Filial Preferences Research Articles

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.

Effects of oxytocin-family peptides and substance P on locomotor activity and filial preferences in visually naïve chicks.

Nonapeptides from the vasopressin/oxytocin family have been implicated in a wide variety of social behaviours across vertebrates. Experimental manipulations that alter nonapeptide levels or receptor function in the brain have provided evidence for understanding how nonapeptides influence responses to social stimuli in adults. While behaviours in adults have been extensively studied, much less in known about roles of nonapeptides in early life and the development of affiliative social behaviours. We examined an experience-independent preference (social predisposition) that is present at hatching and is characterized by the tendency of visually naïve chicks (Gallus gallus) to prefer to approach a stuffed hen stimulus over a control stimulus in a choice test. Among chicks that show the social predisposition preference, bilateral intracranial mesotocin injections resulted in higher mean hen preference scores compared with saline-injected controls. Equimolar doses of mesotocin and vasotocin injections had different effects on locomotor activity: vasotocin, but not mesotocin, resulted in hypoactivity. We also tested whether intraperitoneal substance P had an effect on hen preference scores because previous research has proposed that vasotocin effects on social approach are mediated by peripheral release of substance P, but found no significant effect. All together, our data suggest that mesotocin signalling may be important for social predispositions and can potentially enhance the perceived salience of social stimuli soon after hatching. Specifically, mesotocin release and signalling in the brain may regulate the ability to recognize naturalistic stimuli and/or to act on the motivation to approach naturalistic stimuli.

Filial imprinting and associative learning

Evidence is reviewed that is relevant to an interpretation of filial imprinting as a form of classical or Pavlovian conditioning. For such an interpretation it has to be assumed that the imprinting object provides both the unconditioned stimulus (UCS) and the conditioned stimulus (CS). The difficulty for an experimental approach is that CS and UCS are always presented simultaneously and cannot be manipulated independently, making it virtually impossible to test phenomena such as latent inhibition and extinction. Existing evidence is consistent with a conditioning theory of imprinting, for instance with regard to the reversibility of filial preferences. Some hitherto unexplained findings can be accounted for in terms of overshadowing and blocking. Results of an experiment are discussed in which the occurrence of blocking was explicitly tested. The findings support an associative learning interpretation of imprinting, but further experiments are needed to be able to rule cut alternative explanations.

Prenatal Sensory Stimulation Induces BDNF Gene Expression in the Brain and Potentiates the Development of Species-Specific Predisposition in Newborn Chicks.

We studied the effects of light and non-specific sound stimulation of domestic chick embryos on their filial preference as well as on the expression of two transcriptional factors c-Fos and Egr-1 and neurotrophin BDNF in the embryo brain. Prenatal light stimulation increased preference of the "natural" object, thus producing a priming effect. In the brain of E19 embryos, c-Fos and Egr-1 were expressed at a high basal level and neither light nor sound stimulation affected the number of cells expressing these factors. BDNF mRNA was also present in a number of brain areas of non-stimulated embryos, but light and sound stimulation enhanced the expression of BDNF mRNA in brain structures associated with filial imprinting. These findings suggest that BDNF is probably involved in the effects of prenatal priming on the development of species-specific behavior.

Blinking Bird Brains: A Timing Specific Deficit in Auditory Learning in Quail Hatchlings

Contingency perception is critical during infancy, providing the basis for the continuous learning (and re-learning) of the relation between the developing body, self-produced actions, and the environment. Nevertheless, relatively few studies have systematically examined the spatiotemporal parameters that optimize learning during development. Here, we present a series of experiments exploring a novel timing-specific deficit in auditory learning in an animal model, the bobwhite quail (Colinus virginianus). In this paradigm, chicks vocalize to hear playback of an unfamiliar maternal call and are later tested for their filial preference for that call over a novel maternal call. Rather than a simple, hyperbolic decline in learning with increased delay between chick vocalization and playback, we found a window—450–900 msec after chicks ceased vocalizing—in which chicks appeared to have difficulty learning and forming a preference for the maternal call. This deficit nonetheless occurred only when the spatial location of call playback switched semi-randomly during training, suggesting an attentional explanation for this deficit. Our findings indicate that optimization of the temporal parameters in operant paradigms with infants can be complex, particularly if tasks requiring the switching of attention between spatial locations. Our findings may thus be instructive for other developmental research with infants employing operant components.

