Src-NADH dehydrogenase subunit 2 complex and recognition memory of imprinting in domestic chicks.

Src is a non-receptor tyrosine kinase participating in a range of neuronal processes, including synaptic plasticity. We have recently shown that the amounts of total Src and its two phosphorylated forms, at tyrosine-416 (activated) and tyrosine-527 (inhibited), undergoes time-dependent, region-specific learning-related changes in the domestic chick forebrain after visual imprinting. These changes occur in the intermediate medial mesopallium (IMM), a site of memory formation for visual imprinting, but not the posterior pole of the nidopallium (PPN), a control brain region not involved in imprinting. Src interacts with mitochondrial genome-coded NADH dehydrogenase subunit 2 (NADH2), a component of mitochondrial respiratory complex I. This interaction occurs at brain excitatory synapses bearing NMDA glutamate receptors. The involvement of Src-NADH2 complexes in learning and memory is not yet explored. We show for the first time that, independently of changes in total Src or total NADH2, NADH2 bound to Src immunoprecipitated from the P2 plasma membrane-mitochondrial fraction: (i) is increased in a learning-related manner in the left IMM 1 h after the end of training; (ii), is decreased in the right IMM in a learning-related way 24 h after training. These changes occurred in the IMM but not the PPN. They are attributable to learning occurring during training rather than a predisposition to learn. Learning-related changes in Src-bound NADH2 are thus time- and region-dependent.

Filial imprinting in domestic chicks; cytoplasmic polyadenylation element binding protein 3, predispositions and learning.

Visual imprinting is a learning process, whereby young animals come to prefer a visual stimulus after exposure to it (training). Available evidence indicates that the intermediate medial mesopallium (IMM) in the domestic chick forebrain is a site of memory formation during visual imprinting. We have found previously that cytoplasmic polyadenylation element binding protein 3 in the P2 plasma membrane-mitochondrial fraction (CPEB3-P2) is upregulated in a learning-dependent way in the left IMM 24 h after training. CPEB3 has two forms, soluble and aggregated. Soluble CPEB3 represses translation; the aggregated form (CPEB3-AF) is amyloid-like and can promote translation. Our previous study did not show which of these two forms is increased after imprinting. We have now resolved this matter by measuring, 24 h after training, CPEB3-P2 and CPEB3-AF in the IMM and a control brain region, the posterior pole of nidopallium (PPN). The methods include imprinting training with a visual stimulus, behavioral measurement of preference, preparation of aggregated CPEB3, western immunoblotting, quantitation of proteins, statistical linear modeling. Only in the left IMM were the level of CPEB3-AF and learning strength correlated, increased CPEB3-AF level reflecting a predisposition to learn readily. CPEB3-P2 level also increased with learning strength in the left IMM, but as a result of learning. No correlations were detected in the right IMM or PPN. We propose two separate systems, both modulating synaptic strength through control of local translation. They are represented by CPEB3-AF (associated with a predisposition to learn) and soluble CPEB3 (associated with learning itself).

Presence of sibling during the learning phase of imprinting affects escape behavior from a new object in chicks.

Imprinting is a crucial learning behavior by the hatchlings of precocious birds. In nature, hatchlings in a group environment imprint on a hen, but the effect of siblings on the imprinting process remains largely unknown. To investigate this issue, we examined how the social context modulated visual imprinting in domestic chicks. One-day-old postnatal chicks in isolation (RS chicks) or with siblings (RD chicks), were first exposed to an imprinting stimulus, and subsequently the responses to the imprinting stimulus as well as a new stimulus were examined and compared. The experiment constituted three types of siblings: a 20-min pre-trained tutor, a 60-min pre-trained tutor, and a naïve chick. A multiple comparison test revealed that the preference score (PS) to the new stimulus of RD chicks trained with a 60-min pre-trained tutor was significantly lower than that of RS chicks. Multiple linear regression analysis revealed that the length of the tutor's pre-training significantly correlated negatively with the PS to the new stimulus, but this variable did not correlate with the PS to the imprinting stimulus. These results revealed that the presence of highly imprinted siblings could enhance the escape response to the new stimulus. We discussed the possible involvement of the chick's medial amygdala in the social aspect of imprinting.

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.

