Familiarity interferes with filial imprinting

The present study was performed to investigate whether and how pre-exposure to an object affects subsequent filial imprinting to that object. In Experiment 1 junglefowl chicks (Gallus gallus spadiceus) were first exposed to either a red object alone (control group), or a red and a yellow object simultaneously (experimental group; phase 1). Subsequently, all chicks were exposed to the yellow object in the presence of a black and blue one (phase 2). At the end of phase 1, most experimental chicks had developed a preference for the red object over the yellow one. At the end of phase 2, preferences of experimental chicks were shifted away from the yellow object towards the novel black and blue object, relative to preferences of control chicks. This shows that pre-exposure may interfere with imprinting. Experiment 2 revealed that when control chicks were tested with the yellow object at the end of phase 1, filial responses were as strong as in experimental chicks. This shows that the yellow object had not acquired control over filial behaviour during phase 1, and also that the relatively impaired imprinting on that object in phase 2 was not due to reduced generalization from the red object. One possible explanation why pre-exposure may interfere with imprinting is that familiarity alters the level of attention attracted by an object, a mechanism suggested to underlie ‘latent inhibition’ in conditioning.     

Pecking: another measurement for filial attachment in group-reared domestic fowl chicks

This study examines different types of attachment measurements and pecking behavior in group-reared domestic chicks imprinted to a silent imprinting object. Immediately upon arriving from the hatchery, groups of heavy strain chicks were imprinted to a colored foam rubber ball for 72 h. The bond between these chicks and the imprinting object was then tested from 8 days until 5 weeks of age. Three days of imprinting sessions demonstrated that a strong attachment could be formed between the imprinted chicks and the imprinting object. In both experimental and control groups, the number of pecks was found to be significantly correlated with the latency measurements. It is, therefore, reasonable to consider the number of pecks of the imprinting object as another measurement for filial attachment.     

Neural bases of recognition memory investigated through an analysis of imprinting

Through a learning process known as imprinting, the young of some animals, including the domestic chick, come to recognize an object by being exposed to it. Visually naive chicks vigorously approach a wide range of objects. After an adequate period of exposure to one object chicks selectively approach it in a recognition test. The nervous system of dark-reared chicks is not a tabula rasa, as chicks have predispositions to approach some stimuli rather than others. Nevertheless, visual imprinting leads to changes in a nervous system that may not have been 'marked' by previous visual experience, and so encourages the hope of discovering the neural bases of the learning process. The intermediate and medial part of the hyperstriatum ventrale, a sheet of cells within the cerebral hemispheres, plays a crucial role in visual imprinting, particularly in the memory process of recognition. The cellular and sub-cellular changes that take place in this part of the hyperstriatum ventrale after imprinting are described. The right and left hyperstriatum ventrale regions play different roles in the imprinting process, and evidence is given for the existence of multiple memory systems in the chick brain.     

Ontogeny of magnetoreception in chickens (Gallus gallus domesticus)

Chickens are precocial birds, capable of moving independently from within a few hours of hatching, and thus provide a useful model to investigate the development of magnetoreception in young birds. Chicks show some sharply-timed behavioural changes at around 11 days of age that may be indicative of improvements in navigation ability around this age. We trained Young (<10 days, n = 7) and Old (11 days or older, n = 6) chicks to find a hidden imprinting stimulus behind one of four screens in a square arena. Once criterion was reached, the directional choices of chicks were recorded in unrewarded tests in the geomagnetic field and in an experimental field shifted by 90° clockwise. These tests were separated with rewarded training trials to avoid extinction. In the first, and the first 3 tests, no indication was found that chicks chose the correct unimodal magnetic direction. Instead, in all tests, Old chicks preferred the screens in the same magnetic axis as the training direction in tests in the geomagnetic and shifted experimental fields significantly more than Young chicks (P < 0.05). Choices of Young chicks were no different to chance in tests, whereas choices by Old chicks were significantly different from chance (P < 0.05). Our findings support the hypothesis that magnetoreception appears in the second week of life in the chicken. It is, however, unclear when a truly directional magnetic response (i.e. an unimodal, rather than axial, response in our test) develops that could be used by the chicks for accurate navigation.     