Maternal Contact Differentially Modulates Central and Peripheral Oxytocin in Rat Pups During a Brief Regime of Mother–Pup Interaction that Induces a Filial Huddling Preference

Central oxytocin mediates the acquisition of a filial preference for maternal odour in rat pups, manifested by their huddling preferences. The present study was designed to examine whether maternal care modulates oxytocin concentrations in rat pups and, if so, how different types of maternal contact are associated with the pups' oxytocin concentrations. Pairs of 14-day-old littermates were removed from their home cage for 1 h and then placed with a lactating foster mother for 2 h, or they remained isolated at room temperature. Enzyme immunoassays revealed that maternal care and maternal separation can differentially modulate pups' oxytocin concentrations. Both hypothalamic and serum oxytocin increased during the 1-h separation. Pups placed with a foster mother after the separation maintained the same concentrations in the hypothalamus and serum through the fostering period. By contrast, pups placed with no mother showed a further increase in hypothalamic oxytocin but serum oxytocin decreased. Behavioural analyses revealed that skin-to-skin contact with the mother, but not simple physical contact or maternal licking/grooming, was positively correlated with the pups' hypothalamic oxytocin concentrations. These neuroendocrine data match previous findings showing that skin-to-skin contact with mother facilitates the acquisition of the pups' huddling preference for a maternally-associated odour. Taken together, the present study suggests that maternal skin-to-skin contact stimulates pups' central oxytocin, at the same time as creating the conditions for inducing a preference for maternal odour and establishing a social affiliation in rat pups; the natural schedule of maternal separation and reunion may modulate pups' oxytocin concentrations, providing scaffolding for the acquisition of their filial huddling preference.

Oxytocin mediates the acquisition of filial, odor-guided huddling for maternally-associated odor in preweanling rats

The present study was designed to examine possible roles of oxytocin (OT) in the acquisition of a filial huddling preference in preweanling rats. We used a procedure in which a scented, foster mother can induce an odor-guided huddling preference in preweanling pups, following a single, 2-h-long co-habitation (Kojima and Alberts, 2009, 2011). This single, discrete period for preference learning enables us to observe the mother–pup interactions that establish the pups' preferences and to intervene with experimental manipulations. Four, 14-day-old littermates interacted with a scented foster mother that provided maternal care during a 2-h session. Two of the pups were pretreated with an intracerebroventricular injection of OT or an oxytocin antagonist (OTA), and the others received a vehicle injection. Filial preference for a maternally-paired odor was measured in a huddling test the next day. OT is necessary for acquisition of the filial preference: The preference learning was blocked in the pups treated with OTA, but not in their vehicle-treated littermates who experienced the same mother at the same time. Injection with exogenous OT did not augment the pups' preference. Manipulating pups' central OT also altered the contact interactions of the mother and pups. When some pups received OT, mother–litter aggregations formed as frequently and with similar combinations of bodies, but contact aggregations were significantly more cohesive than when some pups in the litter received OTA. We discuss dual, behavioral and neuroendocrine roles of OT in social learning by preweanling rats.

Warmth from skin‐to‐skin contact with mother is essential for the acquisition of filial huddling preference in preweanling rats

During a single, 2-hr session with a scented foster dam, preweanling rat pups form an affiliative attraction to an odor associated with the maternal caregiver, manifest as a huddling preference. To identify maternal stimuli that induce this filial preference, we quantitatively examined behavioral interactions during odor conditioning. Bout duration of skin-to-skin (STS) contact was positively associated with the preference. In contrast, simple physical contact and anogenital licking were not significantly related to the preference. The frequency of nonanogenital licking was negatively associated with the preference as well as with bout duration of STS contact. When odor conditioning was conducted with a warm cylinder, ambient warmth, or stroking as the unconditioned stimulus, only pups exposed to the warm cylinder exhibited a preference for the conditioned odor. These results suggest a positive, affiliative effect of maternal STS contact on pup filial preference, which may be disrupted by maternal licking.

