The role of task difficulty in directing selective attention in bobwhite quail (Colinus virginianus) neonates: A developmental test of the intersensory redundancy hypothesis.

The dynamics of selective attention necessarily influences the course of early perceptual development. The intersensory redundancy hypothesis proposes that in early development information presented redundantly across two or more senses selectively recruits attention to the amodal properties of an object or event. In contrast, information presented to a single sense enhances attention to modality-specific properties. The present study assessed the second of these predictions in neonatal bobwhite quail (Colinus virginianus), with a focus on the role of task difficulty in directing selective attention. In Experiment 1, we exposed quail chicks to unimodal auditory, nonredundant audiovisual, or redundant audiovisual presentations of a bobwhite maternal call paired with a pulsing light for 10 min/h on the day following hatching. Chicks were subsequently individually tested 24 h later for their unimodal auditory preference between the familiarized maternal call and the same call with pitch altered by two steps. Chicks from all experimental groups preferred the familiarized maternal call over the altered maternal call. In Experiment 2, we repeated the exposure conditions of Experiment 1, but presented a more difficult task by narrowing the pitch range between the two maternal calls during testing. Chicks in the unimodal auditory and nonredundant audiovisual conditions preferred the familiarized call, whereas chicks in the redundant audiovisual exposure group showed no detection of the pitch change. Our results indicate that early discrimination of pitch change is disrupted by intersensory redundancy under difficult but not easy task conditions. These findings, along with findings from human infants, highlight the role of task difficulty in shifting attentional selectivity and underscore the dynamic nature of neonatal attentional salience hierarchies.

Hearing Better with the Right Eye? The Lateralization of Multisensory Processing Affects Auditory Learning in Northern Bobwhite Quail (Colinus Virginianus) Chicks.

Precocial avian species exhibit a high degree of lateralization of perceptual and motor abilities, including preferential eye use for tasks such as social recognition and predator detection. Such lateralization has been related, in part, to differential experience prior to hatch. That is, due to spatial and resulting postural constraints late in incubation, one eye and hemisphere-generally the right eye / left hemisphere-receive greater amounts of stimulation than the contralateral eye / hemisphere. This raises the possibility that the left hemisphere may specialize or show relative advantages in integrating information across visual and auditory modalities, given that it typically receives greater amounts of multimodal auditory and visual stimulation prior to hatch. The present study represents an initial investigation of this question in a precocial avian species, the Northern bobwhite quail (Colinus virginianus). Day-old bobwhite chicks received 5 min training sessions in which they vocalized to receive contingent playback of a bobwhite maternal call, presented with or without a light that flashed in synchrony with the notes of the call (i.e., bimodal versus unimodal exposure, respectively). Chicks were trained with or without eye patches that allowed them to experience the visual component of the bimodal stimulus with only the left eye (LE), right eye (RE), or both eyes (i.e., binocular; BIN). Finally, the light was placed in various positions relative to the speakers playing the maternal call across three experiments. 24 hrs later chicks were provided a simultaneous choice test between the familiarized and a novel bobwhite maternal call. Given that the right eye and ear typically face outward and are thus unoccluded by the body during late prenatal development, we hypothesized that RE chicks would show facilitated learning under bimodal conditions compared to all other training conditions. This hypothesis was partially confirmed in Experiment 1, when the light was positioned 40 cm above the source of the maternal call. However, we also observed evidence of suppressed learning in chicks provided BIN exposure to the bimodal audio-visual stimulus that was not present during auditory-only training. Experiments 2 and 3 demonstrated that this was likely related to activation of a left-hemisphere dependent fear response when the left eye was exposed to a visual stimulus that loomed above the auditory stimulus. These results indicate that multisensory processing is lateralized in a precocial bird and that these species may thus provide a unique model for studying experience-dependent plasticity of intersensory perception.

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.

The influence of prenatal experience on behavioral and social development: The benefits and limitations of an animal model.