Steps towards a computational ethology: an automatized, interactive setup to investigate filial imprinting and biological predispositions.

Soon after hatching, the young of precocial species, such as domestic chicks or ducklings, learn to recognize their social partner by simply being exposed to it (imprinting process). Even artificial objects or stimuli displayed on monitor screens can effectively trigger filial imprinting, though learning is canalized by spontaneous preferences for animacy signals, such as certain kinds of motion or a face-like appearance. Imprinting is used as a behavioural paradigm for studies on memory formation, early learning and predispositions, as well as number and space cognition, and brain asymmetries. Here, we present an automatized setup to expose and/or test animals for a variety of imprinting experiments. The setup consists of a cage with two high-frequency screens at the opposite ends where stimuli are shown. Provided with a camera covering the whole space of the cage, the behaviour of the animal is recorded continuously. A graphic user interface implemented in Matlab allows a custom configuration of the experimental protocol, that together with Psychtoolbox drives the presentation of images on the screens, with accurate time scheduling and a highly precise framerate. The setup can be implemented into a complete workflow to analyse behaviour in a fully automatized way by combining Matlab (and Psychtoolbox) to control the monitor screens and stimuli, DeepLabCut to track animals' behaviour, Python (and R) to extract data and perform statistical analyses. The automated setup allows neuro-behavioural scientists to perform standardized protocols during their experiments, with faster data collection and analyses, and reproducible results.

Stability and individual variability of social attachment in imprinting.

Filial imprinting has become a model for understanding memory, learning and social behaviour in neonate animals. This mechanism allows the youngs of precocial bird species to learn the characteristics of conspicuous visual stimuli and display affiliative response to them. Although longer exposures to an object produce stronger preferences for it afterwards, this relation is not linear. Sometimes, chicks even prefer to approach novel rather than familiar objects. To date, little is known about how filial preferences develop across time. This study aimed to investigate filial preferences for familiar and novel imprinting objects over time. After hatching, chicks were individually placed in an arena where stimuli were displayed on two opposite screens. Using an automated setup, the duration of exposure and the type of stimuli were manipulated while the time spent at the imprinting stimulus was monitored across 6 days. We showed that prolonged exposure (3 days vs 1 day) to a stimulus produced robust filial imprinting preferences. Interestingly, with a shorter exposure (1 day), animals re-evaluated their filial preferences in functions of their spontaneous preferences and past experiences. Our study suggests that predispositions influence learning when the imprinting memories are not fully consolidated, driving animal preferences toward more predisposed stimuli.

Sensitive periods for social development: Interactions between predisposed and learned mechanisms.

We analysed research that makes use of precocial species as animal models to describe the interaction of predisposed mechanisms and environmental factors in early learning, in particular for the development of social cognition. We also highlight the role of sensitive periods in this interaction, focusing on domestic chicks as one of the main animal models for this field. In the first section of the review, we focus on the emergence of early predispositions to attend to social partners. These attentional biases appear before any learning experience about social stimuli. However, non-specific experiences occurring during sensitive periods of the early post-natal life determine the emergence of these predisposed mechanisms for the detection of social partners. Social predispositions have an important role for the development learning-based social cognitive functions, showing the interdependence of predisposed and learned mechanisms in shaping social development. In the second part of the review we concentrate on the reciprocal interactions between filial imprinting and spontaneous (not learned) social predispositions. Reciprocal influences between these two sets of mechanisms ensure that, in the natural environment, filial imprinting will target appropriate social objects. Neural and physiological mechanisms regulating the sensitive periods for the emergence of social predispositions and for filial imprinting learning are also described.

The cow-calf relationship: from maternal responsiveness to the maternal bond and the possibilities for fostering.