Early development of filial preferences in the rabbit: implications of nursing- and pheromone-induced odour learning?

Newborn rabbits, Oryctolagus cuniculus, discriminate between different categories of adult conspecifics on the basis of their abdominal odour cues. Whether these cues can support the development of filial preferences has not been adequately tested. Using a two-choice paradigm, we assessed the ability of 3–8-day-old pups to orient selectively to the mother versus an unfamiliar female, either spontaneously or after odour conditioning. In experiment 1, nonconditioned pups roamed indifferently over the mother and an unfamiliar female. In experiment 2, pups conditioned to a neutral odorant while nursing or with the mammary pheromone became attracted by the odorant. In experiment 3, pups that had learned the odorant while nursing oriented for longer to any female carrying it, but the unscented mother and a scented unfamiliar female were equally attractive. Finally, in experiment 4, pups that had learned the odorant paired with the mammary pheromone showed a preference for their scented mother, but not systematically for a scented unfamiliar female; furthermore, they were equally attracted by the unscented mother and a scented unfamiliar female. In sum, pups did not spontaneously evince an olfactory preference for the mother when opposed to an unfamiliar female, although they seemed able to detect individual maternal odours. In fact, they appeared to react to both species-specific cues and individual cues that they had learned, and their responses depended on their degree of familiarity with the cues and on the context. The mammary pheromone by itself might act as both a releasing and a reinforcing signal in these early socially oriented behaviours.

Nonnutritive sucking: One of the major determinants of filial love

The present study investigated the rewarding effects of nonnutritive sucking on the development of a filial preference. Two experiments were conducted to test whether nonnutritive visceral and oral stimuli have reinforcing properties independent from each other or act in synergy. Lambs could interact freely with their dam but were deprived of suckling by covering the udder for the first 12 hr. In Experiment 1, suckling was prevented and replaced by human giving, in the presence of the mother, either a bottle of water (B5 and B2.5: 5% or 2.5% birth weight, BW, divided into seven portions over 12 hr) or water via tube-feeding (I5 and I2.5: 5% or 2.5% BW, also divided into seven portions over 12 hr). During a two-choice test performed at 12 hr after birth, only B5 and I5 lambs preferred their mother to an alien ewe however, B5 were faster at choosing their mother at the beginning of the test. B2.5 and I2.5 lambs made a random choice. In Experiment 2, suckling was prevented and replaced by human giving, in the presence of the mother, either a bottle of water (B2.5: 2.5% BW, divided into seven portions over 12 hr) or water via tube-feeding (I10 and I2.5: 10% or 2.5% BW, also divided into seven portions over 12 hr). During a two-choice test at 12 hr, tube-fed lambs (I10 and I2.5) preferred their mother to a human. B2.5 lambs were equally attracted to both partners and spent more time near the human than lambs from the other groups. In a test of reactivity to a human performed on neonates isolated from their mother, B2.5 lambs explored the human much more than the other lambs. The presence of the human had soothing properties in B2.5 lambs and once the human left, they were the only lambs displaying enhanced vocal and locomotor activity. In these experiments, nonnutritive gastrointestinal stimuli induced a preference for the mother whereas nonnutritive sucking led to a strong positive relationship with the human. These results suggest that when lambs suckle their dam, the development of filial bonding is facilitated through the combined effects of oral and gastrointestinal stimuli.

Early learning and the development of filial preferences in the chick

Newly hatched domestic chicks ( Gallus gallus domesticus) rapidly form a social preference for a conspicuous stimulus to which they are exposed. The learning process involved is known as filial imprinting. When chicks are exposed to an audio-visual compound stimulus, both auditory and visual learning are enhanced. The enhancement of visual imprinting is virtually abolished when chicks are exposed separately to the auditory element, either before or after training with the audio-visual compound. Simultaneous exposure to the two elements of the compound is superior to sequential exposure in achieving the enhancement of visual learning. These results are unlike Pavlovian conditioning, but are consistent with an interpretation of imprinting as a form of within-event learning, where links are formed between the representations of the elements of the compound, that can be weakened by separate exposure to an element. Apart from imprinting, chicks may show a developing predisposition to approach stimuli resembling conspecifics. The predisposition emerges in dark-reared chicks given some non-specific experience during a sensitive period, and is expressed as a relatively general preference for stimuli with a head and neck region. In the natural situation, the animal’s response may be biased by the predisposition, and through imprinting it then learns the characteristics of individuals.

