Imprinting

BIBLIOGRAPHY

The term “imprinting” refers to the rapid acquisition by young animals of the primary social bond to their parents during a limited period very early in life. This imprinting phenomenon can be most clearly seen in precocial bird species, whose young are hatched at a relatively advanced stage of development and are able to move about independently rather soon after hatching. Such species include ducks and other waterfowl, as well as chickens and turkeys. Imprinting also appears to exist in some precocial mammal species, such as the guinea pig (Hess 1959a; Shipley 1963). In all of these cases the attachment of the young to the mother is evident when he follows her about. As Morgan (1896) remarked, there is evidently an innate tendency to follow but there is no requirement that the object to be followed be the biological mother. After the infantile following behavior has been outgrown, the attachment continues to exist and forms the basis of later social preferences (Lorenz 1935).

It also appears that the primary socialization processes in other social animals contain features highly similar to those of imprinting. It is now well known that early life experiences play a decisive role in the formation of an animal’s or a person’s affectional system (e.g., Bowlby 1951; Harlow 1958; Harlow & Harlow 1962). Under normal conditions the first social experiences are with the parents and, in many species, often also with siblings. It is through these early social experiences that individuals become attached to members of their own species. On the other hand, under unusual circumstances, produced either experimentally in a laboratory or accidentally, social attachments to members of an alien species or even to inanimate objects can be formed during the earliest life period.

Primary socialization is of extreme importance not only in determining the cohesiveness of animal groups, important for immediate survival, but also in the continuation of the species, for it often influences the nature of sexual behavior, in particular with respect to the object chosen or accepted (Lorenz 1935). Precocial species provide the clearest instances of imprinting. In the case of species that are not precocial, primary socialization may have different grades of similarity with the classical imprinting phenomenon. One of the most important differences is that the time period involved is not so dramatically short as it is in imprinting and may extend throughout the period of association between young and parents (e.g., Kling-hammer 1962; Klinghammer & Hess 1964). But in all cases the primary socialization occurs during the first life period.

History. The importance of a relatively limited period in early life for the formation of social bonds has been well noted. Pliny the Elder, for example, told the tale of a goose that followed Lacydes faithfully (Naturalis historia, x). Both D. A. Spalding (1873) and C. L. Morgan (1896) reported that when they hand-reared chicks away from the mother, the chicks completely refused to have anything to do with her when they finally met. C. O. Whitman (Craig 1908) turned this phenomenon to a practical use with nonprecocial, or altricial, species: whenever he wanted to cross two species of pigeons, he would rear the young of one species with foster parents of the other species. When fully grown, pigeons reared with foster parents of a different species preferred to mate with members of that species rather than of their own. Later, Heinroth and Heinroth (1924-1928) hand-reared the young of almost every species of European bird, and noted that many of the social responses of these birds were transferred to their human caretaker. Indeed, interspecies sexual fixation has been observed in other birds, some fishes, and two mammals, the alpaca and vicuñna (Goodwin 1948; Baerends & Baerends-van Roon 1950; Hodge 1946).

It was Konrad Lorenz, the eminent European zoologist, who first looked at the phenomenon of imprinting scientifically and postulated some laws governing its occurrence. In a classic paper in 1935, Lorenz described it and gave it its name (in German, Pragung). Lorenz pointed out for the first time that if imprinting is to occur, the young animal must be exposed to its object during a critical period early in its life. He postulated that the first object to elicit a social response on the part of a young animal later released not only that response but also related ones, such as sexual behavior.

The first systematic investigations on imprinting were published in 1951. The independent. work of Ramsay (1951) in the United States and of Fabri-cius (1951a; 1951b) in Europe gave the first indications of some of the important factors in imprinting. Most of Ramsay’s experiments dealt with exchange of parents and young, although he also imprinted some waterfowl with such objects as a football or a green box. He worked with several species of ducks and a variety of chicken breeds. He noted the importance of auditory stimulation in imprinting and the effect of changes in coloring on recognition of the young by the parents, as well as of the parents by the young. His findings indicated that color is an essential element in recognition, while size or form seemed to be of less importance. Fabricius studied several species of ducks, including tufted ducks, eider ducks, and shovellers. He observed that newly hatched ducklings have a very strong tendency to follow the first moving objects with which they come in contact, for when they were exposed to older ducklings of a different species, they followed them persistently even though they were rewarded only with harassment and violent nipping. Fabricius found that there was a sensitive period during which imprinting occurred most easily: it had its peak at the age of 12 hours and then decreased until, after the age of 24 hours, imprinting was more or less impossible, for the animals became increasingly fearful of new objects. Movement was discovered to be a great influence in eliciting imprinting, as also were rhythmic calls.

