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Visually imprinted maternal preference in ducklings is redirected by social interaction with siblings.

This study examined the influence of social interaction with broodmates on a visually imprinted maternal preference in domestic mallard ducklings (Anas platyrhynchos) during the first three days of postnatal life. Twenty-four-hour-old ducklings were allowed to follow a stuffed mallard hen for 30 min. This experience resulted in a visually imprinted preference for the familiar stuffed hen over 4 stuffed ducklings in simultaneous choice tests at 48 and 72 hr after hatching, but only if the imprinted birds were kept in social isolation. Imprinted ducklings reared in a social group containing either same-age siblings or the stuffed mallard hen and same-age siblings displayed a visual preference for the stuffed ducklings over the familiar mallard hen at 48 and 72 hr tests. As a first step in the analysis of the features of the social exposure to siblings that are necessary for the redirection of the visually imprinted maternal preference, it was found that direct social interaction is essential to establish the preference for ducklings, but even mere visual exposure to siblings does away with the imprinted maternal preference. These results provide striking evidence of the ready redirection of a species-specific maternal preference in otherwise imprinted ducklings.

Animals↗

Training ducklings in broods interferes with maternal imprinting.

Under natural conditions, if maternal imprinting is to occur it must occur in a social situation which includes the presence of broodmates. In the laboratory it has been shown that social rearing with siblings prior to maternal imprinting interferes with the establishment of maternal imprinting, whereas social experience with siblings after maternal imprinting enhances the imprinting experience. The present study examined the influence of social experience with broodmates during an imprinting trial on the establishment of a visually imprinted maternal preference in domestic mallard ducklings (Anas platyrhynchos). Twenty-four-hour-old ducklings were allowed to follow a stuffed mallard hen for 30 min either individually or in a brood of four same-aged ducklings. The birds trained alone subsequently showed an imprinted preference for the familiar mallard hen over an unfamiliar pintail hen or four stuffed ducklings in simultaneous choice tests at 48 and 72 hr after hatching. Ducklings trained with broodmates did not show a preference for the familiar mallard hen over the unfamiliar pintail hen and displayed a preference for the stuffed ducklings over the mallard hen at 48 and 72 hr choice tests. These results demonstrate that even brief (30 min) experience with siblings during a maternal imprinting trial results in peer imprinting that interferes with the establishment of maternal imprinting. These and other results of a similar sort render dubious the significance of most laboratory studies of imprinting for an understanding of such events in nature.

Age Factors↗

Does behavior contingent stimulus movement enhance filial imprinting in Japanese quail?

Japanese quail chicks were exposed for 2.5 hrs to either a white or a normal stuffed adult conspecific (= model). During this period the model was either nonmoving or it moved for short periods. This movement could be contingent or noncontingent upon distress calls of the chicks. In each condition, exposure led to a significant preference for the familiar model over the nonfamiliar one during a 10-min choice test. Chicks exposed to a nonmoving model had the weakest preference for the familiar model, whereas this preference was strongest in chicks exposed to the contingent moving model; the preference of the chicks exposed to the noncontingent moving model was in between. The results indicate that the extend to which stimulus movement enhances filial imprinting depends on the relation between the chicks behavior and the timing of the stimulus movement. However, it is not clear yet whether the effect arose because the chicks perceived the contingency between the stimulus movement and their behavior or by another mechanism.

Animals↗

Social specificity: interaction with own species is necessary to foster species-specific maternal preference in ducklings.

