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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.

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.

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.

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.

Filial imprinting has become a model for understanding memory, learning and social behaviour in neonate animals. This fast attachment mechanism allows the young of precocial bird species to learn the characteristics of conspicuous visual stimuli and display affiliative response to them. Although more prolonged exposure to an object produces a stronger preference for it afterwards, this relation is not linear. Chicks can even prefer to approach novel rather than familiar objects at some stages of imprinting. The time course and stability of imprinting has just started to be investigated. To date, little is known about how filial preferences develop across time, due to the challenges in assessing individual performance. This study aimed to investigate filial preferences for familiar and novel imprinting objects over time. We have used an automated setup to track the behaviour of chicks continuously for subsequent days. After hatching, chicks were individually placed in an arena where stimuli were displayed on two opposite screens. The duration of exposure and the type of stimuli were manipulated while the time spent at the imprinting stimulus was monitored across six 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 innate 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.

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.

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.

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, 2, 3, 4, 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, 7, 8, 9, 10, 11, 12, 13, 14, 15, 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.

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.

With a nervous system that has about a billion times fewer neurons than the human brain, C. 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.

Visual imprinting is a learning process whereby young animals come to prefer a visual stimulus after exposure to it (training). The intermediate medial mesopallium (IMM) in the domestic chick forebrain is critical for visual imprinting and contributes to molecular regulation of memory formation. We investigated the role of micro-RNAs (miRNAs) in such regulation. Twenty-four hours after training, miRNA spectra in the left IMM were compared between chicks with high preference scores (strong memory for imprinting stimulus), and chicks with low preference scores (weak memory for imprinting stimulus). Using criteria of significance and expression level, we chose gga-miR-130b-3p for further study and found that down-regulation correlated with learning strength. No effect was detected in posterior nidopallium, a region not involved in imprinting. We studied two targets of gga-miR-130b-3p, cytoplasmic polyadenylation element binding proteins 1 (CPEB-1) and 3 (CPEB-3), in two subcellular fractions (P2 membrane-mitochondrial and cytoplasmic) of IMM and posterior nidopallium. Only in the left IMM was a learning-related effect observed, in membrane CPEB-3. Variances from the regression with preference score and untrained chicks suggest that, in the IMM, gga-miR-130b-3p level reflects a predisposition, i.e. capacity to learn, whereas P2 membrane-mitochondrial CPEB-3 is up-regulated in a learning-specific way.

Filial imprinting leads to the formation of social attachment if training is performed during a brief sensitive period after hatching. We found that thyroid hormone (3,5,3′-triiodothyronine, T3) acts as a critical determining factor of the sensitive period in domestic chicks. Imprinting upregulates gene expression of the converting enzyme (Dio2, type 2 iodothyronine deiodinase) in the telencephalon, leading to increased brain T3 content. If systemically applied, T3 facilitates imprinting in aged chicks even after the sensitive period is over. Imprinting is also associated with the rapid development of visual perception. Exposure to motion pictures induces a predisposed preference to Johansson’s biological motion (BM), and those individuals with higher BM preference are more easily imprinted. Here, we examined whether Dio2 expression is also linked with BM predisposition. Chicks were trained by a rotating red block, and tested for imprinting (experiment 1) and BM preference (experiment 2). To examine the time courses of behavioural and physiological processes, Dio2 expression in telencephalon was compared among three groups: naive control chicks, and chicks trained for a short (0.5 h) or long period (2 h). In experiment 1, higher Dio2 expression appeared in the 2-h group than in the 0.5-h/control groups, but it was not correlated with the individual imprinting score. In experiment 2, a significant positive correlation appeared between Dio2 expression and BM preference in 2-h-trained chicks. Memory priming by T3 is therefore functionally linked to BM preference induction, leading to successful imprinting to natural objects even when they are initially exposed to artificial objects.

Filial imprinting is the behavior observed in chicks during the sensitive or critical period of the first 2–3 days after hatching; however, after this period they cannot be imprinted when raised in darkness. Our previous study showed that temporal augmentation of the endogenous thyroid hormone 3,5,3′-triiodothyronine (T3) in the telencephalon, by imprinting training, starts the sensitive period just after hatching. Intravenous injection of T3 enables imprinting of chicks on days 4 or 6 post-hatching, even when the sensitive period has ended. However, the molecular mechanism of how T3 acts as a determinant of the sensitive period is unknown. Here, we show that Wnt-2b mRNA level is increased in the T3-injected telencephalon of 4-day old chicks. Pharmacological inhibition of Wnt signaling in the intermediate hyperpallium apicale (IMHA), which is the caudal area of the telencephalon, blocked the recovery of the sensitive period following T3 injection. In addition, injection of recombinant Wnt-2b protein into the IMHA helped chicks recover the sensitive period without the injection of T3. Lastly, we showed Wnt signaling to be involved in imprinting via the IMHA region on day 1 during the sensitive period. These results indicate that Wnt signaling plays a critical role in the opening of the sensitive period downstream of T3.