Ramsay and Hess (1954) reported a method of studying imprinting in the laboratory, using a runway and a model fitted with a loudspeaker. Later the apparatus was modified as seen in Figure 1. Then Hinde (1955), using moorhens and coots, confirmed the importance of motion in eliciting imprinting responses. He also reported that following

was most easily elicited during the first day after hatching; older birds usually fled from the model he presented to them, thus showing the role of fear in ending the sensitive period for imprinting. Furthermore, he noted that if birds were exposed to different models, persistent following took place only with a familiar model.

Since then there have been an increasing number of experimenters who have attempted to assay the imprinting phenomenon, and their work has brought about an increasing understanding of the imprinting process and of the socialization process in general.

The critical period. The most salient feature of the imprinting phenomenon is that it occurs so early in life. Very soon after hatching, chicks and ducklings can follow mother objects and, in fact, show a strong desire to do so. At the very outset, Lorenz (1935) postulated that imprinting could “only take place within a brief critical period in the life of an individual,” which was “a very specific physiological state in the young animal’s development.” He noted that Greylag geese were imprinted during the first few hours after hatching and suggested that imprinting could occur as early as the first few minutes after hatching. He also recorded his observation that some partridges he happened to come across in a field when they were only a few hours old had obviously already been imprinted to their parents and could not be induced to approach him. Other researchers have noted that the readiness to follow an object wanes with increasing age (Alley & Boyd 1950; Hinde 1955; Hinde et al. 1956; Fabricius 1951b; Fabricius & Boyd 1954).

However, it was Ramsay and Hess (1954) who determined in the laboratory that there is indeed a rather limited age period during which mallard ducklings can be well imprinted, and that maximum imprinting occurs consistently only in ducklings imprinted at the age of 13 to 16 hours. The existence of an optimum developmental stage for imprinting has also been confirmed by Gottlieb (1961a), who used special procedures in order to pinpoint the age of his ducklings in days and hours from the very beginning of their embryonic development. It was determined that the age of 27 to 27½ days from the beginning of incubation was indisputably the most sensitive time for imprinting, and that by the age of 28½ days very little imprinting could take place.

Fear has been suggested by many writers as the factor that ends the period of imprintability, and Fabricius (1951a) has suggested that the initial inability of birds to locomote could account for the first rise in imprintability. Hess (1959b) actually plotted locomotor ability and fearfulness of chicks as a function of age and found that the emergence of fearfulness coincided exactly with the limits of the critical period for imprinting. However, initial imprintability is higher than increasing locomotor skill would suggest.

Interspecies and intraspecies differences. Species and breed differences are emerging as an increasingly important factor in assessing the various parameters of the imprinting phenomenon. According to Hess (1959a), some species and breeds, such as wild mallard ducks, show an extremely high degree of imprintability and usually respond quite vigorously to the first imprinting object they meet. They also retain the effects of the experience quite firmly. Leghorn chicks, in comparison with Vantress broiler chicks, may not show as much responsiveness in a laboratory imprinting situation, and even when they have had relatively extensive exposure to an imprinting object, this experience may not be as effective. In spite of the fact that chicks and ducklings have the same critical-period ages for imprinting, the peak of the strength-of-imprinting curve is much lower for chicks than it is for ducklings, as is the general curve itself. There are probably also differences among different species in the type of object that is adequate to arouse imprinting. Other differences between species and between breeds will be brought up as the topic is further pursued. It is, therefore, well to remember that while the socialization processes in different animals may resemble imprinting, generalization between, and even within, species must be cautious and limited.

Prior social and sensory experiences. Many researchers have found that housing chicks communally prior to the imprinting experience decreases imprintability or responsiveness (Guiton 1958; 1959; Sluckin & Salzen 1961; Hess 1962; 1964). It appears that under these circumstances they become imprinted to each other, and that this prior imprinting hinders the formation of imprinting toward a new object. The inhibition of imprinting to a new object when imprinting has already occurred appears to be a basic characteristic of the imprinting phenomenon and has been confirmed by Hess (1959a), who found that ducklings imprinted more strongly to models to which they had been first exposed than to a model they met immediately afterward.

Under natural conditions it does appear that imprinting to siblings can occur either simultaneously with or immediately after imprinting to the mother; this might account for “flocking” behavior. The nature of the effect of exposure to siblings before the laboratory imprinting experience has been found to be related both to species membership and to age at exposure to the imprinting experience (Hess 1964). In chicks and ducklings the effect of prior socialization was found to lower imprintability to the model. However, in the case of chicks the amount of following of the model was increased as a result of the socialization experience, especially when these chicks were well past the critical-period age, 36 hours. With ducklings, however, socialization decreased the amount of following as well as of imprintability.