The relationship between the cow and calf develops over time after birth. The behavioural mechanisms underlying its development are important and comparisons with other species may increase our understanding. In nature the cow will separate herself from the herd to give birth and then the cow-calf relationship will develop with the ability to recognise each other. While twinning levels are low in cows, they do rear their twin calves. If the calf is lost at or after birth the cow can be responsive towards other calves and in specific circumstances the cow can develop a maternal bond with an alien calf, i.e. foster. In this Research Reflection a distinction is made between the development of, on the one hand, maternal responsiveness (the tendency of the cow to care for a calf which occurs before birth) and, on the other hand, the development of the maternal-filial bond or relationship which is reciprocal, occurs after birth and is characterised by the ability to discriminate the mother's own calf from alien calves. These processes can overlap and the relationship between cow and calf in this 'hider' species is more plastic than in some other mammals. For example, a cow might form an attachment with an alien calf before she gives birth. After the cow has given birth the loss of her own calf may result in the state of maternal responsiveness being maintained, such that developing a maternal bond with one or several appropriate alien calves is possible. Viable fostering techniques are possible. If a maternal relationship to the mother's own calf has developed then fostering will be more difficult. If the cow's relationship with her own calf is not exclusive, and she is in a state of maternal responsiveness then fostering of calves of an appropriate age and status can be achieved.

What can a worm learn in a bacteria-rich habitat?

With a nervous system that has only a few hundred neurons, Caenorhabditis elegans was initially not regarded as a model for studies on learning. However, the collective effort of the C. elegans field in the past several decades has shown that the worm displays plasticity in its behavioral response to a wide range of sensory cues in the environment. As a bacteria-feeding worm, C. elegans is highly adaptive to the bacteria enriched in its habitat, especially those that are pathogenic and pose a threat to survival. It uses several common forms of behavioral plasticity that last for different amounts of time, including imprinting and adult-stage associative learning, to modulate its interactions with pathogenic bacteria. Probing the molecular, cellular and circuit mechanisms underlying these forms of experience-dependent plasticity has identified signaling pathways and regulatory insights that are conserved in more complex animals.

The effect of pre-training of abstract stimuli to exert control over tact and mand responses on stimulus equivalence class formation

Recent studies show that the formation of stimulus equivalence classes can be enhanced by meaningful stimuli. The purpose of this study was to investigate whether acquired meaningfulness, through pre-training of meaningless stimuli to exert control over tact or mand responses, would enhance stimulus equivalence class formation. Participants were eighteen university students aging 18-over 40 that were alternately assigned to either the Tact (n= 9) or the Mand Group (n= 9). Participants in all groups received a card sorting test following either a tact or mand pre-training. They then received training and testing procedures to establish three 3-node 5-member equivalence classes under the simultaneous protocol. After serialized training of AB, BC, CD, and DE relations, all probes used to assess the emergence of symmetrical, transitive, and equivalence relations were presented for two test blocks. Lastly, the card sorting procedure was repeated. Results showed that the pre-training of abstract stimuli to exert control over tact and mand responses did not produce equivalence class enhancement. Future studies should further investigate the relationship between the verbal properties of meaningful stimuli and the formation of stimulus equivalence classes

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Natal imprinting to the Earth's magnetic field in a pelagic seabird.

In migratory animals for whom post-natal care is limited, it is essential that there are inherited mechanisms whereby an individual can navigate-first, to the terminus of their migration, and second, back to a suitable breeding site. In birds, empirical evidence suggests that orientation on first migration is controlled by an inherited navigational vector, a direction and a distance in which to move (the "clock and compass" model) [1-5]. The mechanism and information that underlie the return to the natal breeding site are, however, almost entirely unknown. A potential solution to this problem would be for an animal to learn the values for spatially and temporally stable gradient cues that specifically indicate the location of the natal site [6-16]. One potential cue for latitude is magnetic inclination. Here, we use ringing recoveries made over the last 80 years to investigate whether magnetic inclination might be used as a navigational cue to control the latitude of recruitment in a trans-global migrant, the Manx shearwater (Puffinus puffinus). We find that small changes in inclination between when a bird fledges and when it returns from first migration correlate with probabilistic changes in latitude at recruitment, in doing so quantitatively fulfilling a priori predictions as to the magnitude and direction of latitudinal shift. This, we believe, suggests that (1) natal magnetic inclination is learnt prior to fledging and (2) is used to provide latitudinal information when making the first return trip from the wintering grounds.

Sexual imprinting overrides order effects during sampling of prospective mates.

Through crossfostering experiments between two subspecies of mice, Moreira et al. show that females normally undergo sexual imprinting early in life. When fostered by individuals from another subspecies, they tend to prefer males from the sub-species they first encounter, suggesting sexual imprinting normally over-rides this inclination.