Predispositions and preferences. Effects on imprinting of lesions to the chick brain

Domestic chicks were exposed to a moving, stuffed jungle fowl or a rotating red box. The effects on the imprinting process of lesions to a restricted part of the hyperstriatum ventrale (IMHV) were studied in a series of experiments. Sham-operated control chicks developed a strong preference for the training object. Damage to IMHV impaired chicks' preferences for the training stimulus. However, the effect on chicks exposed to the red box was profound, whereas the effect on chicks exposed to the jungle fowl was relatively weak. The results suggest that information about a complex object, which in the experiments described resembled the chicks' own species, is stored in a different way from information derived from a relatively simple artificial object.     

Visual lateralization and development of spatial and social spacing behaviour of chicks (Gallus gallus domesticus)

We investigated whether the development of spatial behaviour of the domestic chicken is influenced by light exposure of the embryo, as is known to be the case for some other lateralized visual functions. Ninety-six chicks were incubated in the dark or exposed to light during the final days of incubation. Half of the chicks in each group had the experience of moving behind opaque screens from 10 to 12 days of age. The other half were given transparent screens as a control. Chicks were tested in a detour test and a rotated floor test and their dispersal in groups was observed in larger pens. In the rotated floor test, chicks that had had experience with opaque screens used distal cues significantly more often than chicks that had experience with transparent screens (P = 0.042), regardless of whether they had been exposed to light before hatching or incubated in the dark. There were no significant differences between treatments in the detour test or in the dispersal behaviour. Hence, visual lateralization has no influence on the development of the spatial behaviour that we tested, whereas the occlusion experience is quite specific and results in shifted attention to distal spatial cues.     

Arithmetic in newborn chicks

Newly hatched domestic chicks were reared with five identical objects. On days 3 or 4, chicks underwent free-choice tests in which sets of three and two of the five original objects disappeared (either simultaneously or one by one), each behind one of two opaque identical screens. Chicks spontaneously inspected the screen occluding the larger set (experiment 1). Results were confirmed under conditions controlling for continuous variables (total surface area or contour length; experiment 2). In the third experiment, after the initial disappearance of the two sets (first event, FE), some of the objects were visibly transferred, one by one, from one screen to the other (second event, SE). Thus, computation of a series of subsequent additions or subtractions of elements that appeared and disappeared, one by one, was needed in order to perform the task successfully. Chicks spontaneously chose the screen, hiding the larger number of elements at the end of the SE, irrespective of the directional cues provided by the initial (FE) and final (SE) displacements. Results suggest impressive proto-arithmetic capacities in the young and relatively inexperienced chicks of this precocial species.     

Secondary imprinting in the domestic chick blocked by previous exposure to a live hen

Two experiments were carried out to investigate secondary imprinting in the domestic chick, Gallus gallus. Experiment 1 established that, after chicks with very limited prior visual experience had been exposed to a moving cup during the first 3 days of life, the cup when stationary would suppress distress calling. The main experiment, experiment 2, then examined the effects of various forms of prior experience on the development of this kind of imprinting. Three groups of chicks were exposed on days 1 and 2 to either a live hen (Hen group), a moving object (Windmill group) or the same object when stationary (Control group). On days 4, 5 and 6 all subjects were given training of the kind used in experiment 1; imprinting to the cup was obtained in the Windmill and Control groups, but not in the Hen group. On days 11 and 12 retention tests were given; these showed good retention of primary imprinting, in that the cup was still effective in suppressing distress calling in the Control group and likewise the windmill in the Windmill group, but no effect of secondary imprinting was detected, in that the cup no longer affected the behaviour of the chicks in the Windmill group. These results indicated that primary imprinting with certain stimuli, as in the Hen group, can subsequently exert powerful interference with secondary imprinting and they supported a previous claim that, where secondary imprinting does occur, it is relatively unstable.     