Moltz and Stettner (1961) varied the visual stimulation of some ducklings with hoods that permitted them only diffuse light stimulation. When subjects were tested for imprintability, those that had experienced diffuse light were found to show greater imprintability when first exposed to the imprinting model at the ages of 12, 24, and 48 hours than did those that had lived in normal light conditions. The animals raised in diffuse light were most responsive at the age of 24 hours, while the normal animals were most responsive at the age of 12 hours and responded very little at the age of 48 hours, when the diffuse-light subjects still showed strong responsiveness. Hess (1964), however, has reported somewhat different results with chickens. Dark-reared chicks (like dark-reared ducklings) have maximum responsiveness at the age of 13 to 16 hours after hatching. However, socially isolated chicks exposed for two hours to patterned light stimulation prior to the imprinting experience behaved no differently from completely dark-reared animals if they were placed in the imprinting situation at the age of 16 hours; but if they were exposed to imprinting at the age of 48 hours, they followed somewhat better than the dark-reared ones. This difference, nevertheless, is much less than that resulting from prior social experience.

Experimental variables. Hess (1957) has postulated a law of effort in imprinting, which states that the more effort a young chick or duckling expends while following or attempting to be with the imprinting model, the more strongly it will be imprinted, as shown by later preference behavior when both the imprinting model and an unfamiliar one are offered. Imprinting-strength scores were obtained for 12- to 17-hour-old ducklings, who were made to follow an imprinting model for different distances in a ten-minute period. The greater the distance the ducklings had to follow, the better they were imprinted. This held true up to 50 feet, after which further distances did not materially increase imprinting strength. Moreover, when ducklings were allowed different amounts of time to follow the model for the same distance, the imprinting-strength scores for the same following distances were essentially identical. Evidently time in itself has no effect on the strength of imprinting.

Furthermore, muscle relaxation prevents imprinting, as shown by the failure of chicks and ducks that had been imprinted while under the influence of either meprobamate or carisoprodol to show any effect of the experience when tested later. If animals are imprinted normally but tested under drug conditions, there is no effect of the drug (Hess 1957; Hess et al. 1959). This, together with the fact that socialized chicks follow well but do not imprint well when an attempt is made to imprint them after the critical period, demonstrates that the law of effort applies only to socially naive normal animals exposed to the imprinting situation at the critical-age period.

It also appears, on the basis of several experiments (Hess 1957; 1959a; 1959c), that some of the research that has attempted to assess the law of effort by preventing animals from following the imprinting model have failed to take into account the effort expended by subjects struggling to escape restraint or approach the model. The effectiveness of struggle when animals cannot move is shown by the fact that chicks and ducklings have a greater imprintability in the first few hours after hatching than their locomotor skill would seem to indicate. Furthermore, Gottlieb (1961b) has shown that equal imprinting strength in two different duck varieties does not necessarily reflect the same amount of following; thus, if the amount of following is to be taken as a valid indicator of probable able imprinting strength, any comparisons must be between animals of the same variety.

The effect of painful stimulation during the imprinting experience is also an important factor. Fabricius (1951a) early reported the fact that his ducklings persisted in following older ducklings who maltreated them vigorously. Hess (1959c) observed that when ducklings were being imprinted to a human being who carelessly stepped on their toes, they did not run away in fear but stayed even closer. Kovach and Hess (1963) have demonstrated experimentally that during the critical-age period the administration of painful electric shocks enhances the amount of following during the imprinting experience, while after the critical age electric shocks depress following. These results emphasize the importance of the critical-age period; during it imprinting is enhanced by punishment, while after it imprinting is hindered, suggesting that the processes occurring after the critical period conform far more closely to the laws of conventional association learning than do the processes occurring during the critical period.

Other variables. While a perusal of the research literature shows that young birds can respond to an amazingly wide variety of different objects in the same way in which they would respond to their own mother, there are also indications that some characteristics of a potential imprinting object are more effective in eliciting imprinting than are others. Ramsay (1951), for example, indicated early that color was important, while size and shape appeared to be less so. Others (Lorenz 1935; Fabricius 1951a) have shown that rhythmic sounds are more effective than other types of sounds, that low-pitched ones arouse imprinting more than high-pitched ones (Collias & Collias 1956), and so forth. Schaefer and Hess (1959) have demonstrated that certain colors are more capable of eliciting imprinting, and that certain shapes are more potent than others in terms of both following behavior during imprinting and test scores when the chicks were confronted at a later age with the imprinting model and unfamiliar ones.