Chicken cognin interactome and the memory of filial imprinting.

Visual imprinting is a learning process whereby young animals come to prefer a visual stimulus after exposure to it (training). The intermediate medial mesopallium in the domestic chick forebrain is critical for visual imprinting and contributes to molecular regulation of memory formation. Criteria used to infer that a change following training is learning-related have been formulated and published. Cognin (protein disulphide isomerase) is one of several identified plasma membrane and mitochondrial proteins that are upregulated in a learning-related way 24 hours after training. Since virtually nothing is known about the cognin interactome, we have used immunoaffinity chromatography and mass spectrometry to identify proteins that interact with cognin in the cytoplasmic and plasma membrane-mitochondrial fractions. As the learning-related upregulation of cognin has been shown to occur in the plasma membrane-mitochondrial fraction and not in the cytoplasmic fraction, we studied the effect of training on three cognin-interacting partners in the plasma membrane-mitochondrial fraction: the b5 subunit of mitochondrial ATP synthase and the alpha-2 and alpha-3 subunits of sodium-potassium ATPase. Learning-related upregulation was found in the left intermediate medial mesopallium 24 hours after training for the b5 subunit of mitochondrial ATP synthase and the alpha-2 subunit of sodium-potassium ATPase. The hemispheric asymmetry revealed here is consistent with the predominance of many other learning-related effects in the left intermediate medial mesopallium. The alpha-2 subunit of sodium-potassium ATPase is mainly expressed in astrocytes, supporting a role for these glial cells in memory.

Cross-continental test of natal philopatry and habitat-imprinting hypotheses to explain host specificity in an obligate brood parasite.

Several hypotheses have been proposed to explain the mechanisms responsible for maintenance of host-specific gentes in the common cuckoo (Cuculus canorus). Some of them expect that when adult cuckoos return to lay their eggs to their natal site (natal philopatry hypothesis) or habitat in which they were reared (habitat-imprinting hypothesis), there is a higher probability of finding nests of the host species by which they were reared. Since published evidence is ambiguous, we here evaluate the natal philopatry and habitat-imprinting hypotheses using information on habitat homogeneity and cross-continental long-term ringing data. We found no evidence for the natal philopatry hypothesis-instead of returning to their natal site, juvenile cuckoos exhibited longer dispersal movements than adults, and the difference was even larger in comparison with a wide array of cuckoo host species. On the contrary, we found support for the habitat-imprinting hypothesis-juvenile cuckoos followed similar levels of natal habitat homogeneity at 5- and 25-km scale when returning to breed in the next years. Our results suggest that preference for the particular habitat structures may help cuckoos to find appropriate hosts.

Behavioral evidence for geomagnetic imprinting and transgenerational inheritance in fruit flies.

Certain long-distance migratory animals, such as salmon and sea turtles, are thought to imprint on the magnetic field of their natal area and to use this information to help them return as adults. Despite a growing body of indirect support for such imprinting, direct experimental evidence thereof remains elusive. Here, using the fruit fly as a magnetoreceptive model organism, we demonstrate that exposure to a specific geographic magnetic field during a critical period of early development affected responses to a matching magnetic field gradient later in life. Specifically, hungry flies that had imprinted on a specific magnetic field from 1 of 3 widely separated geographic locations responded to the imprinted field, but not other magnetic fields, by moving downward, a geotactic behavior associated with foraging. This same behavior occurred spontaneously in the progeny of the next generation: female progeny moved downward in response to the field on which their parents had imprinted, whereas male progeny did so only in the presence of these females. These results represent experimental evidence that organisms can learn and remember a magnetic field to which they were exposed during a critical period of development. Although the function of the behavior is not known, one possibility is that imprinting on the magnetic field of a natal area assists flies and their offspring in recognizing locations likely to be favorable for foraging and reproduction.

Combined predisposed preferences for colour and biological motion make robust development of social attachment through imprinting.