Previous studies have shown that if domestic mallard ducklings are allowed social interaction with broodmates after their initial exposure to a stuffed mallard (Anas platyrhynchos) hen, they later show a visual preference for the familiar mallard over an unfamiliar redhead (Aythya americana) hen. Birds kept in social isolation do not make this difficult discrimination. In the present study, we examined whether this social enhancement of imprintability to a natural maternal model is merely the result of social stimulation in its most general sense, or if its effects are specific to social interaction for 30 min (training). This experience resulted in visual preference for the familiar mallard hen over the unfamiliar redhead hen in simultaneous choices tests at 48 hr and 72 hr after hatching only if the birds were allowed social experience with a group of same-age undomesticated mallard hatchings. No visual preference for the familiar mallard hen was found if the ducklings were permitted social experience with a group of same-age chick (Gallus domesticus) hatchlings or muscovy (Cairina moschata) ducklings. Thus, it appears that for ducklings to show a visually imprinted preference for a natural maternal model, they must be allowed social interaction with broodmates of their own species. Social rearing with other precocial bird hatchlings, even other ducklings, is without apparent effect. These results provide further evidence of the importance of nonobvious experimental factors in the development of species-typical behavior. They also suggest that in the evolution of the species-specific learning underlying early species identification, natural selection has operated on the entire (organism-environment) developmental manifold and not merely on genetic, organic, or organismic aspects of that system.

Animals↗

Metaphors for development: how important are experiences early in life?

The many students of development have held rather diverse views on the importance of early experience. Some gave early experiences great prominence (e.g., Freud and his followers, Kuo, 1967), while others largely rejected the pivotal importance of particular early events (e.g., Thorndike), and yet others took a more eclectic tack: Some events in certain species but not all events or in all cases (e.g., Hinde, 1974, Lehrman, 1970). The extremes among the prevailing views are often characterized metaphorically. I propose to do this, then to examine the kinds of situations the metaphors describe, and inquire into their generality and usefulness. Clearly this runs the risk of undue simplification, but there is, I believe merit in occasionally ignoring some of the subtleties that usually must concern us.

Animals↗

Maternal and peer imprinting in mallard ducklings under experimentally simulated natural social conditions.

Previous studies revealed that if socially reared mallard ducklings actively follow a stuffed mallard (Anas platyrhynchos) hen, they later show a visual preference for the familiar mallard hen over an unfamiliar redhead (Aythya americana) hen. The present study determined that the experience of actively following the hen is essential to the induction of a visually controlled, species-typical, maternal preference. Domestic mallard ducklings that had not been given the opportunity to follow the mallard hen were "passively" reared in social groups consisting of a stuffed mallard hen and seven same-aged siblings for either 24, 48, or 72 hr after hatching. These birds were largely unresponsive to the hen in a later choice test, even when they were passively exposed to the mallard hen for as long as 72 hr prior to testing. The question arose as to whether passive exposure to the ducklings induced a preference for them that interfered with establishment of maternal imprinting under these simulated natural nest conditions. Results indicated that socially reared ducklings do prefer stuffed ducklings to a stuffed mallard hen in a simultaneous choice test even when the hen is present and vocalizing during social rearing. Further, even ducklings reared individually with the mallard hen were unresponsive to her in the later choice test. That there is something special about the stimulation provided by ducklings was further demonstrated by the finding that stuffed ducklings were preferred over the mallard hen (1) when the social rearing situation precluded active physical interaction with live ducklings and (2) when reared with inanimate stuffed ducklings. Thus, the ineffectiveness of the stuffed mallard hen in inducing visual imprinting under simulated nesting conditions cannot be attributed to the fact that she was not alive or reciprocally interactive. The present results suggest that mallard ducklings do not become visually imprinted to their hen until after departure from the nest, that the visual component of maternal imprinting likely involves active following subsequent to nest departure, and that early in postnatal development siblings are more visually attractive than is the hen.

Animals↗

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.

Acoustic Stimulation↗

The effect of the neurotoxin DSP4 on the development of a predisposition in the domestic chick.