Experimental analysis of systemogenesis process: c-fos gene expression in chicken brain during stimulation of development of a species-specific acceptor of action response

The aim of this study was to localize the areas of the chick brain involved in the development of filial predisposition to follow conspecifics. Expression of the immediate early gene c-fos mRNA was used to map such structures. One-day-old chicks were stimulated (primed) by placing for 90 min into a running wheel in darkness or by exposure to a loud nonspecific sound for 180 min. Brains of a part of these chicks taken 45 min after the beginning of priming were used for c-fos expression study. The remaining chicks were tested 24 hours after priming by simultaneous presentation of a "natural" object (stuffed fowl) and an "artifical" object (rotating red cube). Primed chicks demonstrated significant preference for the natural object as compared to untreated control chicks. In the forebrain of chicks primed both in the running wheel and by acoustic stimulation a significant c-fos expression was found in the medial part of the caudal neostriatum. Priming in the running wheel additionally induced c-fos expression in the lobus parolfactorius, while priming by acoustic stimulation produced high c-fos expression in the archistriatum. Both these areas are known to be involved in filial imprinting. The results suggest that these structures can be also involved in the development of filial predisposition in chicks.     

Development of spatial memory in occlusion-experienced domestic chicks

At around day 11 of life, domestic chicks show a tendency to move out of sight of their mother before returning and regaining social and visual contact. We conducted a series of experiments to investigate the role of this voluntary ‘out-of-sight’ behaviour on the development of spatial memory in young chicks. We compared the behaviour of chicks that were reared in environments that provided opportunities to move out of sight of an imprinting stimulus (occlusion-experienced chicks) with the behaviour of chicks that were given minimal occlusion experience (controls). As in natural conditions, out-of-sight behaviour peaked on day 11. When chicks were released into larger pens at 14 days of age, occlusion-experienced chicks walked more than control chicks, but otherwise showed similar degrees of dispersal. Occlusion-experienced chicks tended to show better (although not significant, P=0.09) retrieval of a visually displaced imprinting stimulus than control chicks. Time spent out of sight in the rearing pens was negatively related to the number of orientation errors in a detour test. Occlusion-experienced chicks also tended to make fewer orientation errors in the first trial (P=0.07) and in subsequent trials (P=0.05). In contrast, experimentally manipulating the amount of time that chicks were out of sight of an imprinting stimulus (by confining the chicks) had no effect on their performance in displacement or detour tests. The results presented here suggest that active experience of occlusion around day 11 improved egocentric orientation towards an out-of-sight goal, supporting the hypothesis that enrichment-induced behavioural changes are dependent on the interaction with objects.     

Visual memory of shapes in quail chicks: discrimination among 2-dimensional objects

Newly hatched chicks spontaneously peck at conspicuous objects, and soon learn to discriminate between edible food particles and inedible objects. To examine whether this discrimination is based on a chick's ability to memorize objects by shape cues, we analyzed the pecking behavior. One- to 3-day old quail chicks (Coturnix japonica) were presented with dry objects of different shapes (ball, disk, triangle and T-shape) of similar size (4 mm) and color (green). Habituation occurred after repeated presentation of any one of these objects (duration: 30 sec; interval: 4 min). When chicks showed significantly more pecks at a novel object (dishabituation), we assumed that chicks had memorized the habituated shapes and distinguished the novel object. Chicks did not show dishabituation between a ball and a disk. On the other hand, chicks discriminated a triangle or T-shape from the memorized image of disk, but did not memorize either triangle or T-shape by its shape. Similarly, chicks did not memorize the size of disks as a reference for subsequent pecking behavior. Chicks proved to have a limited ability to memorize shape and size cues for selective pecking behavior, in strong contrast to their accurate memorization of colors.     

The behaviour of domestic chicks during exposure to two stimuli

Chicks were observed during exposure to red and to blue cylinders. Although chicks apparently become imprinted with both stimuli regardless of their temporal characteristics there were differences in their responses to the two stimuli which depended on the way they were presented. When the two objects appeared in rapid alternation the chicks behaved similarly in the presence of both stimuli, and any differences tended to disappear as exposure progressed. When the two stimuli appeared in separate 1/2-hr blocks there were changes of behaviour at the changeover from one object to the other. The behaviour of chicks during the different sorts of stimulus presentation can be related to their performance on a subsequent discrimination involving the same two stimuli.     

