditory and visual stimulation earlier in postnatal development than do normally reared chicks to direct their filial behavior. These findings point to the importance of normally occurring developmental limitation of sensory input to early species-typical sensory/perceptual organization.     

Augmented prenatal visual stimulation alters postnatal auditory and visual responsiveness in bobwhite quail chicks

This study examined whether previously reported effects of altered prenatal sensory experience on subsequent acceleration of intersensory development in precocial birds are mediated by mechanisms sensitive to the overall amount of stimulation provided. Results revealed that bobwhite quail chicks exposed to substantially augmented amounts of prenatal visual stimulation show altered patterns of species-typical perceptual development. Specifically, chicks continued to respond to maternal auditory cues into later stages of postnatal development and failed to demonstrate responsiveness to maternal visual cues. Embryos also failed to demonstrate prenatal auditory learning of an individual maternal call, a behavior reliably seen in unmanipulated embryos. These findings suggest that substantially increased amounts of prenatal sensory stimulation can interfere with the emergence of species-typical patterns of postnatal intersensory functioning and lend support to the notion that sensory stimulation that falls within some optimal range maintains or facilitates normal patterns of perceptual development, whereas stimulation beyond the range of the species norm can result in intersensory interference. © 1995 John Wiley & Sons, Inc.     

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.     

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.     

Intersensory experience and early perceptual development: The role of spatial contiguity in bobwhite quail chicks' responsiveness to multimodal maternal cues

In contrast to the large body of work on young infants' capacity to perceive temporarilly based intersensory relations, little research has been done on the role of spatial contiguity in the development of audio-visual integration. This study examined the effects of early postnatal sensory experience on an avian neonate's responsiveness to the spatial contiguity between maternal auditory and visual cues. Specifically, we assessed whether a bobwhite quail chick's ability to respond to the correspondence between the location of auditory and visual events is affected by its sensory-stimulation history. Results revealed that chicks denied species-typical auditory or visual experience in the period immediately following hatching showed altered patterns of responsiveness to maternal auditory and visual cues. In particular, chicks that received modified postnatal sensory experience demonstrated a higher tolerance for audio-visual spatial discrepancy than did control chicks. These results provide evidence of the important role of sensory experience in the emergence of intersensory integration during the perinatal period and highlight the role of spatial information in early perceptual responsiveness to maternal cues. © 1996 John Wiley & Sons, Inc.     

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.     

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.     

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.     

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.     

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.     

Temporal processing of active and passive head movement

The brain can know about an active head movement even in advance of its execution by means of an efference copy signal. In fact, sensory correlates of active movements appear to be suppressed. Passive disturbances of the head, however, can be detected only by sensory feedback. Might the perceived timing of an active head movement be speeded relative to the perception of a passive movement due to the efferent copy (anticipation hypothesis) or delayed because of sensory suppression (suppression hypothesis)? We compared the perceived timing of active and passive head movement using other sensory events as temporal reference points. Participants made unspeeded temporal order and synchronicity judgments comparing the perceived onset of active and passive head movement with the onset of tactile, auditory and visual stimuli. The comparison stimuli had to be delayed by about 45 ms to appear coincident with passive head movement or by about 80 ms to appear aligned with an active head movement. The slow perceptual reaction to vestibular activation is compatible with our earlier study using galvanic stimulation (Barnett-Cowan and Harris 2009). The unexpected additional delay in processing the timing of an active head movement is compatible with the suppression hypothesis and is discussed in relation to suppression of vestibular signals during self-generated head movement.     

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.     

Neural correlates of multisensory cue integration in macaque MSTd

Human observers combine multiple sensory cues synergistically to achieve greater perceptual sensitivity, but little is known about the underlying neuronal mechanisms. We recorded the activity of neurons in the dorsal medial superior temporal (MSTd) area during a task in which trained monkeys combined visual and vestibular cues near-optimally to discriminate heading. During bimodal stimulation, MSTd neurons combined visual and vestibular inputs linearly with subadditive weights. Neurons with congruent heading preferences for visual and vestibular stimuli showed improvements in sensitivity that parallel behavioral effects. In contrast, neurons with opposite preferences showed diminished sensitivity under cue combination. Responses of congruent cells were more strongly correlated with monkeys' perceptual decisions than were responses of opposite cells, suggesting that the monkey monitored the activity of congruent cells to a greater extent during cue integration. These findings show that perceptual cue integration occurs in nonhuman primates and identify a population of neurons that may form its neural basis.     

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.     