Under certain conditions, dark-reared chicks preferentially approach objects resembling conspecifics. In the current study we investigated the effect of the catecholaminergic neurotoxin DSP4 on this predisposition. After hatching, chicks received an intraperitoneal injection of either DSP4 or vehicle (controls). The chicks were individually placed in running wheels for 2 x 1 hr, 24 hr before testing. The chicks were maintained in darkness until given a preference test, which involved the simultaneous presentation of an illuminated red box and a stuffed fowl at 36, 48, 60, 66, or 72 hr after hatching. The approach of each chick toward the two objects was recorded over 5 min and a preference score calculated. Control chicks placed in the running wheels at 24 and 36 hr posthatch and tested 24 hr later showed a significant preference for the fowl compared to the red box. In contrast, DSP4-treated chicks did not show such a preference at corresponding ages, but did express a greater preference for the fowl when placed in the running wheels at 42 and 48 hr posthatch and tested 24 hr later. These results suggest that experience of the running wheel or of associated factors, e.g., handling, must occur during a restricted period of time to influence the emergence of the predisposition to approach the stuffed fowl. DSP4 treatment delays the onset of this period.

Animals↗

Stability of preference for odors after short-term exposure in young spiny mice.

The stability of olfactory preferences for artificial odors was studied in young spiny mouse pups (Acomys cahirinus). Subjects aged between 2 and 20 days were exposed to the odor of either cinnamon or cumin for 1.5 hr. The durability of preferences for the familiar versus novel odor was subsequently monitored in a three-choice preference test. The results suggest the existence of a sensitive phase for learning odor characteristics, through simple exposure, between Days 2 and 18 of the pups' postnatal life. The sensitive phase proved not to be an "on-off" process, but the strongest effect of exposure to odors took place at about Days 4 and 6. However, the duration of preference for exposed odors was dependent on later experience with the odors during retests. The results point to an unusual plasticity in rapid learning of odors through simple exposure in precocial young spiny mice.

Age Factors↗

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 maternal 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.

Animals↗

c-fos is induced in the hippocampus during consolidation of sexual imprinting in the zebra finch (Taeniopygia guttata).

c-fos was used to mark regions of enhanced neuronal activity during sexual imprinting, an early learning process by which information about the prospective sexual partner is acquired and consolidated. In the present study, we demonstrate that the hippocampus, already known for its specialized spatial memory capacities in navigating pigeons and in food-storing birds, depicts a selective differential c-fos induction in a situation shown to lead to sexual imprinting, that is, exposing previously isolated male birds to a female for 1 h. c-fos induction is lateralized, the left hippocampus showing more c-fos activity than the right. Our results would indicate a role for the hippocampus in the consolidation process of imprinting, probably in the transfer of information to the other telencephalic areas that show alterations in synaptic connectivity as a result of consolidation of sexual imprinting.

Animals↗

Cholinergic synaptic signaling mechanisms underlying behavioral teratogenicity: effects of nicotine, chlorpyrifos, and heroin converge on protein kinase C translocation in the intermedial part of the hyperstriatum ventrale and on imprinting behavior in an avian model.

A wide variety of otherwise unrelated neuroteratogens elicit a common set of behavioral defects centering around cholinergic contributions to cognitive function. We utilized the developing chick to overcome confounds related to maternal effects and compared the actions of nicotine, chlorpyrifos, and heroin on cholinergic signaling in the intermedial part of the hyperstriatum ventrale (IMHV), which controls imprinting behavior. Chicken eggs were injected with nicotine (10 mg/kg of egg), chlorpyrifos (10 mg/kg of egg), or heroin (20 mg/kg of egg; all doses below the threshold for dysmorphology) on incubation days (ID) 0 and 5, and then tests were conducted posthatching. All three compounds elicited significant deficits in imprinting behavior. We also found defects in cholinergic synaptic signaling specifically involving the muscarinic receptor-mediated membrane translocation of protein kinase C (PKC)-gamma and in the basal levels of both PKCgamma and PKCbetaII, the two isoforms known to be relevant to behavioral performance. In contrast, there were no alterations in the response of PKCalpha, an isoform that does not contribute to the behavior, nor were cytosolic levels of any of the isoforms affected. Taken together with similar results obtained in rodents, our findings suggest that disparate neuroteratogens all involve signaling defects centering on the ability of cholinergic receptors to elicit PKCgamma translocation/activation and that this effect is direct, i.e., not mediated by maternal confounds. The chick thus provides a suitable model for the rapid screening of neuroteratogens and elucidation of the mechanisms underlying behavioral anomalies.