Prenatal experience is both a formative and a regulatory force in the process of development. As a result, birth is not an adequate starting point for explanations of behavioral development. However, surprisingly little is currently known regarding the role of prenatal experience in the emergence and facilitation of perceptual, cognitive, or social development. Our lack of knowledge in this area is due in part to the very restricted experimental manipulations possible with human fetuses. A comparative approach utilizing animal models provides an essential step in addressing this gap in our knowledge and providing testable predictions for studies with human fetuses, infants, and children. Further, animal-based comparative research serves to minimize the amount of exploratory research undertaken with human subjects and hone in on issues and research directions worthy of further research investment. In this article, I review selected animal-based research exploring how developmental influences during the prenatal period can guide and constrain subsequent behavioral and social development. I then discuss the importance of linking the prenatal environment to postnatal outcomes in terms of how psychologists conceptualize "innate" biases, preferences, and skills in the study of human development.

The intersensory redundancy hypothesis: Extending the principle of unimodal facilitation to prenatal development.

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.

Elevated yolk progesterone moderates prenatal heart rate and postnatal auditory learning in bobwhite quail (Colinus virginianus).

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.

Increased yolk progesterone interferes with prenatal auditory learning and elevates emotional reactivity in bobwhite quail (Colinus virginianus) chicks.

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..

Neural correlates of intersensory processing in 5-month-old infants.

Two experiments assessing event-related potentials in 5-month-old infants were conducted to examine neural correlates of attentional salience and efficiency of processing of a visual event (woman speaking) paired with redundant (synchronous) speech, nonredundant (asynchronous) speech, or no speech. In Experiment 1, the Nc component associated with attentional salience was greater in amplitude following synchronous audiovisual as compared with asynchronous audiovisual and unimodal visual presentations. A block design was utilized in Experiment 2 to examine efficiency of processing of a visual event. Only infants exposed to synchronous audiovisual speech demonstrated a significant reduction in amplitude of the late slow wave associated with successful stimulus processing and recognition memory from early to late blocks of trials. These findings indicate that events that provide intersensory redundancy are associated with enhanced neural responsiveness indicative of greater attentional salience and more efficient stimulus processing as compared with the same events when they provide no intersensory redundancy in 5-month-old infants.

The concept of homology as a basis for evaluating developmental mechanisms: exploring selective attention across the life-span.

Research with human infants as well as non-human animal embryos and infants has consistently demonstrated the benefits of intersensory redundancy for perceptual learning and memory for redundantly specified information during early development. Studies of infant affect discrimination, face discrimination, numerical discrimination, sequence detection, abstract rule learning, and word comprehension and segmentation have all shown that intersensory redundancy promotes earlier detection of these properties when compared to unimodal exposure to the same properties. Here we explore the idea that such intersensory facilitation is evident across the life-span and that this continuity is an example of a developmental behavioral homology. We present evidence that intersensory facilitation is most apparent during early phases of learning for a variety of tasks, regardless of developmental level, including domains that are novel or tasks that require discrimination of fine detail or speeded responses. Under these conditions, infants, children, and adults all show intersensory facilitation, suggesting a developmental homology. We discuss the challenge and propose strategies for establishing appropriate guidelines for identifying developmental behavioral homologies. We conclude that evaluating the extent to which continuities observed across development are homologous can contribute to a better understanding of the processes of development.

Development as explanation: Understanding phenotypic stability and variability after the failure of genetic determinism.

In the predominately gene-centered view of 20th century biology, the relationship between genotype and phenotype was essentially a relationship between cause and effect, between a plan and a product. Abandoning the idea of genes as inherited instructions or blueprints for phenotypes raises the question of how to best account for observed phenotypic stability and variability within and across generations of a population. We argue that the processes responsible for phenotypic stability and the processes responsible for phenotypic variability are one and the same, namely, the dynamics of development. This argument proposes that stability of phenotypic form is found not because of the transmission of genotypes, genetic programs, or the transfer of internal blueprints, but because similar internal and external conditions-collectively conceptualized as resources of development-can be reliably reconstituted in each generation. Variability of phenotypic form, which is an indispensable feature of any evolving system, relies on these same resources, but because the internal and external conditions of development are not reconstituted identically in succeeding generations, these conditions-and the phenotypes to which they give rise-will always be characterized by at least some variability.

From gene activity to behavior (and back again).