Imprinting on time-structured acoustic stimuli in ducklings

Filial imprinting is a dedicated learning process that lacks explicit reinforcement. The phenomenon itself is narrowly heritably canalized, but its content, the representation of the parental object, reflects the circumstances of the newborn. Imprinting has recently been shown to be even more subtle and complex than previously envisaged, since ducklings and chicks are now known to select and represent for later generalization abstract conceptual properties of the objects they perceive as neonates, including movement pattern, heterogeneity and inter-component relationships of same or different. Here, we investigate day-old Mallard (Anas platyrhynchos) ducklings’ bias towards imprinting on acoustic stimuli made from mallards’ vocalizations as opposed to white noise, whether they imprint on the temporal structure of brief acoustic stimuli of either kind, and whether they generalize timing information across the two sounds. Our data are consistent with a strong innate preference for natural sounds, but do not reliably establish sensitivity to temporal relations. This fits with the view that imprinting includes the establishment of representations of both primary percepts and selective abstract properties of their early perceptual input, meshing together genetically transmitted prior pre-dispositions with active selection and processing of the perceptual input.     

Effects of beta-chlornaltrexamine on separation distress in chicks

Intraventricular B-chlornaltrexamine (2 micrograms) increased distress vocalizations (DVs) in chicks, and reduced the ability of intraventricular morphine (.1-.5 micrograms), to inhibit DVs. Object imprinting was not blocked by central CNA, but systemic naloxone (10 mg/kg) did attenuate imprinting to a green but not a red object.     

雏鸡听觉印记学习

雏鸡听觉印记学习是研究新生个体在早期发育阶段学习与记忆形成的神经机制的良好实验模型.听觉刺激对印记学习有很好的强化作用,作用效果依赖于频率、强度和持续时间等声音特征.从声音的选择、听觉刺激所引起的分子水平和组织水平改变等方面综述雏鸡听觉印记学习的研究进展.     

Activation of cholecystokinin neurons in the dorsal pallium of the telencephalon is indispensable for the acquisition of chick imprinting behavior

Chick imprinting behavior is a good model for the study of learning and memory. Imprinting object is recognized and processed in the visual wulst, and the memory is stored in the intermediate medial mesopallium in the dorsal pallium of the telencephalon. We identified chicken cholecystokinin (CCK)-expressing cells localized in these area. The number of CCK mRNA-positive cells increased in chicks underwent imprinting training, and these cells expressed nuclear Fos immunoreactivity at high frequency in these regions. Most of these CCK-positive cells were glutamatergic and negative for parvalbumin immunoreactivity. Semi-quantitative PCR analysis revealed that the CCK mRNA levels were significantly increased in the trained chicks compared with untrained chicks. In contrast, the increase in CCK- and c-Fos-double-positive cells associated with the training was not observed after closure of the critical period. These results indicate that CCK cells in the dorsal pallium are activated acutely by visual training that can elicit imprinting. In addition, the CCK receptor antagonist significantly suppressed the acquisition of memory. These results suggest that the activation of CCK cells in the visual wulst as well as in the intermediate medial mesopallium by visual stimuli is indispensable for the acquisition of visual imprinting.     

Spontaneous discrimination of possible and impossible objects by newly hatched chicks

Four-month-old infants can integrate local cues provided by two-dimensional pictures and interpret global inconsistencies in structural information to discriminate between possible and impossible objects. This leaves unanswered the issue of the relative contribution of maturation of biologically predisposed mechanisms and of experience with real objects, to the development of this capability. Here we show that, after exposure to objects in which junctions providing cues to global structure were occluded, day-old chicks selectively approach the two-dimensional image that depicted the possible rather than the impossible version of a three-dimensional object, after restoration of the junctions. Even more impressively, completely naive newly hatched chicks showed spontaneous preferences towards approaching two-dimensional depictions of structurally possible rather than impossible objects. These findings suggest that the vertebrate brain can be biologically predisposed towards approaching a two-dimensional image representing a view of a structurally possible three-dimensional object.     