It is generally accepted that information about some of the odorants in the natal streams of anadromous Pacific salmon (Genus Oncorhynchus) is imprinted during their seaward migration, and that anadromous Pacific salmon use olfaction to identify their natal streams during the homeward migration. However, little is known about the molecular mechanisms of the various pre-synaptic functions that are important for olfactory imprinting and memory retrieval in the salmon brain. Synaptosome-associated protein-25 (SNAP-25) mediates pre-synaptic vesicle exocytosis and regulates synaptic transmission and neuronal plasticity. Despite the importance of synaptic plasticity for memorization, the expression of SNAP-25 in the salmon brain is not well understood. In this study, snap25 expression was detected in chum salmon (O. keta) brains using molecular biological techniques. Two cDNAs encoding salmon SNAP-25 were isolated and sequenced (SNAP-25a and SNAP-25b). These cDNAs encoded proteins with 204 amino acid residues, which showed marked homology with each other (97%). The protein and nucleotide sequences demonstrated a high level of homology between salmon SNAP-25s and those of other teleost species. By quantitative PCR, the expression of snap25a and snap25b was detected in all regions of the salmon brain, especially in the telencephalon. The expression levels of snap25a in the olfactory blub were higher during seaward migration than in upriver and post-upriver migrations, reflecting synaptogenesis in the olfactory nervous system, and snap25b in the telencephalon was increased during upriver period. Our results indicated that snap25s gene is involved in synaptic plasticity for olfactory imprinting and/or olfactory memory retrieval in Pacific salmon.

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.

Feeding imprinting, considered a survival-enabling process, is not well understood. Infants born very preterm, who first feed passively, are an effective model for studying feeding imprinting. Retrospective analysis of neonatal intensive care unit (NICU) records of 255 infants (Mgestational age = 29.98 ± 1.64) enabled exploring the notion that direct breastfeeding (DBF) during NICU stay leads to consumption of more mother's milk and earlier NICU discharge. Results showed that DBF before the first bottle feeding is related to shorter transition into oral feeding, a younger age of full oral feeding accomplishment and earlier discharge. Furthermore, the number of DBF meals before first bottle feeding predicts more maternal milk consumption and improved NICU outcomes. Improved performance in response to initial exposure to DBF at the age of budding feeding abilities supports a feeding imprinting hypothesis.

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.

International audience; Regular visual presence of humans is known to reduce chickens' human-generated stress responses. Here we questioned whether, more than mere visual presence, human behaviour affects laying hen behaviour and subsequently their offspring's behaviour. We hypothesized that human behaviour triggers maternal effects via variations in yolk hormone levels. For five consecutive weeks, two groups of hens were exposed to the same durations of human presence (30 min twice a day, five days a week) but the behaviour of the human differed between groups. The first group (H+) was exposed to predictable arrival of the experimenter, slow movements combined with static presence, stroking during handling and human voice. Whereas the second group of hens (H-) was exposed to unpredictable arrival of the experimenter which remained silent, in motion, and did not provide stroking during handling. At the end of the treatment, we evaluated egg quality and offspring behaviour. We found that avoidance of the experimenter by H+ hens but not by H– hens decreased significantly. Fertility rates and concentrations of yolk progesterone and estradiol in H+ hens' eggs were higher than in H– hens' eggs. Fear of humans, neophobia or the capacity to solve a detour task did not differ significantly between H+ and H– chicks. Social discrimination tests showed that H+ chicks but not H– chicks typically preferred a familiar conspecific to a stranger. These results show that, with the same duration in the presence of the birds, humans through their behaviour engender variations in fertility rates, yolk hormone levels and transgenerational effects on social skills. Rarely explored, our data suggest that maternal effects influence filial imprinting. These data have broad implications for laboratory, commercial systems and conservatory programs where the inevitable presence of humans could trigger maternal effects on offspring phenotype.

Species from phylogenetically distant animal groups, such as birds and primates including humans, share early experience-independent social predispositions that cause offspring, soon after birth, to attend to and learn about conspecifics. One example of this phenomenon is provided by the behaviour of newly-hatched visually-naïve domestic chicks that preferentially approach a stimulus resembling a conspecific (a stuffed fowl) rather than a less naturalistic object (a scrambled version of the stuffed fowl). However, the neuronal mechanisms underlying this behaviour are mostly unknown. Here we analysed chicks' brain activity with immunohistochemical detection of the transcription factor c-Fos. In a spontaneous choice test we confirmed a significant preference for approaching the stuffed fowl over a texture fowl (a fowl that was cut in small pieces attached to the sides of a box in scrambled order). Comparison of brain activation of a subgroup of chicks that approached either one or the other stimulus revealed differential activation in an area relevant for imprinting (IMM, intermediate medial mesopallium), suggesting that a different level of plasticity is associated with approach to naturalistic and artificial stimuli. c-Fos immunoreactive neurons were present also in the intermediate layers of the optic tectum (a plausible candidate for processing early social predispositions) showing a trend similar to the results for the IMM.

