Effects of multimodal synchrony on infant attention and heart rate during events with social and nonsocial stimuli.

Attention is a state of readiness or alertness, associated with behavioral and psychophysiological responses, that facilitates learning and memory. Multisensory and dynamic events have been shown to elicit more attention and produce greater sustained attention in infants than auditory or visual events alone. Such redundant and often temporally synchronous information guides selectivity and facilitates perception, learning, and memory of properties of events specified by redundancy. In addition, events involving faces or other social stimuli provide an extraordinary amount of redundant information that attracts and sustains attention. In the current study, 4- and 8-month-old infants were shown 2-min multimodal videos featuring social or nonsocial stimuli to determine the relative roles of synchrony and stimulus category in inducing attention. Behavioral measures included average looking time and peak look duration, and convergent measurement of heart rate (HR) allowed for the calculation of HR-defined phases of attention: Orienting (OR), sustained attention (SA), and attention termination (AT). The synchronous condition produced an earlier onset of SA (less time in OR) and a deeper state of SA than the asynchronous condition. Social stimuli attracted and held attention (longer duration of peak looks and lower HR than nonsocial stimuli). Effects of synchrony and the social nature of stimuli were additive, suggesting independence of their influence on attention. These findings are the first to demonstrate different HR-defined phases of attention as a function of intersensory redundancy, suggesting greater salience and deeper processing of naturalistic synchronous audiovisual events compared with asynchronous ones.

Increased yolk testosterone facilitates prenatal perceptual learning in Northern bobwhite quail (Colinus virginianus).

Prenatal learning plays an important role in the ontogeny of behavior and birds provide a useful model to explore whether and how prenatal exposure to hormones of maternal origin can influence prenatal learning and the development of behavior. In this study we assessed if prenatal exposure to yolk testosterone can influence auditory learning in embryos of Northern bobwhite quail (Colinus virginianus). We experimentally enhanced testosterone concentrations in bobwhite quail eggs prior to incubation. The embryos from these T-treated eggs as well as control embryos that had received the vehicle-only or were non-treated were exposed to an individual bobwhite hen's maternal call for 120 min over the course of the day prior to hatching. All chicks were tested at 24 h following hatching for their auditory preference between the familiar bobwhite maternal call versus an unfamiliar bobwhite maternal call. T-treated chicks spent significantly more time in proximity to the familiar call compared to the unfamiliar call and also showed shorter latencies to approach the familiar call than control birds. Increased emotional reactivity, i.e. propensity to express fear responses, was also found in T-treated chicks. Baseline heart rates recorded in a second group of T-treated embryos and control embryos did not differ, which suggests no effect of yolk testosterone on baseline arousal level. To our knowledge this is the first demonstration of the influence of prenatal exposure to testosterone on auditory learning.

Extrinsic embryonic sensory stimulation alters multimodal behavior and cellular activation.

Embryonic vision is generated and maintained by spontaneous neuronal activation patterns, yet extrinsic stimulation also sculpts sensory development. Because the sensory and motor systems are interconnected in embryogenesis, how extrinsic sensory activation guides multimodal differentiation is an important topic. Further, it is unknown whether extrinsic stimulation experienced near sensory sensitivity onset contributes to persistent brain changes, ultimately affecting postnatal behavior. To determine the effects of extrinsic stimulation on multimodal development, we delivered auditory stimulation to bobwhite quail groups during early, middle, or late embryogenesis, and then tested postnatal behavioral responsiveness to auditory or visual cues. Auditory preference tendencies were more consistently toward the conspecific stimulus for animals stimulated during late embryogenesis. Groups stimulated during middle or late embryogenesis showed altered postnatal species-typical visual responsiveness, demonstrating a persistent multimodal effect. We also examined whether auditory-related brain regions are receptive to extrinsic input during middle embryogenesis by measuring postnatal cellular activation. Stimulated birds showed a greater number of ZENK-immunopositive cells per unit volume of brain tissue in deep optic tectum, a midbrain region strongly implicated in multimodal function. We observed similar results in the medial and caudomedial nidopallia in the telencephalon. There were no ZENK differences between groups in inferior colliculus or in caudolateral nidopallium, avian analog to prefrontal cortex. To our knowledge, these are the first results linking extrinsic stimulation delivered so early in embryogenesis to changes in postnatal multimodal behavior and cellular activation. The potential role of competitive interactions between the sensory and motor systems is discussed.

Intersensory redundancy educates selective attention in bobwhite quail embryos.

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

Prenatally elevated physiological arousal interferes with perceptual learning in bobwhite quail (Colinus virginianus) embryos.

Neonatal studies suggest elevated arousal can negatively influence perceptual and cognitive processes during early development. The authors explored this issue during the prenatal period by pharmacologically elevating physiological arousal in bobwhite quail (Colinus virginianus) embryos during exposure to a maternal call, then assessing preference for the familiar call following hatching. Embryos receiving norepinephrine showed a prenatal elevation in heart rate and failed to demonstrate a preference for the familiar call following hatching. Embryos not receiving norepinephrine showed no elevation in heart rate and demonstrated a preference for the familiar call. These results indicate elevated arousal can interfere with perceptual learning during the prenatal period and provide additional evidence for an optimal window of arousal necessary to foster species-typical perceptual functioning during early development.

Effects of 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.