Analysis of Variance↗

Olfactory imprinting is correlated with changes in gene expression in the olfactory epithelia of the zebrafish.

Odors experienced as juveniles can have significant effects on the behavior of mature organisms. A dramatic example of this occurs in salmon, where the odors experienced by developing fish determine the river to which they return as adults. Further examples of olfactory memories are found in many animals including vertebrates and invertebrates. Yet, the cellular and molecular bases underlying the formation of olfactory memory are poorly understood. We have devised a series of experiments to determine whether zebrafish can form olfactory memories much like those observed in salmonids. Here we show for the first time that zebrafish form and retain olfactory memories of an artificial odorant, phenylethyl alcohol (PEA), experienced as juveniles. Furthermore, we demonstrate that exposure to PEA results in changes in gene expression within the olfactory sensory system. These changes are evident by in situ hybridization in the olfactory epithelium of the developing zebrafish. Strikingly, our analysis by in situ hybridization demonstrates that the transcription factor, otx2, is up regulated in the olfactory sensory epithelia in response to PEA. This increase is evident at 2-3 days postfertilization and is maintained in the adult animals. We propose that the changes in otx2 gene expression are manifest as an increase in the number of neuronal precursors in the cells olfactory epithelium of the odor-exposed fish. Thus, our results reveal a role for the environment in controlling gene expression in the developing peripheral nervous system.

Animals↗

Effects of imprinting on lysine uptake and incorporation into protein in chick brain.

One-day old chicks were exposed for either 30, 60, or 120 min to an imprinting stimulus or kept in darkness in similar conditions. At the end of this time they were injected peripherally with 14C-lysine and killed 20 min later. The radioactivity of free lysine and that incorporated into protein was measured; incorporation was found to differ between exposed and dark birds only in the anterior part of the forebrain roof after 60-min treatment (E/D = 1.25). However, more free radioactive lysine was found in all brain regions of exposed birds at this time. When the specific radioactivity of the free lysine (dpm/nmol lysine) was measured there were no differences between the two types of birds, indicating that the incorporation difference was not due to a change in precursor radioactivity. The use of 14C-2-aminoisobutyrate confirmed that even with a nonincorporated amino acid pool size changes still occurred. The greater lysine incorporation in anterior forebrain roof was largely restricted to the cytoplasmic soluble fraction.

Aminoisobutyric Acids↗

Analysis and identification of imprinted genes.

Genomic imprinting in mammals results in the unequal expression of the two parental alleles of specific genes. The existence of imprinting in the mouse emerged from nuclear transplantation studies and from the abnormal phenotypes associated with uniparental inheritance of particular chromosome segments. Over the past 5 years, 20 or so imprinted genes have been identified. This has emphasized the important roles played by some imprinted genes in development, permitted a description of the epigenetic properties associated with imprinting, and provided the first insights into the regulation of imprinting. In this article, we discuss the generation of experimental material in which imprinting effects can be analyzed, review the properties of imprinted genes, and discuss how to examine them using state-of-the-art techniques. Finally, we consider the means by which new imprinted genes can be identified.

Alleles↗

Influence of the N-methyl-D-aspartate receptor antagonist DL-2-amino-5-phosphonovaleric acid on auditory filial imprinting in the domestic chick.