Many species of invasive plants are spreading out rapidly in Europe. The common milkweed occupies increasingly more area. Being poisonous, most animals will not graze on it however rabbits would be an effective organism for the biological control of milkweed. Rabbit kittens can learn the maternal diet in various ways. They prefer aromatic foods which their mother had eaten during pregnancy or lactation period, -even if it is poisonous- but they can also learn the maternal diet from the fecal pellets deposited by the mother into the nest during the nursing events. The present study was aimed to investigate if rabbit kittens can learn that the common milkweed is a potential food also. In the first 10days of their lives kits got fecal pellets originating from individuals having fed on common milkweed previously. When weaned on day 28 postpartum, these pups preferred the milkweed in the 3-way food choice test, opposite to the control group. Most surprisingly in a second experiment it was also shown that the common milkweed was also preferred by the kittens if their mother ate it not during, but one month before pregnancy.

Building new networks in the brain Donald Hebb's hypothesis that coactivation of neurons leads to the formation of ensembles of neurons has inspired neuroscientists for decades. The experimental creation of such ensembles has been technically challenging. Using two-photon optogenetic stimulation with single-cell resolution, Carrillo-Reid et al. discovered that recurrent activation of a group of neurons creates an ensemble that is imprinted in the brain circuitry. Activation of a single neuron can lead to recall of the entire ensemble in a phenomenon called pattern completion. The artificial ensemble persists over days and can be reactivated at later time points without interfering with endogenous circuitry. Science , this issue p. 691

Memories formed early in life are particularly stable and influential, representing privileged experiences that shape enduring behaviors. Here we show that exposing newly-hatched C. elegans to pathogenic bacteria results in persistent aversion to those bacterial odors, whereas adult exposure generates only transient aversive memory. Long-lasting imprinted aversion has a critical period in the first larval stage, and is specific to the experienced pathogen. Distinct groups of neurons are required during formation (AIB, RIM) and retrieval (AIY, RIA) of the imprinted memory. RIM synthesizes the neuromodulator tyramine, which is required in the L1 stage for learning. AIY memory retrieval neurons sense tyramine via the SER-2 receptor, which is essential for imprinted but not for adult-learned aversion. Odor responses in several neurons, most notably RIA, are altered in imprinted animals. These findings provide insight into neuronal substrates of different forms of memory, and lay a foundation for further understanding of early learning.

Global biodiversity is being degraded at an unprecedented rate, so it is important to preserve the potential for future speciation. Providing for the future requires understanding speciation as a contemporary ecological process. Phylogenetically young adaptive radiations are a good choice for detailed study because diversification is ongoing. A key question is how incipient species become reproductively isolated from each other. Barriers to gene exchange have been investigated experimentally in the laboratory and in the field, but little information exists from the quantitative study of mating patterns in nature. Although the degree to which genetic variation underlying mate-preference learning is unknown, we provide evidence that two species of Darwin’s finches imprint on morphological cues of their parents and mate assortatively. Statistical evidence of presumed imprinting is stronger for sons than for daughters and is stronger for imprinting on fathers than on mothers. In combination, morphology and species-specific song learned from the father constitute a barrier to interbreeding. The barrier becomes stronger the more the species diverge morphologically and ecologically. It occasionally breaks down, and the species hybridize. Hybridization is most likely to happen when species are similar to each other in adaptive morphological traits, e.g., body size and beak size and shape. Hybridization can lead to the formation of a new species reproductively isolated from the parental species as a result of sexual imprinting. Conservation of sufficiently diverse natural habitat is needed to sustain a large sample of extant biota and preserve the potential for future speciation.

Dysregulation of the mechanistic target of rapamycin complex 1 (mTORC1) signaling leads to memory deficits and abnormal social behaviors in adults. However, whether mTORC1 is involved in critical periods of early learning remains largely unexplored. Our study addressed this question by investigating imprinting, a form of learning constrained to a sensitive period that supports filial attachment, in newborn chickens. Imprinting to virtual objects and sounds was assessed after acute manipulations of mTORC1. To further understand the role of mTORC1 during the critical period, structural plasticity was analyzed using DiOlistic labeling of dendritic spines. We found that mTORC1 is required for the emergence of experience-dependent preferences and structural plasticity within brain regions controlling behavior. Furthermore, upon critical period closure, pharmacological activation of the AKT/mTORC1 pathway was sufficient to rescue imprinting across sensory modalities. Thus, our results uncover a novel role of mTORC1 in the formation of imprinted memories and experience-dependent reorganization of neural circuits during a critical period.