Imprinting, learning and development: from behaviour to brain and back

Neural and behavioural analyses have shown that the formation of filial preferences in young, precocial birds involves at least two separate processes. One process is an emerging predisposition to approach stimuli with the characteristics of the natural mother. The other (learning) process of filial imprinting results in chicks preferentially approaching a stimulus to which they have been exposed and involves forming links between the components of the exposed stimulus. The neural substrate for the predisposition is different from that underlying imprinting, and different regions of the chick brain are involved in distinct aspects of learning about imprinting stimuli.

Delayed Induction of a Filial Predisposition in the Chick after Anaesthesia

BOLHUIS, J. J. AND G. HORN. Delayed induction of a filial predisposition in the chick after anaesthesia. PHYSIOL BEHAV 62(6) 1235–1239, 1997.—In domestic chicks, Gallus gallus domesticus, early filial preferences are formed as the result of at least two processes: learning by exposure to conspicuous objects (filial imprinting) and a developing predisposition to approach some stimuli rather than others. The predisposition may be measured in visually naive chicks, e.g. as a preference for a rotating stuffed jungle fowl hen rather than for a rotating red box. Non-specific experience, such as handling or being placed in a running wheel in darkness, for a short time, is sufficient to induce the predisposition. In Experiment 1, the existence of a sensitive period for the induction of the predisposition, between approximately 14 and 42 h after hatching, was confirmed. The putative effect of anaesthesia on the induction of the predisposition was investigated in Experiment 2. Soon after hatching dark-reared chicks received injections of the anaesthetic equithesin (0.12 ml, IP), or saline, or they did not receive injections (controls). The chicks were subsequently placed in running wheels for a total of 2 h at either 24 h or 48 h after hatching. The following day the chicks’ preferences were tested. In the 24 h-chicks, the saline and control groups showed a significant mean preference for the stuffed fowl, whilst the equithesin group did not. In contrast, in the 48 h-groups of chicks, only the equithesin group showed a significant mean preference for the stuffed fowl. These results suggest that the anaesthetic equithesin affects a developing filial predisposition in the domestic chick, and does so by delaying the onset of a sensitive period for the induction of the predisposition.

Archistriatal Lesions Impair the Acquisition of Filial Preferences During Imprinting in the Domestic Chick

The avian archistriatum has been demonstrated to play a role in agonistic behaviours and avoidance learning. However, the extent of its role in learning is unknown. The involvement of the archistriatum in the learning process of filial imprinting was therefore investigated in day-old chicks. Bilateral archistriatal lesions, lateral cerebral area lesions or sham archistriatal penetrations were made in dark-reared, day-old chicks, which were subsequently exposed to either a rotating red box or blue cylinder for 2 x 1 h training sessions. Three hours later, the approach of chicks to their training object and to the other, novel object was measured. Chicks with archistriatal lesions ran a similar distance towards each stimulus and therefore failed to display a preference for their training object. However, chicks with sham archistriatal penetrations or lateral cerebral area lesions exhibited a significant preference for the object they had been trained upon. These results demonstrate that the archistriatum is essential for the expression of an imprinted preference. All chicks approached their training object significantly more on their second compared to their first training exposure, suggesting that some aspects of imprinting behaviour remain intact in chicks with archistriatal lesions. Taken together with the results of previous work, the current data suggest that the archistriatum may be involved in retention of significant aspects of the imprinting experience, or in motivation to approach imprinting objects.