Documenting the bidirectional traffic from gene action to the external environment and its effects on behavior remains a major conceptual, empirical, and analytical challenge for developmental science. Charney has provided an instructive snapshot of where we are in meeting this challenge and, in so doing, exposes the considerable shortcomings of the traditional genomic model employed by behavior genetics.

How deep do we have to go to rehabilitate evolutionary psychology? Reply to Bjorklund et al. (2022).

Disciplines like evolutionary developmental psychology admirably focus on trying to rehabilitate narrow evolutionary psychology (NEP) from within, by adding a developmental focus to NEP's tenets of adaptationism and computationalism. We argue, however, that these tenets are fundamentally incompatible with taking psychology and its development seriously, and that the kinds of modifications introduced by evolutionary developmental psychologists do not go deep enough to qualitatively change the nondevelopmental outlook of NEP. (PsycInfo Database Record (c) 2022 APA, all rights reserved).

Evolving evolutionary psychology.

Which evolutionary theory can best benefit psychological theory, research, and application? The most well-known school of evolutionary psychology has a narrow conceptual perspective (a.k.a., "Narrow Evolutionary Psychology" or NEP). Proponents of NEP have long argued that their brand of evolutionary psychology represents a full-fledged scientific revolution, with Buss (2020) recently likening NEP's scientific impact to that of a Copernican or Darwinian paradigm shift. However, NEP stands on two traditions that are now the subjects of serious debate and revision: the neo-Darwinian adaptationist framework within evolutionary biology, and the computationalist "mind-as-computer" framework within cognitive science. Although NEP calls itself revolutionary, the significant revolutions taking place today in both evolutionary biology and cognitive science reveal NEP to be rooted in the orthodoxies of the past. We propose a more inclusive, developmental evolutionary psychology theory (DEPTH) better suited for our field in multiple ways, from acknowledging epigenesis to incorporating developmental science. To discern appropriate baselines for human nature and for human becoming, one must integrate developmental neuroscience, anthropology, and cognitive archeology. To be of value in addressing and remedying the challenges facing humanity, psychological theories must recognize the central importance of our plasticity, evolved developmental niche, and deep history. (PsycInfo Database Record (c) 2022 APA, all rights reserved).

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.

Increasing task difficulty enhances effects of intersensory redundancy: testing a new prediction of the Intersensory Redundancy Hypothesis.

Prior research has demonstrated intersensory facilitation for perception of amodal properties of events such as tempo and rhythm in early development, supporting predictions of the Intersensory Redundancy Hypothesis (IRH). Specifically, infants discriminate amodal properties in bimodal, redundant stimulation but not in unimodal, nonredundant stimulation in early development, whereas later in development infants can detect amodal properties in both redundant and nonredundant stimulation. The present study tested a new prediction of the IRH: that effects of intersensory redundancy on attention and perceptual processing are most apparent in tasks of high difficulty relative to the skills of the perceiver. We assessed whether by increasing task difficulty, older infants would revert to patterns of intersensory facilitation shown by younger infants. Results confirmed our prediction and demonstrated that in difficult tempo discrimination tasks, 5-month-olds perform like 3-month-olds, showing intersensory facilitation for tempo discrimination. In contrast, in tasks of low and moderate difficulty, 5-month-olds discriminate tempo changes in both redundant audiovisual and nonredundant unimodal visual stimulation. These findings indicate that intersensory facilitation is most apparent for tasks of relatively high difficulty and may therefore persist across the lifespan.

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.

Bobwhite quail (Colinus virginianus) hatchlings track the direction of human gaze.

Gaze following allows individuals to detect the locus of attention of both conspecifics and other species. However, little is known about how this ability develops. We explored the emergence of bobwhite quail hatchlings' ability to track human gaze by assessing their avoidance behavior in an open arena under five testing conditions: (1) a Direct Gaze condition, in which an experimenter looking down was positioned above one of two approach areas; (2) a Gaze Follow condition in which an experimenter, positioned equidistant between two approach areas, directed his/her gaze towards one of the areas; (3) a Masked Gaze Follow condition, in which the experimenter wore a mask during the Gaze Follow test; (4) a Deprived Face Experience condition, in which hatchlings were deprived of experience with human faces prior to the Gaze Follow test; and (5) a Control condition in which no experimenter was present during testing. Results revealed that hatchlings from the Direct Gaze condition preferred the non-gazed approach area at all ages tested. Hatchlings from the Gaze Follow condition preferred the non-gazed approach area at 48 and 72 h, but not at 24 h of age. In contrast, hatchlings from the Masked Gaze Follow, Deprived Face and Control conditions did not prefer either approach area at any age tested. These results indicate that experience with human faces plays a key role in the rapid emergence of gaze following behavior in bobwhite quail hatchlings.