Juvenile Oncorhynchus spp. can memorise their natal stream during downstream migration; juveniles migrate to feed during their growth phase and then they migrate long distances from their feeding habitat to their natal stream to reproduce as adults. Two different sensory mechanisms, olfaction and navigation, are involved in the imprinting and homing processes during short-distance migration within the natal stream and long-distance migration in open water, respectively. Here, olfactory functions are reviewed from both neurophysiological studies on the olfactory discrimination ability of natal stream odours and neuroendocrinological studies on the hormonal controlling mechanisms of olfactory memory formation and retrieval in the brain. These studies revealed that the long-term stability of dissolved free amino-acid composition in the natal stream is crucial for olfactory imprinting and homing. Additionally, the brain-pituitary-thyroid and brain-pituitary-gonadal hormones play important roles in olfactory memory formation and retrieval, respectively. Navigation functions were reviewed from physiological biotelemetry techniques with sensory interference experiments during the homing migration of anadromous and lacustrine Oncorhynchus spp. The experiments demonstrated that Oncorhynchus spp. used compass navigation mechanisms in the open water. These findings are discussed in relation to the sensory mechanisms involved in natal stream imprinting and homing in Oncorhynchus spp.

Visual imprinting is a learning process through which young, visually naive animals come to recognize a visual stimulus by being exposed to it (training) and subsequently approach the stimulus in preference to others. A large body of evidence indicates that a restricted part of the forebrain, the intermediate medial mesopallium (IMM), is a memory region for visual imprinting in the domestic chick. Previous studies have shown learning-related up-regulation of several mitochondrial proteins in the IMM 24 h after training. Learning-related increases in transcription factors involved in mitochondrial biogenesis were found without significant change in mitochondrial DNA copy number, but the issue of whether mitochondrial fusion or fission processes change with learning was unresolved. The present study enquired whether proteins involved in mitochondrial fusion and fission contribute to memory following imprinting. Tissue was sampled from the left and right IMM, and the left and right posterior pole of the nidopallium (a control brain region not involved in imprinting). The amounts of the following proteins were measured by Western immunoblotting 24 h after training: mitochondrial mitofusin-1 (MTF-1, as indicator of mitochondrial fusion), membrane dynamin-related protein-1 (DRP-1, as indicator of mitochondrial fission) and cytoplasmic DRP-1. Learning-related increases in MTF-1 and DRP-1 were observed bilaterally in the IMM, but not in either side of the posterior pole of the nidopallium. Cytoplasmic DRP-1 was not changed significantly in any region studied. The results implicate increased, balanced levels of mitochondrial fusion and fission in memory formation up to 24 h after training.Supplementary Video Abstract (Supplemental digital content 1, http://links.lww.com/WNR/A446).

Filial imprinting in precocial birds is a useful model for studying early learning and cognitive development, as it is characterized by a well-defined sensitive or critical period. We recently showed that the thyroid hormone 3,5,3′-triiodothyronine (T3) determines the onset of the sensitive period. Moreover, exogenous injection of T3 into the intermediate medial mesopallium (IMM) region (analogous to the associative cortex in mammals) enables imprinting even on post-hatch day 4 or 6 when the sensitive period has been terminated. However, the neural mechanisms downstream from T3 action in the IMM region remain elusive. Here, we analyzed the functional involvement of the intermediate hyperpallium apicale (IMHA) in T3 action. Bilateral excitotoxic ablation of the IMHA prevented imprinting in newly hatched chicks, and also suppressed the recovery of the sensitive period by systemic intra-venous or localized intra-IMM injection of T3 in day-4 chicks. In contrast to the effect in the IMM, direct injection of T3 into the IMHA did not enable imprinting in day-4 chicks. Moreover, bilateral ablation of IMHA after imprinting training impaired recall. These results suggest that the IMHA is critical for memory acquisition downstream following T3 action in the IMM and further, that it receives and retains information stored in the IMM for recall. Furthermore, both an avian adeno-associated viral construct containing an anterograde tracer (wheat-germ agglutinin) and a retrograde tracer (cholera toxin subunit B) revealed neural connections from the IMM to the IMHA. Taken together, our findings suggest that hierarchical processes from the primary area (IMM) to the secondary area (IMHA) are required for imprinting.