Food imprinting. Hess (1962; 1964) has suggested that imprinting, conceived of as the rapid acquisition of an object toward which an innate response could be directed, is not limited to the formation of social bonds but also applies to the learning of food objects by chicks at the third day of age. He carried out experiments in which chicks were given food reward for pecking at specific stimuli and were not rewarded for pecking at others. In the face of withdrawal of food, the effects of this experience were strongest when the rewarding had occurred during the third day of age; the greater the time interval between that age and the time of rewarding, the less was the effect of the experience. When the rewarding had occurred at the age of one day or at more than five days, there was no effect on the pecking behavior; but when the chicks had been rewarded at the age of three days, they continued to peck at the specific stimuli for at least ten days without any signs of decreasing intensity, even though there was no longer any food reward.

Furthermore, Hess (1962; 1964) found that if the food-reward experience took place while the three-day-old chicks were under the influence of either meprobamate or carisoprodol, when food reward was removed the chicks behaved essentially as if they had never had the reward experience. Hess therefore concluded that this phenomenon showed much more similarity to imprinting than to more common association-learning processes and must represent true imprinting of food objects. He did not, of course, claim food imprinting and social imprinting to be alike in all respects, for they are related to two very different vital functions—social cohesiveness, necessary for the survival of a social species, and ingestion of nutritious material, necessary for the survival of the individual.

Imprinting and learning. While in both imprinting and learning, a relationship or “connection” is established between an object and a response, there is a basic distinction between the two processes. In imprinting there is a critical period, developmentally timed, during which certain wide classes of stimuli act as releasers or unconditioned stimuli for certain types of innate responses; whereas, in ordinary association learning, the object in question does not act as an unconditional stimulus for the response but is initially neutral in its effect on the animal’s behavior. There is no critical period for association learning, although cases have been found where learning ability increases with age, in contrast to the decreasing of imprintability as the animal grows older.

Association learning is more effective when practice trials are spaced than when they are massed, whereas in imprinting massed effort has been found to facilitate the formation of imprinted social bonds.

Furthermore, Hess (1962; 1964) has reported that meprobamate and carisoprodol do not at all hinder either the learning or the retention of ordinary visual-discrimination learning with food as a reward, whereas it impedes both social and food imprinting.

Finally, it is well established that in association learning it is what has been most recently learned that is remembered the best. However, in imprinting, what has been learned first is the strongest, as shown by experiments in which ducklings were exposed to two different imprinting models during the critical-age period (Hess 1959a; 1959b; 1959c). The studies of the effects of socialization with siblings on imprintability to a parent model also demonstrate the importance of primacy in imprinting (Hess 1964).

It is of extreme importance to be aware of these differences between imprinting and association learning, because once the appropriate critical-age period has passed without imprinting’s having occurred, for lack of exposure to a suitable object, it is possible to use any stimulus to which the animal could have responded earlier as a potential conditioned stimulus, to which it may be trained, through conventional means, to make conditioned responses. Here the animal can readily generalize to other objects, thus increasing the range to which it can make conditioned responses, in contrast to the fact that when an animal has actually been imprinted to an object during the critical period, only this particular object or ones very much like it will, from then on, act as unconditional stimuli, though the range to which the animal was first capable of responding was very broad. What is more, even if imprinting has already occurred during the critical period, the animal can still be trained, through association learning, to make conditioned responses to objects to which it has not been imprinted. In such a case the response to the imprinted object may seem, superficially, to be just like the conditioned responses that the animal has been trained to make to a conditioned stimulus. But these two categories of responses are completely different in terms of the conditions of their origins and also in terms of their long-range effects on the character of the animal’s behavior.

Both social imprinting and food imprinting have counterparts in association learning. Taming is the association-learning counterpart of social imprinting; humans can tame an animal that has already been imprinted to its own species. But the two social bonds are not alike, for a tamed animal will court and attempt to mate with members of the opposite sex of its own species, not with human beings. Skinnerian experiments, in which birds are trained to peck at colored lights in order to obtain food or water, reflect the association-learning counterpart of food imprinting. But upon complete withdrawal of food reward, the bird’s pecking response to a colored light will soon disappear, while chicks imprinted to certain food objects when three days old do not lose their acquired pecking habits, even after long experience with no food reward.

Eckhard H. Hess

[Other relevant material may be found inEthology; Instinct; Learning; Psychology, article onComparative Psychology; Socialization.]