To study how predisposed preferences shape the formation of social attachment through imprinting, newly hatched domestic chicks (Gallus gallus domesticus) were simultaneously exposed to two animations composed of comparable light points in different colours (red and yellow), one for a walking motion and another for a linear motion. When a walking animation in red was combined with a linear one in yellow, chicks formed a learned preference for the former that represented biological motion (BM). When the motion-colour association was swapped, chicks failed to form a preference for a walking in yellow, indicating a bias to a specific association of motion and colour. Accordingly, experiments using realistic walking chicken videos revealed a preference for a red video over a yellow one, when the whole body or the head was coloured. On the other hand, when the BM preference had been pre-induced using an artefact moving rigidly (non-BM), a clear preference for a yellow walking animation emerged after training by the swapped association. Even if the first-seen moving object was a nonbiological artefact such as the toy, the visual experience would induce a predisposed BM preference, making chicks selectively memorize the object with natural features. Imprinting causes a rapid inflow of thyroid hormone in the telencephalon leading to the induction of the BM preference, which would make the robust formation of social attachment selectively to the BM-associated object such as the mother hen.

Character cues modulate the affordance effects during danger warning

It has been demonstrated that perception of objects automatically evokes potential actions to interact with those objects; this is termed as affordance. The present study investigated how the corresponding affordance effect of graspable objects was modulated by the cue about risk levels of object. Participants were presented with pictures of dangerous graspable objects or neutral graspable objects. The participants were required to perform an upright/upside down discrimination task by pressing different keys. Results showed that both the affordance effects of dangerous object and neutral object in children were enhanced when a cue preceded the object, t(35) = 3.83, p < .01, Cohen's d = 1.29. These results indicate that the prompt of risk level can improve individual's appropriate manipulation to the object

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Ducklings imprint on chromatic heterogeneity.

Avian filial imprinting is a rapid form of learning occurring just after hatching in precocial bird species. The acquired imprint on either or both parents goes on to affect the young bird's survival and social behaviour later in life (Bateson in Biol Rev 41:177-217, 1966). The imprinting mechanism is specialized but flexible, and causes the hatchling to develop high-fidelity recognition and attraction to any moving stimulus of suitable size seen during a predefined sensitive period. It has been observed (Martinho and Kacelnik in Science 353:286-288, 2016; Versace et al. in Anim Cogn 20:521-529, 2017) that in addition to visual and acoustic sensory inputs, imprinting may incorporate informational rules or abstract concepts. Here we report a study of mallard ducklings (Anas platyrhynchos domesticus) undergoing imprinting on the chromatic heterogeneity of stimuli, with a focus on how this may be transferred to novel objects. Ducklings were exposed to a series of chromatically heterogeneous or homogeneous stimuli and tested for preference between two novel stimuli, one heterogeneous and the other homogeneous. Exposure to heterogeneity significantly enhanced preference for novel heterogeneous stimuli, relative to ducklings exposed to homogeneous stimuli or unexposed controls. These findings support the view that imprinting does not rely solely on exemplars, or snapshot-like representations of visual input, but that instead young precocial animals form complex multidimensional representations of the target object, involving abstract properties, either at the time of learning, or later, through generalization from the learnt exemplars.

Behavioural and neuronal basis of olfactory imprinting and kin recognition in larval fish.

Imprinting is a specific form of long-term memory of a cue acquired during a sensitive phase of development. To ensure that organisms memorize the right cue, the learning process must happen during a specific short time period, mostly soon after hatching, which should end before irrelevant or misleading signals are encountered. A well-known case of olfactory imprinting in the aquatic environment is that of the anadromous Atlantic and Pacific salmon, which prefer the olfactory cues of natal rivers to which they return after migrating several years in the open ocean. Recent research has shown that olfactory imprinting and olfactory guided navigation in the marine realm are far more common than previously assumed. Here, we present evidence for the involvement of olfactory imprinting in the navigation behaviour of coral reef fish, which prefer their home reef odour over that of other reefs. Two main olfactory imprinting processes can be differentiated: (1) imprinting on environmental cues and (2) imprinting on chemical compounds released by kin, which is based on genetic relatedness among conspecifics. While the first process allows for plasticity, so that organisms can imprint on a variety of chemical signals, the latter seems to be restricted to specific genetically determined kin signals. We focus on the second, elucidating the behavioural and neuronal basis of the imprinting process on kin cues using larval zebrafish (Danio rerio) as a model. Our data suggest that the process of imprinting is not confined to the central nervous system but also triggers some changes in the olfactory epithelium.