UNLABELLED Instinctive behaviours have evolved favouring the mother-infant dyad based on fundamental processes of neurological development, including oral tactile imprinting and latchment. Latchment is the first stage of emotional development based on the successful achievement of biological imprinting. The mechanisms underpinning imprinting are identified and the evolutionary benefits discussed. CONCLUSION It is proposed that the oral tactile imprint to the breast is a keystone for optimal latchment and breastfeeding, promoting evolutionary success.

Johnson and Morton (1991. Biology and Cognitive Development: The Case of Face Recognition. Blackwell, Oxford) used Gabriel Horn's work on the filial imprinting model to inspire a two-process theory of the development of face processing in humans. In this paper we review evidence accrued over the past two decades from infants and adults, and from other primates, that informs this two-process model. While work with newborns and infants has been broadly consistent with predictions from the model, further refinements and questions have been raised. With regard to adults, we discuss more recent evidence on the extension of the model to eye contact detection, and to subcortical face processing, reviewing functional imaging and patient studies. We conclude with discussion of outstanding caveats and future directions of research in this field.

Amongst an array of stimuli from countless species, animals must recognize salient signals, including those of their own species. In songbirds, behavioral tests have demonstrated that preferences for conspecific male songs are determined by both preexisting biases and social experience with a male 'tutor' during the sensitive period for learning. Although immediate early gene expression (e.g. ZENK) and electrophysiological experiments generally find greater neural responses for conspecific songs, it remains unclear whether distinct mechanisms, such as sensory gating, are engaged to filter out irrelevant heterospecific songs. Here we compare the transcriptomic profiles, via RNA-seq, of non-singing females of a songbird, the zebra finch (Taeniopygia guttata), by focusing on the auditory forebrain, a region known to be critical in the processing of conspecific vs. heterospecific songs. Gene expression profiles demonstrate that different neural mechanisms are involved in the processing of conspecific versus heterospecific Bengalese finch (Lonchura striata) songs. In particular, one gene known to mediate sensory gating, the alpha 3 subunit member of nicotinic cholinergic receptors (CHRNA3), was significantly downregulated in response to hearing Bengalese finch song, but not when young females were tutored by a Bengalese male during early development. Overall, our results confirm previous behavioral and physiological studies, such that heterospecific-tutored individuals processed both conspecific and tutor songs similarly. Using transcriptomic profiling of peripheral blood samples, we also demonstrate the methodological potential of non-terminal sampling to identify transcriptomic biomarkers for conspecific auditory recognition. These results show how experience and inherited preferences facilitate the neural processing of salient songs by female songbirds.

Sexual isolation, a reproductive barrier, can prevent interbreeding between diverging populations or species. Sexual isolation can have a clear genetic basis; however, it may also result from learned mate preferences that form via sexual imprinting. Here, we demonstrate that two sympatric species of mice-the white-footed mouse (Peromyscus leucopus) and its sister species, the cotton mouse (P. gossypinus)-hybridize only rarely in the wild despite co-occurrence in the same habitat and lack of any measurable intrinsic postzygotic barriers in laboratory crosses. We present evidence that strong conspecific mating preferences in each species result in significant sexual isolation. We find that these preferences are learned in at least one species: P. gossypinus sexually imprints on its parents, but in P. leucopus, additional factors influence mating preferences. Our study demonstrates that sexual imprinting contributes to reproductive isolation that reduces hybridization between otherwise interfertile species, supporting the role for learning in mammalian speciation.

Zebrafish larvae imprint on visual and olfactory cues of their kin on day 5 and 6 postfertilization, respectively. Only imprinted (but not non-imprinted) larvae show strongly activated crypt (and some microvillous) cells demonstrated by pERK levels after subsequent exposure to kin odor. Here, we investigate the olfactory bulb of zebrafish larvae for activated neurons located at the sole glomerulus mdG2 which receives crypt cell input. Imprinted larvae show a significantly increased activation of olfactory bulb cells compared to non-imprinted larvae after exposure to kin odor. Surprisingly, pERK activated Orthopedia-positive cell numbers in the intermediate ventral telencephalic nucleus were higher in non-imprinted, kin odor stimulated larvae compared to control and to kin-odor stimulated imprinted larvae and control. Moreover, DiI tracing experiments in adult zebrafish show a neuronal circuit from crypt/microvillous olfactory sensory neurons via dorsomedial olfactory bulb and intermediate ventral telencephalic nucleus (thus, arguably the teleostean medial amygdala) to tuberal hypothalamus, demonstrating for the first time an accessory olfactory system in teleosts.