BIBLIOGRAPHY

Alley, R.; and Boyd, H. 1950 Parent-Young Recognition in the Coot. Ibis 92:46-51.

Baerends, G. P.; and Baerends-van Roon, J. M. 1950 An Introduction to the Study of the Ethology of Cichlid Fishes. Behaviour Supplement no. 1. Leiden (Netherlands): Brill.

Bowlby, john 1951 Maternal Care and Mental Health. Geneva: World Health Organisation.

Collias, Nicholas E.; and Collias, Elsie C. 1956 Some Mechanisms of Family Integration in Ducks. Auk 73: 378-400.

Craig, Wallace 1908 The Voices of Pigeons Regarded as a Means of Social Control. American Journal of Sociology 14:86-100.

Fabricius, Eric 1951a Zur Ethologie junger Anatiden. Acta zoologica fennica 68:1-178.

Fabricius, Eric 1951b Some Experiments on Imprinting Phenomena in Ducks. Pages 375-379 in International Ornithological Congress, Tenth, Uppsala, 1950, Proceedings. Uppsala (Sweden): Almqvist & Wiksell.

Fabricius, Eric; and Boyd, H. 1954 Experiments on the Following Reactions of Ducklings. Wildfowl Trust, Annual Report 6:84-89.

Goodwin, D. 1948 Some Abnormal Sexual Fixations in Birds. Ibis 90:45-48.

Gottlieb, Gilbert 1961a Developmental Age as a Baseline for Determination of the Critical Period in Imprinting. Journal of Comparative and Physiological Psychology 54:422-427.

Gottlieb, Gilbert 1961b The Following-response and Imprinting in Wild and Domestic Ducklings of the Same Species. Behaviour 18:205-228.

Guiton, Philip 1958 The Effect of Isolation on the Following Response of Brown Leghorn Chicks. Royal Physics Society of Edinburgh, Proceedings 27:9-14.

Guiton, Philip 1959 Socialization and Imprinting in Brown Leghorn Chicks. Animal Behavior 7:26-34.

Harlow, Harry F. 1958 The Nature of Love. American Psychologist 13:673-685.

Harlow, Harry F.; and Harlow, Margaret K. 1962 Social Deprivation in Monkeys. Scientific American 207, Nov.: 136-146.

Heinroth, Oskar; and Heinroth, Magdalena 1924-1928 Die Vaögel Mitteleuropas. 3 vols. Berlin: Bermühler.

Hess, Eckhard H. 1957 Effects of Meprobamate on Imprinting in Waterfowl. New York Academy of Sciences, Annals 67:724-732.

Hess, Eckhard H. 1959a Imprinting. Science 130:133-141.

Hess, Eckhard H. 1959b The Relationship Between Imprinting and Motivation. Volume 7, pages 44-77 in Nebraska Symposium on Motivation. Edited by Marshall R. Jones. Lincoln: Univ. of Nebraska Press.

Hess, Eckhard H. 1959c Two Conditions Limiting Critical Age for Imprinting. Journal of Comparative and Physiological Psychology 52:515—518.

Hess, Eckhard H. 1962 Imprinting and the “Critical Period” Concept. Pages 254-263 in Eugene L. Bliss (editor), Roots of Behavior. New York: Harper.

Hess, Eckhard H. 1964 Imprinting in Birds. Science 146:1128-1139.

Hess, Eckhard H.; Polt, James M.; and Goodwin, Elizabeth 1959 Effects of Carisoprodol on Early Experience and Learning. Pages 51-64 in James G. Miller (editor), The Pharmacology and Clinical Usefulness of Carisoprodol, Detroit, Mich.: Wayne State Univ. Press.

Hinde, R. A. 1955 The Following Response of Moorhens and Coots. British Journal of Animal Behaviour 3: 121-122.

Hinde, R. A.; Thorpe, W. H.; and Vince, M. A. 1956 The Following Response of Young Coots and Moorhens. Behaviour 9:214-242.

Hodge, W. H. 1946 Camels of the Clouds. National Geographic Magazine 89:641-656.

Klinghammer, Erich 1962 Imprinting in Altricial Birds: The Ring Dove Streptopelia roseogrisia and the Mourning Dove Zenaidura macruora carolensis. Ph.D. dissertation, Univ. of Chicago.

Klinghammer, Erich; and Hess, Eckhard H. 1964 Imprinting in an Altricial Bird: The Blond Ring Dove Streptopelia risoria. Science 146:265-266.

Kovach, Joseph; and Hess, Eckhard H. 1963 Imprinting: Effects of Painful Stimulation on the Following Response. Journal of Comparative and Physiological Psychology 56:461-464.