Temporal binding of auditory and rotational stimuli

Integration of cues from multiple sensory channels improves our ability to sense and respond to stimuli. Cues arising from a single event may arrive at the brain asynchronously, requiring them to be ??bound?? in time. The perceptual asynchrony between vestibular and auditory stimuli has been reported to be several times greater than other stimulus pairs. However, these data were collected using electrically evoked vestibular stimuli, which may not provide similar results to those obtained using actual head rotations. Here, we tested whether auditory stimuli and vestibular stimuli consisting of physiologically relevant mechanical rotations are perceived with asynchronies consistent with other sensory systems. We rotated 14 normal subjects about the earth-vertical axis over a raised-cosine trajectory (0.5?Hz, peak velocity 10?deg/s) while isolated from external noise and light. This trajectory minimized any input from extravestibular sources such as proprioception. An 800-Hz, 10-ms auditory tone was presented at stimulus onset asynchronies ranging from 200?ms before to 700?ms after the onset of motion. After each trial, subjects reported whether the stimuli were ??simultaneous?? or ??not simultaneous.?? The experiment was repeated, with subjects reporting whether the tone or rotation came first. After correction for the time the rotational stimulus took to reach vestibular perceptual threshold, asynchronies spanned from ?41?ms (auditory stimulus leading vestibular) to 91?ms (vestibular stimulus leading auditory). These values are significantly lower than those previously reported for stimulus pairs involving electrically evoked vestibular stimuli and are more consistent with timing relationships between pairs of non-vestibular stimuli.     

Challenges to maternal wellbeing during pregnancy impact temperament, attention, and neuromotor responses in the infant rhesus monkey

The relative maturity, alertness, and reactivity of an infant at birth are sensitive indices of the neonate's health, the quality of the pregnancy, and the mother's wellbeing. Even when fetal growth and gestation length have been normal, the maturing fetus can still be adversely impacted by both physical events and psychological challenges to the mother during the prenatal period. The following research evaluated 413 rhesus monkeys from 7 different types of pregnancies to determine which conditions significantly influenced the behavioral responsiveness and state of the young infant. A standardized test battery modeled after the Neonatal Behavioral Assessment Scale for human newborns was employed. The largest impairments in orientation and increases in infant emotional reactivity were seen when female monkeys drank alcohol, even though consumed at only moderate levels during part of the pregnancy. The infants' ability to focus and attend to visual and auditory cues was also affected when the gravid female's adrenal hormones were transiently elevated for 2 weeks by ACTH administration. In addition, responses to tactile and vestibular stimulation were altered by both this ACTH treatment and psychological disturbance during gestation. Conversely, a 2-day course of antenatal corticosteroids 1 month before term resulted in infants with lower motor activity and reactivity. These findings highlight several pregnancy conditions that can affect a young infant's neurobehavioral status, even when otherwise healthy, and demonstrate that alterations or deficits are specific to the type of insult experienced by the mother and fetus.     

Reference frames for representing visual and tactile locations in parietal cortex

The ventral intraparietal area (VIP) receives converging inputs from visual, somatosensory, auditory and vestibular systems that use diverse reference frames to encode sensory information. A key issue is how VIP combines those inputs together. We mapped the visual and tactile receptive fields of multimodal VIP neurons in macaque monkeys trained to gaze at three different stationary targets. Tactile receptive fields were found to be encoded into a single somatotopic, or head-centered, reference frame, whereas visual receptive fields were widely distributed between eye- to head-centered coordinates. These findings are inconsistent with a remapping of all sensory modalities in a common frame of reference. Instead, they support an alternative model of multisensory integration based on multidirectional sensory predictions (such as predicting the location of a visual stimulus given where it is felt on the skin and vice versa). This approach can also explain related findings in other multimodal areas.     

Interactions between sleep and sensory physiology

The processing of sensory information is definitely present during sleep, however, profound modifications occur. All sensory systems reviewed (visual, auditory, vestibular, somesthetic and olfactory) demonstrate some influence on sleep and, at the same time, sensory systems undergo changes that depend on the sleep or waking state of the brain. Thus, different sensory modalities encoded by their specific receptors and pathways may not only alter the sleep and waking physiology, but also the sleeping brain imposes ‘rules’ on the incoming information. It is suggested that the neural networks responsible for sleep and waking control are actively modulated by sensory inputs in order to enter and maintain normal sleep and wakefulness. Furthermore, both sensory stimulation and deprivation may induce changes in sleep/waking neural networks. This leads to the conclusion that the central nervous system and sensory input have reciprocal interactions, on which normal sleep/waking cycling and behaviour depends.