Newly hatched domestic chicks were injected uni- or bilaterally into the imprinting relevant forebrain region mediostral neostriatum/ hyperstriatum ventrale (MNH) with different concentrations (1, 3, 12.5, 50 nmol) of the competitive NMDA antagonist DL-5-amino-5- phosphonovaleric acid (APV) prior to exposure to the imprinting stimulus (400-Hz tone pulses). In both APV-injected experimental groups there was a dose-dependent decrease of imprinting rates compared to that seen in controls, suggesting an APV-induced blockade of the learning process. In order to find out how the injected APV interferes with the stimulus-evoked enhanced metabolic activity in imprinting-relevant brain regions and to gain information about the spatial extent of its physiological effect, 2-fluorodeoxyglucose (2-FDG) experiments were performed. Chronically APV-treated chicks which failed in the imprinting tests showed similarly low 2-FDG uptake in imprinting relevant areas as naive untreated controls, further suggesting that no learning process has occurred in these animals. In imprinted chicks acute APV injections into the MNH led to a suppression of the stimulus-evoked 2-FDG uptake in this region. This pharmacologically induced reduction extended beyond the MNH region to adjacent regions. Furthermore, unilateral injections into the MNH always resulted in a bilateral reduction of 2-FDG uptake in this area. The results suggest that NMDA-mediated mechanisms in restricted telecephalic areas such as the MNH play a crucial role in the process of auditory filial imprinting.

2-Amino-5-phosphonovalerate↗

Lesions of the intermediate medial hyperstriatum ventrale impair sickness-conditioned learning in day-old chicks.

Lesion studies show that the intermediate medial hyperstriatum ventrale (IMHV), a forebrain visual association area in chicks, is involved in learning and memory for one-trial passive avoidance and imprinting. We examined the effects of IMHV lesions in a one-trial, nongustatory, sickness-conditioned learning task. This task is similar to passive avoidance and imprinting because all three tasks require the chick to remember visual cues in order to respond correctly. However, sickness-conditioned learning differs from imprinting and passive avoidance because it uses sickness as the aversive stimulus and there is a longer conditioned stimulus-unconditioned stimulus interval (30-min delay compared to seconds). Bilateral IMHV lesions given 24 h before training impaired the ability of the chicks to avoid a bead associated with sickness produced by lithium chloride injection, as did pretraining unilateral left or right IMHV lesions. Post-training IMHV lesions given 1 h after training did not impair avoidance of the test bead in the sickness-conditioned learning task. However, lesioned chicks showed generalized avoidance of all test beads. The pretraining lesion results are similar to those found in imprinting and passive avoidance learning; however, the effects of unilateral IMHV lesions differed. Post-training lesion effects are similar to those found in passive avoidance learning. We propose that both left and right IMHV are necessary for sickness-conditioned learning and that post-training IMHV lesions impair the ability of the chick to learn or remember the association between the color of the bead and the aversive consequences of LiCl injection.

Age Factors↗

Evidence for the involvement of two areas of the zebra finch forebrain in sexual imprinting.

Sexual imprinting in male zebra finches is a two-step process, including an acquisition period early in life and a stabilization process normally occuring during the first courtship attempts of the male. During the acquisition period, a young male learns about its social environment. During stabilization, which can be delayed experimentally until day 100, it develops a preference for the appropriate object for courtship behavior on the basis of its previous and acute experience. Thereafter, this preference cannot be altered again. Exploring the physiological basis for imprinting, we have previously shown that the neurons of two forebrain areas (ANC and HAD) increase their spine density in the course of the stabilization process, while in two other areas (MNH and LNH) a decrease of spine density can be observed. With the present experiments, we tested the idea that the spine density decrease in MNH and LNH is the anatomical manifestation of the imprinting process. Previous behavioral experiments have shown that exposure to a nestbox after 100 days of age stabilizes the sexual preference of a zebra finch male as well as does exposure to a female. The present study shows that nestbox exposure also reduces the spine density in MNH and LNH, but has no effect on ANC and HAD. It has also been shown previously that treating males with an antiandrogen between days 40 and 100 affects the final preference of a male. The present experiment indicates that the same treatment affects spine growth during development in MNH and LNH and prevents the increase of spine density within HAD and ANC normally induced by exposure to a female. The results are interpreted as strong evidence for the involvement of MNH and LNH in sexual imprinting.

Androgen Antagonists↗