Operant generalization of auditory tempo in quail neonates.

Operant generalization, a building block of cognition, has never been studied in neonates. We developed a preparation for newly hatched quail in order to investigate the form of the generalization gradient very early in development. For their first 4-5 days after hatching, northern bobwhite chicks pecked for brief heat presentations while hearing a high-pitched sound repeated at a constant rate (nondifferential training). Tempo generalization was then assessed in extinction. A significantly excitatory average gradient resulted despite minimal postnatal experience.

Prenatal light exposure influences gait performance and body composition in bobwhite quail chicks.

Maternal nesting behavior, which includes periods of patterned inattention, provides key elements essential for avian embryonic development, including regulation of temperature and light. For example, avian research consistently shows the importance of prenatal light exposure for several developmental processes; however, this research has primarily focused on artificial light regimens (i.e. 24 hr, 0 hr light). Comparatively less is known about how exposure to naturally occurring light patterns during incubation influence motor performance, body composition (i.e. body mass, bone length), and developmental age (incubation length). Here we conducted two experiments which investigated the effects of prenatal light exposure on developmental age, body composition, and gait performance in 1-day-old bobwhite quail. Experiment 1 investigated crepuscular light exposure during the last two days of incubation under two light duration treatments (2 hr & 6 hr) compared to a 12 hr continuous light schedule. Results indicated crepuscular prenatal light experience extended the incubation period for 2 hr exposed embryos, but not for 6 hr exposed embryos and negatively influenced postnatal body composition and postnatal gait performance when compared to 12 hr continuous light embryos. Experiment 2 examined the influence of prenatal light duration (2 hr vs 6 hr) and light presentation (crepuscular vs sporadic). Results demonstrated sporadic light presentation improved gait performance in 2 hr exposed hatchlings, but not 6 hr exposed hatchlings, improved body composition in 6 hr exposed hatchlings, but not 2 hr exposed hatchlings, and did not alter incubation length when compared to crepuscular light counterparts. This study provides further evidence for the importance of maternally regulated sensory stimulation during the prenatal period on early postnatal motor development.

Prenatal incubation temperature affects neonatal precocial birds' locomotor behavior.

Temperature during the prenatal period is an important factor for developing embryos. Extensive human and animal research indicate embryos are sensitive to small fluctuations in temperature which has profound effects on phenotype development. Much of this research has focused on survivability, morphology, and incubation duration, but comparatively less in known about how prenatal temperature influences the development of motor coordination. In this study, we experimentally tested whether exposure to naturally occurring cool (36.9 °C) or warm (38.1 °C) thermal conditions for a brief period (4 days) during early incubation can influence postnatal motor performance in neonatal bobwhite quail hatchlings. We compared gait spatiotemporal parameters, body kinematics, and locomotive behaviors of control chicks incubated in an optimal thermal environment (37.5 °C) with thermally manipulated chicks. Experimental temperature treatment began on embryonic day five (E5) and ended on E8. Chicks were tested 24-h after hatching. Cool thermal exposure during incubation delayed hatching, reduced body mass, and increased fall frequency, intertarsal joint angle and stride length variability during the gait task compared to optimally incubated chicks. Warm thermal exposure during incubation delayed bone growth and increased fall frequency relative to controls. We discuss the relationship between motor development and thermal regulatory processes and provide insight into how spatiotemporal parameters aid in elucidating subtle differences in coordinated movement which may contribute to atypical motor development and be associated with neural developmental disorders. We provide the first spatiotemporal evidence for the importance of optimal thermal microclimates for typical prenatal motor development.