Lorenz, K. Z. 1935 Der Kumpan in der Umwelt des Vogels. Journal fiir Ornithologie 83:137-213, 289-413

Moltz, Howard 1960 Imprinting: Empirical Basis and Theoretical Significance. Psychological Bulletin 57: 291-314.

Moltz, Howard; and Stettner, L. Jay 1961 The Influence of Patterned-light Deprivation on the Critical Period for Imprinting. Journal of Comparative and Physiological Psychology 54:279-283.

Morgan, C. Lloyd 1896 Habit and Instinct. London and New York: Arnold.

Ramsay, A. O. 1951 Familial Recognition in Domestic Birds. Auk 68:1-16.

Ramsay, A. O.; and Hess, E. H. 1954 A Laboratory Approach to the Study of Imprinting. Wilson Bulletin 66:196-206.

Schaefer, Halmuth H.; and Hess, Eckhard H. 1959 Color Preferences in Imprinting Objects. Zeitschrift fur Tierpsychologie 16:161-172.

Shipley, William U. 1963 The Demonstration in the Domestic Guinea Pig of a Process Resembling Classical Imprinting. Animal Behaviour 11:470-474.

Sluckin, W. 1964 Imprinting and Early Learning. London: Methuen.

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IMPRINTING

Imprinting is the learning process through which the social preferences of animals of certain species become restricted to a particular object or class of objects. A distinction is made between filial and sexual imprinting. Filial imprinting is involved in the formation, in young animals, of an attachment to, and a preference for, the parent, parent surrogate, or siblings. Sexual imprinting is involved in the formation of mating preferences that are expressed in later life. The phenomenon of filial imprinting was described as early as 1518 by Sir Thomas More in his Utopia. However, imprinting was investigated experimentally much later, by D. A. Spalding in 1873 and by Oscar Heinroth in 1911. Konrad Lorenz, who gave the phenomenon its name, subsequently provided a detailed description of imprinting in a number of bird species in an influential work published in 1935.

Filial Imprinting

Although filial imprinting may occur in mammals (Sluckin, 1972), it has been studied mostly in precocial birds such as ducklings and chicks. These birds can move about shortly after hatching, and they approach and follow an object to which they are exposed. In a natural situation the first object the young bird encounters usually is its mother. In the absence of the mother, inanimate mother surrogates are effective in eliciting filial behavior (Bateson, 1966; Horn, 1985; Sluckin, 1972). When the chick or duckling is close to an appropriate object, it will attempt to snuggle up to it, frequently emitting soft twitters. Initially the young bird approaches a wide range of objects, though some are more attractive to it than others. After the bird has been exposed to one object long enough, it remains close to this object and may run away from novel ones. If the familiar object is removed, the bird becomes restless and emits shrill calls. When given a choice between the familiar stimulus and a novel one, the bird shows a preference for the familiar stimulus. Thus, filial imprinting refers to the acquisition of a social preference and not just an increase in following (Sluckin, 1972).

Conditions for Imprinting

To study visual imprinting in the laboratory, chicks or ducklings may be hatched in darkness and exposed for a period of one to two hours to a conspicuous object when they are about twenty-four hours old. The animals are then returned to a dark incubator and kept there until their preferences are tested by exposing them to the familiar object and a novel object. A widely used measure of filial preference is approach to the familiar object relative to approach to a novel object. Another measure takes advantage of the fact that an imprinted chick emits distress calls in the presence of a novel object and does not do so, or does so less frequently, in the presence of the familiar.

The effectiveness of imprinting stimuli varies. For example, young ducklings approach and follow objects larger than a matchbox, but peck at smaller objects. For chicks, red and blue objects are more effective imprinting stimuli than yellow and green objects. Movement, brightness, contrast, and sound all enhance the attractiveness of an imprinting stimulus.

Imprinting and Learning

Filial imprinting has been regarded as different from other forms of learning because it proceeds without any obvious reinforcement such as food or warmth (Bolhuis, De Vos, and Kruijt, 1990). However, an imprinting object may itself be a reinforcer, that is, a stimulus that an animal finds rewarding. Just as a rat learns to press a pedal to receive a reward of food, so a visually naive chick learns to press a pedal to see an imprinting object. When chicks are exposed to two imprinting stimuli simultaneously, they learn more about the individual stimuli than when they are exposed to the stimuli sequentially, or to only one stimulus. This so-called within-event learning has also been found in conditioning paradigms in rats and humans (Bolhuis and Honey, 1998). The ability to learn and remember the characteristics of objects to which an animal is exposed may be a common form of learning.