MECHANISMS OF AVIAN IMPRINTING: A REVIEW

Filial imprinting is the process through which early social preferences become restricted to a particular object or class of objects. Evidence is presented showing that filial preferences are formed not only as a result of learning through exposure to an object, but also under the influence of visual and auditory predispositions. The development of these predispositions is dependent upon certain non-specific experience. There is little evidence for an endogenously affected sensitive period for imprinting. It is more likely that the end of sensitivity is a result of the imprinting process itself. Similarly, it is now firmly established that filial and sexual preferences are reversible. Evidence suggests, however, that the first stimulus to which the young animal is exposed may exert a greater influence on filial preferences than subsequent stimuli. The learning process of imprinting is often regarded as being different from conventional associative learning. However, the imprinting object itself can function as a reinforcer. Recent studies have attempted to test predictions from an interpretation of filial imprinting as a form of associative learning. The first results suggest that ‘blocking’ may occur in imprinting, whilst there is no evidence for ‘overshadowing’. Social interactions with siblings and parent(-surrogates) have been shown to affect the formation of filial and sexual preferences. The influence of these interactions is particularly prominent in sexual imprinting, making earlier claims about naive species-specific biases unlikely. Although auditory stimuli play an important role in the formation of social attachments, there is little evidence for auditory imprinting per se. Auditory preferences formed as a result of mere (pre- or postnatal) exposure are relatively weak and short-lasting. Exposure to visual stimuli during auditory training significantly improves auditory learning, possibly through a process of reinforcement. It is becoming increasingly clear that filial and sexual imprinting are two different (although perhaps analogous) processes. Different mechanisms are likely to underlie the two processes, although there is evidence to suggest that the same brain region is involved in recognition of familiar stimuli in both filial and sexual imprinting. There is little evidence for a direct role of hormones in the learning process of imprinting. Androgen metabolism may be a factor constraining the development of a predisposition in the chick. Research into the neural mechanism of filial imprinting in the chick has revealed that a restricted part of the forebrain (IMHV) is likely to be a site of memory storage. Changes in synapse morphology and in the number of NMDA receptors have been found, limited to this region, and correlated with the strength of preference.     

Neurotransmitter Release from the Medial Hyperstriatum Ventrale of the Chick Forebrain Accompanying Filial Imprinting Behavior,Measured by In Vivo Microdialysis

The imprinting behavior of chicks was quantified as a preference score (correct response ratio) achieved in a running wheel apparatus. A total of 249 chicks were exposed to an imprinting stimulus and tested for stimulus-approaching behavior. The chicks were then classified as good learners (imprinted), poor learners (non-imprinted) and a gray-zone group, those were 46%, 31% and 23% of the total chicks respectively. Using the classified chicks, the acetylcholine (ACh) and glutamate releases from the medial hyperstriatum ventrale (MHV) of the chick forebrains were determined by in vivo microdialysis. The non-imprinted chicks were used as yoked controls. Increases of ACh and glutamate released were observed in the imprinted chicks during exposure to the imprinting stimulus, whereas there were no changes in the release of these neurotransmitters in the non-imprinted chicks during the imprinting exposure. These results might be indicated that cholinergic and glutamatergic synapses which are newly formed as functioning synapses with imprinting stimulus in the MHV are involved in the performance of imprinting behavior.     

Getting better all the time: improving preference scores reflect increases in the strength of filial imprinting

In the investigation of the neural mechanisms of filial imprinting, neurochemical measures are often correlated with preference score (PS): approach activity to the training stimulus/total approach in a test. In a previous study, domestic chicks, Gallus gallus domesticus, that had a PS under 65% were classed as 'poor learners' and those with a PS greater than 65% were called 'good learners'. We tested the effects of continued imprinting training in chicks from these two categories. After exposure to an imprinting stimulus for 30 min on day 1 after hatching, preferences were tested and then the chicks were exposed to the same stimulus for either 90 min, 3 h or 4 h on the next day, followed by a second preference test. In all these experiments there was a significant improvement in mean PS in the 'poor learners' between the first and second test, such that these chicks acquired a significant mean preference for the training stimulus. There was no such improvement in chicks that did not receive further training on day 2. When absolute approach was analysed, there was no significant difference between 'poor learners' and 'good learners' at the second test, after 4 h of retraining. Overall, mean preference scores increased with length of training. These results suggest that 'poor learners' are better characterized as 'slow learners', and that their initially low PS is not caused by, for example, a lack of motivation to express a preference. Preference scores reflect the strength of learning during imprinting. Copyright 2000 The Association for the Study of Animal Behaviour.