Imprinting behaviour in chicks can be induced exclusively during a short period after hatching. During this period, visual information on the imprinting stimulus is conveyed to the visual Wulst (VW) in the telencephalon, which corresponds to the visual cortex of mammals, and then to the memory-storing region known as the intermediate medial mesopallium. These two regions are indispensable for imprinting. We previously showed that imprinting training altered the response pattern of the VW to the imprinting stimulus; however, the precise distribution of cells and the mechanism involved with this altered response remains unclear. Here we showed that a specific population of rostral VW cells responded to the imprinting stimulus by analysing the subcellular localization of Arc/arg3.1 transcripts in VW cells. GABAergic parvalbumin (PV) cells are abundant in the dorsal region of this area, and imprinting training doubled the number of activated PV-positive neurons. An injection of bicuculline, a GABA(A) receptor antagonist, in the dorsal VW disturbed the rostral distribution of responsive cells and thus resulted in a lack of imprinting. These results suggest that activated PV cells restrict VW cells response to dorsal area to form a specific imprinting pathway.

From the early stages of life, learning the regularities associated with specific objects is crucial for making sense of experiences. Through filial imprinting, young precocial birds quickly learn the features of their social partners by mere exposure. It is not clear though to what extent chicks can extract abstract patterns of the visual and acoustic stimuli present in the imprinting object, and how they combine them. To investigate this issue, we exposed chicks (Gallus gallus) to three days of visual and acoustic imprinting, using either patterns with two identical items or patterns with two different items, presented visually, acoustically or in both modalities. Next, chicks were given a choice between the familiar and the unfamiliar pattern, present in either the multimodal, visual or acoustic modality. The responses to the novel stimuli were affected by their imprinting experience, and the effect was stronger for chicks imprinted with multimodal patterns than for the other groups. Interestingly, males and females adopted a different strategy, with males more attracted by unfamiliar patterns and females more attracted by familiar patterns. Our data show that chicks can generalize abstract patterns by mere exposure through filial imprinting and that multimodal stimulation is more effective than unimodal stimulation for pattern learning.

The effects of glucocorticoid receptor dysfunction during embryogenesis on the imprinting abilities and social behaviors of hatchlings were examined using "fertile hen's egg-embryo-chick" system.Of embryos treated with mifepristone (0.4μmol/egg) on day 14, over 75% hatched a day later than the controls (day 22) without external anomalies. The mifepristone-treated hatchlings were assayed for imprinting ability on post-hatching day 2 and for social behaviors on day 3. The findings were as follows: imprinting ability (expressed as preference score) was significantly lower in mifepristone-treated hatchlings than in controls (0.65±0.06 vs. 0.92±0.02, P0.005). Aggregation tests to evaluate the speed (seconds) required for four chicks, individually isolated with cardboard dividers in a box, to form a group after removal of the barriers showed that aggregation was significantly slower in mifepristone-treated hatchlings than in controls (8.7±1.1 vs. 2.6±0.3, P0.001). In belongingness tests to evaluate the speed (seconds) for a chick isolated at a corner to join a group of three chicks placed at the opposite corner, mifepristone-treated hatchlings took significantly longer than controls (4.5±0.4/40 cm vs. 2.4±0.08/40 cm, P0.001). In vocalization tests, using a decibel meter to measure average decibel level/30s (chick vocalization), mifepristone-treated hatchlings had significantly weaker vocalizations than controls (14.2±1.9/30s vs. 26.4±1.3/30s P0.001). In conclusion, glucocorticoid receptor dysfunction during the last week embryogenesis altered the programming of brain development, resulting in impaired behavioral activities in late life.

The formation of imprinted memories during a critical period is crucial for vital behaviors, including filial attachment. Yet, little is known about the underlying molecular mechanisms. Using a combination of behavior, pharmacology, in vivo surface sensing of translation (SUnSET) and DiOlistic labeling we found that, translational control by the eukaryotic translation initiation factor 2 alpha (eIF2α) bidirectionally regulates auditory but not visual imprinting and related changes in structural plasticity in chickens. Increasing phosphorylation of eIF2α (p-eIF2α) reduces translation rates and spine plasticity, and selectively impairs auditory imprinting. By contrast, inhibition of an eIF2α kinase or blocking the translational program controlled by p-eIF2α enhances auditory imprinting. Importantly, these manipulations are able to reopen the critical period. Thus, we have identified a translational control mechanism that selectively underlies auditory imprinting. Restoring translational control of eIF2α holds the promise to rejuvenate adult brain plasticity and restore learning and memory in a variety of cognitive disorders. DOI: http://dx.doi.org/10.7554/eLife.17197.001, eLife digest Shortly after hatching, a chick recognizes the sight and sound of its mother and follows her around. This requires a type of learning called imprinting, which only occurs during a short period of time in young life known as the “critical period”. This process has been reported in a variety of birds and other animals where long-term memory formed during a critical period guides vital behaviors. In order to form imprinted memories, neurons must produce new proteins. However, it is not clear how new experiences trigger the production of these proteins during imprinting. Unraveling such mechanisms may help us to develop drugs that can recover plasticity in the adult brain, which could help individuals with brain injuries relearn skills after critical periods are closed. It is possible to imprint newly hatched chicks to arbitrary sounds and visual stimuli by placing the chicks in running wheels and exposing them to repeated noises and videos. Later on, the chicks respond to these stimuli by running towards the screen, mimicking how they would naturally follow their mother. This system allows researchers to measure imprinting in a carefully controlled laboratory setting. A protein called elF2α plays a major role in regulating the production of new proteins and has been shown to be required for the formation of long-term memories in adult rodents. Batista et al. found that elF2α is required to imprint newly hatched chicks to sound. During the critical period, this factor mediates an increase in “memory-spines”, which are small bumps on neurons that are thought to be involved in memory storage. On the other hand, elF2α was not required to imprint newly hatched chicks to visual stimuli, suggesting that there are different pathways involved in regulating imprinting to different senses. Batista et al. also demonstrate that using drugs to increase the activity of eIF2α in older chicks could allow these chicks to be imprinted to new sounds. The next steps following on from this work are to identify proteins that eIF2α regulates to form memories, and to find out why eIF2α is only required to imprint sounds. Future research will investigate the mechanisms that control visual imprinting and how it differs from imprinting to sounds. DOI: http://dx.doi.org/10.7554/eLife.17197.002