Reversibility and Sensitive Periods

Imprinting was thought to be irreversible and to occur during a sensitive period (or critical period). Numerous studies have demonstrated that filial preferences can in fact be reversed when the original object is removed and the animal is exposed to a novel object. Evidence suggests that there is a difference between the memory of the first stimulus and that of subsequent stimuli to which the animal is exposed. Under certain circumstances the preference for the first object may return (Bolhuis, 1991). The ability to form filial attachments has been shown to depend on both developmental age and time since hatching. The ability to imprint is related to the development of the animal's sensorimotor abilities. The sensitive period is brought to an end by the learning experience (imprinting) itself: Once the bird has formed a preference for a particular object, it avoids novel objects. Consequently it tends not to be exposed to them for long and so may learn little about them. When the bird is left in its cage, it may form an attachment to features of its rearing environment. Rearing the bird in a visually impoverished environment (in darkness or deprived of patterned light) extends the period during which it forms an attachment to a conspicuous object (Bateson, 1966). The sensitive period pertains to filial attachment and may relate to the link formed between the (neural) representation of the imprinted object and approach behavior. Although the formation of this link may have a sensitive period, there is no reason to suppose that the learning and recognition processes have one.

Auditory Imprinting

In the natural context auditory stimuli play an important role in the formation of filial preferences (Gottlieb, 1971). Auditory preferences may be formed in the same way as visual preferences (i.e., learning as a result of exposure). However, preferences resulting from exposure to an auditory stimulus only, whether before or after the birds have hatched, are relatively weak and short-lived. Such preferences can be strengthened when the young bird is simultaneously exposed to an auditory stimulus and a visual stimulus during auditory training, just as exposure to auditory stimuli can improve visual imprinting.

Sexual Imprinting

It might seem that one of the consequences of filial imprinting would be the determination of adult sexual preferences, but research suggests that filial imprinting and sexual imprinting are two separate (although perhaps partially overlapping) processes. Not only is the time of expression of the preferences different, but so is the period during which experience affects preferences. Sexual preferences continue to be affected by experience up to the time of mating. Furthermore, filial preferences may be formed after a relatively short period of exposure to an object. In contrast, sexual preferences develop as the result of a long period of exposure to and social interaction with the parents as well as the siblings. Normally, sexual imprinting ensures that the bird will mate with a member of its own strain or species. When the young bird is cross-fostered—that is, reared with adults of a different species—it develops a sexual preference for the foster species. In Japanese quail (Coturnix coturnix japonica) and domestic chickens (Gallus gallus domesticus), mating preferences are for individual members of the opposite sex that are different, but not too different, from individuals with which the young bird was reared (Bateson, 1978).

Predispositions

Research shows that filial preferences are formed not only as a result of learning through exposure but that they are also influenced by a specific predisposition (Bolhuis, 1991; Horn, 1985; Johnson and Bolhuis, 2000). This predisposition may be measured in the laboratory by giving chicks a choice between a rotating stuffed jungle fowl and (for instance) a rotating red box. Under some conditions the two stimuli are equally attractive. But if the young chick is given a certain amount of nonspecific experience, such as being handled and allowed to run, the chick prefers the fowl to the box when tested twenty-four hours later. In order to be effective, this nonspecific experience must occur within a sensitive period (about twenty to forty hours after hatching). It appears that the "target" stimuli of the predisposition are in the head and neck region but are not species-specific. Once the predisposition has developed, it does not function as a filter that prevents the chick from learning about objects that do not resemble conspecifics; such chicks can learn about other objects by being exposed to them. Thus, it is likely that the mechanisms underlying the predisposition and those underlying learning influence behavior independently.

Neural Mechanisms of Filial Imprinting

The neural basis of the recognition memory underlying filial imprinting has been studied most extensively in the domestic chick (Horn, 1985, 1998, 2000). When dark-reared chicks are trained by exposing them to an imprinting object for approximately one to two hours, metabolic changes occur in the dorsal part of the cerebral hemispheres. Specifically, there is an increase in the incorporation of radioactively tagged uracil into RNA in this brain region of trained chicks compared with control chicks (dark-reared chicks or chicks that have merely been exposed to overhead light). Several reasons support the idea that the biochemical changes are related to learning rather than to various side effects of training (e.g., to differences in movement, excitement, sensory stimulation between the trained chicks and their controls): when visual input is restricted to one hemisphere, incorporation of radioactive uracil into RNA is higher in the trained than in the untrained hemisphere; the amount incorporated is related to how much the chicks learn and not to various other measures of behavior; the increase is not related to short-term effects of sensory stimulation.