Acquisition of a filial preference in an altricial bird without food reinforcement

Acquisition of a filial preference in an altricial bird without food reinforcement

Predispositions and learning: behavioural dissociations in the chick

In young domestic chicks, Gallus gallus domesticus, the formation of filial preferences involves at least two processes: a learning process through which chicks come to recognize the features of certain stimuli to which they are exposed and a predisposition to approach stimuli resembling conspecifics. The predisposition becomes manifest as an increasing preference for a rotating, stuffed adult fowl over a rotating red box. This change over time occurs even in chicks that have been trained by exposure to the red box. The present experiment confirmed the latter result, and also showed that preferences did not change over time when they were measured in tests involving the familiar red box and a novel, striped blue box. Furthermore, when chicks were trained with the red box after a sensitive period for the development of the predisposition had elapsed, preferences did not change with time of testing, but were determined by learning only. The results rule out an interpretation of earlier findings in terms of stimulus-dependent differential forgetting. They suggest that the mechanism underlying learning is separable from the mechanism underlying the predisposition.

An Evaluation of Auditory Learning in Filial Imprinting

The characteristics of auditory learning in filial imprinting in precocial birds are reviewed. Numerous studies have demonstrated that the addition of an auditory stimulus improves following of a visual stimulus. This paper evaluates whether there is genuine auditory imprinting, i.e. the formation of a preference for an auditory stimulus as a result of exposure to it. Many studies lack important features such as a balanced experimental design or a retention interval, which makes it difficult to draw firm conclusions from their results. The majority of studies of early auditory learning have used a compound of a visual and an auditory stimulus during training. Presentation of a visual object during auditory training improves learning about sounds. The visual stimulus may act as a US for learning about sounds. Alternatively, presentation of a visual stimulus may increase attention or arousal and thereby improve learning about the sound. In a large number of studies visual stimulation during auditory exposure was provided by the presence of a hen or siblings. Relatively few studies using only auditory exposure have demonstrated significant auditory learning. Exposure to a sound before hatching can lead to a significant preference for that sound when tested after hatching. However, such preferences are generally weak and short-lived. In a number of species, a predisposition for species-specific calls has been demonstrated, that is already apparent before hatching. It is concluded that auditory stimuli play an important role in the formation of filial preferences, but that auditory imprinting is not as prominent as has sometimes been suggested, especially when compared to visual imprinting.

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 naïve 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.(ABSTRACT TRUNCATED AT 400 WORDS)

The importance of being first: a primacy effect in filial imprinting

The stability of filial preferences of domestic chicks, Gallus gallus domesticus, was investigated. In a series of experiments, preferences were measured in simultaneous choice tests at the end of 3-day periods of exposure to conspicuous artificial objects. In experiments 1 and 2, day-old chicks were exposed to one of two coloured cylinders, followed by exposure to the alternative stimulus. The original preference was significantly reversed. After a third phase of the experiment, during which the chicks were isolated (experiment 1) or exposed to the two stimuli simultaneously (experiment 2), the preference changed significantly towards the first object. A significant preference for the first object was reacquired in only one combination of stimuli in experiment 2a. The results were similar for experiments 2b–2d, in which the period of exposure to the first (2b) and the second (2d) object was increased or when there was a period of isolation after exposure to the first object (2c). In all these experiments, the stimuli differeed only in the single dimension of colour. In experiment 3, the two stimuli used differed in colour, shape and pattern. Three days of exposure to one object, followed by 3 days exposure to the other object and 3 days to both objects simultaneously, led to a significant ‘resurfacing’ of a preference for the first stimulus, irrespective of which stimulus was presented first. These results confirm that the reversal of filial preferences need not be permanent and are consistent with, a ‘competitive exclusion’ model of imprinting.

Interacting mechanisms during the formation of filial preferences: The development of a predisposition does not prevent learning.

It has previously been demonstrated that under certain circumstances, 2-day-old dark-reared chicks prefer a stimulus that resembles a conspecific to less naturalistic objects. In our first three experiments, we assessed whether exposure to the latter type of object, after the predisposition had developed, affected chicks' preferences. The results of Experiment 4 show that, under rearing conditions in which the predisposition does not develop, exposure to an artificial stimulus leads to a strong preference being established for that stimulus