The ability to extract probabilistic information from visual inputs has been reported in human adults and infants (reviewed in [1,2]), and in adults of non-human species, though only under supervised (conditioning) procedures [3]. Here, we report spontaneous sensitivity to the probabilistic structure underlying sequences of visual stimuli in newly hatched domestic chicks using filial imprinting, suggesting that statistical learning may be fully operating at the onset of life in precocial avian species.

When facing decisions about where to live, juveniles have a strong tendency to choose habitats similar to where their parents successfully bred. Developing larval fishes can imprint on the chemical cues from their natal habitat. However, to demonstrate that imprinting is ecologically important, it must be shown that settlers respond and distinguish among different imprinted cues, and use imprinting for decisions in natural environments. In addition, the potential role innate preferences play compared to imprinted choices also needs to be examined. As environmental variability increases due to anthropogenic causes these two recognition mechanisms, innate and imprinting, could provide conflicting information. Here we used laboratory rearing and chemical choice experiments to test imprinting in larval anemonefish (Amphiprion percula). Individuals exposed to a variety of benthic habitat or novel olfactory cues as larvae either developed a preference for (spent >50 % of their time in the cue) or increased their attraction to (increased preference but did not spend >50 % of their time in the cue) the cue when re-exposed as settlers. Results indicate not only the capacity for imprinting but also the ability to adjust innate preferences after early exposure to a chemical cue. To test ecological relevance in the natural system, recruits were collected from anemones and related to their parents, using genetic parentage analysis, providing information on the natal anemone species and the species chosen at settlement. Results demonstrated that recruits did not preferentially return to their natal species, conflicting with laboratory results indicating the importance imprinting might have in habitat recognition.

One of the most important decisions in a monogamous animal's life is the choice of a partner (partner preference), but the process by which this occurs remains poorly understood. The present study tests the hypothesis that hormones and genes play a role in sexual differentiation of partner preferences, as in the song system. We focused on a Z-linked gene, 17β-hydroxysteroid dehydrogenase type IV (HSD17B4), coding for a steroidogenic enzyme that converts estradiol (E2) into an inactive metabolite. HSD17B4 mRNA is expressed more in the song regions of males compared to females throughout development, suggesting that regulation of E2 is important for male-typical song development. Here, we focused on four regions associated with sexual partner preferences. Females had significantly higher levels of HSD17B4 mRNA in auditory (caudomedial nidopallium) and visual (hyperpallium apicale) regions than did males at day 25. HSD17B4 was expressed in the hippocampus and caudolateral nidopallium, but there were no sex differences. In a second experiment, animals of both sexes were treated with E2 and HSD17B4 and androgen receptor (AR) mRNA were measured, since masculinization of the song system is, in part, accomplished by AR. AR was low across the four regions and was not sexually differentiated. E2 treatments increased HSD17B4 mRNA in the auditory region of males, which is contrary to findings in the song system. Our research suggests that different behaviors may be guided by the same genes and hormones, but that the exact nature of the gene–hormone relationships may differ according to brain region and behavior.

The literature recognises a relationship between clinical experience and a successful undergraduate experience in nursing; however what constitutes an effective approach remains the subject of debate, particularly in relation to first year of learning. There is evidence from a biological standpoint that early experience impacts on the behavioural development of animals, described by Konrad Lorenz (1903-1989) as 'imprinting'. The concept of imprinting has resonance for nursing. In this article the importance of 'getting it right at the beginning' is explored and what, if anything, Lorenz's theory tells us about the impact of early clinical learning on subsequent professional development.

SummaryIn the final phase of their spawning migration, Pacific salmon use chemical cues to identify their home river, but how they navigate from the open ocean to the correct coastal area has remained enigmatic [1]. To test the hypothesis that salmon imprint on the magnetic field that exists where they first enter the sea and later seek the same field upon return [2–4], we analyzed a 56-year fisheries data set on Fraser River sockeye salmon, which must detour around Vancouver Island to approach the river through either a northern or southern passageway [5, 6]. We found that the proportion of salmon using each route was predicted by geomagnetic field drift: the more the field at a passage entrance diverged from the field at the river mouth, the fewer fish used the passage. We also found that more fish used the northern passage in years with warmer sea surface temperature (presumably because fish were constrained to more northern latitudes). Field drift accounted for 16% of the variation in migratory route used, temperature 22%, and the interaction between these variables 28%. These results provide the first empirical evidence of geomagnetic imprinting in any species and imply that forecasting salmon movements is possible using geomagnetic models.

To evaluate direct exposure to sodium valproate (VPA) during embryogenesis, we administered VPA to chick embryos and examined their social behaviors after hatching.Embryos treated with VPA (35 μmol/egg) on day 14 were similar to controls for hatching date (day 21) and hatchlings' abilities, such as motor, imprinting, and surface righting. However, these VPA chicks on posthatching day 3 scored significantly low in the chick's social separation stress (SSS) test as follows. Aggregation test evaluated the speed of four chicks, individually isolated by a cardboard in a box, to aggregate upon removal of the cardboards. Belongingness test evaluated the speed of a chick isolated at a corner to join the group of three chicks placed at the opposite corner. Vocalization test for each chick was performed in an isolated corner by using a sound level meter. The results demonstrated that compared with controls, VPA chicks were significantly slow in aggregation (12.7 ± 2.5 s vs. 2.9 ± 0.9 s, p = 0.006) and belongingness (3.6 ± 0.28 s/40 cm vs. 2.6 ± 0.14 s/40 cm, P = 0.003) and weak in vocalization (13.4 ± 2.8 dB/30 s vs. 26.7 ± 1.3 dB/30 s, P = 0.001), respectively. Weight of cerebellum of VAP chick was 15 % lighter than controls (P = 0.004).Chick embryos exposed to VPA during the last week of embryogenesis had impaired social behaviors in spite of normal mortar and imprinting ability. The present method will be a useful animal model for assessing the effects of environment during embryogenesis on social behaviors in later life.

Newly hatched chicks memorize the characteristics of the first moving object they encounter, and subsequently show a preference for it. This "imprinting" behavior is an example of infant learning and is elicited by visual and/or auditory cues. Visual information of imprinting stimuli in chicks is first processed in the visual Wulst (VW), a telencephalic area corresponding to the mammalian visual cortex, congregates in the core region of the hyperpallium densocellulare (HDCo) cells, and transmitted to the intermediate medial mesopallium (IMM), a region similar to the mammalian association cortex. The imprinting memory is stored in the IMM, and activities of IMM neurons are altered by imprinting. Imprinting also induces functional and structural plastic changes of neurons in the circuit that links the VW and the IMM. Of these neurons, the activity of the HDCo cells is strongly influenced by imprinting. Expression and modulation of NR2B subunit-containing N-methyl-D-aspartate (NMDA) receptors in the HDCo cells are crucial for plastic changes in this circuit as well as the process of visual imprinting. Thus, elucidation of cellular and molecular mechanisms underlying the plastic changes that occurred in the HDCo cells may provide useful knowledge about infant learning.

Pacific salmon (Oncorhynchus spp.) navigate towards spawning grounds using olfactory cues they imprinted on as juveniles. The timing at which imprinting occurs has been studied extensively, and there is strong evidence that salmon imprint on their natal water during the parr-smolt transformation (PST). Researchers have noted, however, that the life histories of some species of Pacific salmon could necessitate imprinting prior to the PST. Juvenile pink salmon (O. gorbuscha) spend less time in fresh water than any other species of Pacific salmon, and presumably must imprint on their natal water at a very young age. The time at which imprinting occurs in this species, however, has not been experimentally tested. We exposed juvenile pink salmon as alevins to phenethyl alcohol (PEA) or control water, reared these fish to adulthood, and then tested their behavioural responses to PEA to determine whether the fish successfully imprinted. We found that pink salmon exposed to PEA as alevins were attracted to the chemical as adults, suggesting that imprinting can occur during this stage. Our finding provides some of the first evidence to support the long-standing belief that imprinting can occur in pink salmon prior to the PST.