Neural Changes Localized to Specific Brain Regions

Imprinting leads to changes in the incorporation of radioactive uracil into RNA in a restricted brain region, the intermediate and medial part of the hyperstriatum ventrale (IMHV), a sheet of cells in the cerebral hemispheres (see Figure 1). Further evidence that the region is crucially involved in learning is the following: destruction of IMHV before training prevents imprinting; if the region is destroyed immediately after training, chicks do not prefer the training object, though for chicks with lesions of IMHV an imprinting object still elicits approach behavior but the chicks appear incapable of learning its characteristics; it is possible to bias chicks' preferences by delivering trains of short pulses of electric current to IMHV through electrodes that have been implanted into the region. At the end of the period of electrical stimulation, the chicks were shown two lights, one flashing at the rate of 4.5 per second and the other at 1.5 per second. If the IMHV region had been stimulated at 4.5 trains per second, the chicks preferred the light flashing at this frequency. In contrast, chicks that had received electrical stimulation of IMHV at the rate of 1.5 trains per second preferred the light flashing at this rate. Electrical stimulation of two visual receiving areas of the forebrain did not influence the chicks' preferences. Taken together, these results strongly suggest that the IMHV region is involved in the recognition memory of imprinting, probably storing information.

Neuronal Mechanisms of Memory

Imprinting leads to changes in the structure of synapses in IMHV, in particular to an increase in the area of thickened membrane on the postsynaptic side of certain synapses. This area of membrane is known as the postsynaptic density. The changes are restricted to synapses on the spines of dendrites (axospinous synapses) and are found in the left but not in the right IMHV. Certain spine synapses in the mammalian brain are excitatory and possess, in the postsynaptic density, receptors for the excitatory neurotransmitter l-glutamate. The increased area of the postsynaptic density of axospinous synapses seems to imply that imprinting leads to an increase in the number of receptors for l-glutamate: After chicks have been trained, there is an increase in the number of a certain type of receptors for l-glutamate in the left IMHV, but not in the right. The increased number of receptors is related to the amount the chicks have learned about the imprinting object. One consequence of this change may be that, after training, the release of a given amount of l-glutamate from a pre-synaptic ending may exert a greater excitatory action on the postsynaptic cell than before training. That is, as many hypotheses have suggested, learning leads to an increased efficacy of synaptic transmission.

The particular l-glutamate receptors shown to be affected by imprinting are those of the N-methyl-D-aspartate (NMDA) variety. In mammals, these receptors are involved in other forms of synaptic plasticity. Thus the cellular mechanisms of synaptic plasticity may be similar in diverse systems though the functions of the synaptic change may be different: In circuits involved in learning, the synaptic changes may play a part in information storage. In other systems, these changes may be a response to either physical damage or physiological dysfunction. Exposure to an imprinting stimulus for approximately two hours leads to a trebling in the proportion of neurons in IMHV responding to the imprinting stimulus compared with the proportion responding before training. Some neurons in IMHV respond in a highly selective way to the imprinted stimulus and so critically have the properties of neurons postulated by Donald Hebb (1949) as forming part of a memory trace. The increase in responsiveness does not develop linearly but, remarkably, develops in contrasting phases during and in the hours that follow training. These findings challenge models of memory based on synaptic strengthening to asymptote (Horn, Nicol, and Brown, 2001).

Cerebral Asymmetry and Imprinting

Studies in which the left or right IMHV region has been surgically damaged suggest that, in accordance with the data on synaptic changes, the left IMHV functions as a long-term store. During the first day after imprinting, however, another memory system, referred to as S', is established outside IMHV. S' is formed under the influence of the right IMHV: If this region is absent, S' is not formed. The right IMHV perhaps transfers information to S', a possibility that implies a dynamic element to memory formation. Electrophysiological evidence (Horn, Nicol, and Brown, 2001) demonstrates that imprinting leads to changes in neuronal responsiveness in the right IMHV that are similar to those in the left. These results are puzzling because various morphological and biochemical measures indicate differences in the effect of learning on the two brain regions. To reconcile these findings it has been suggested that both regions are similarly affected by learning, but that other functions of the right IMHV (e.g., in the formation of S') bring about additional structural and biochemical changes that obscure these effects (Horn, 1998). The right and left IMHV regions are not directly interconnected, so it is likely that they and S' are independent stores working in parallel. Thus, even in the case of the recognition memory of imprinting, more than one memory system is formed. Further evidence that several memory systems exist in the young chick is that chicks with lesions of IMHV (placed before S' has been formed), while being severely impaired in their ability to imprint, are nevertheless able to learn certain other tasks. Multiple memory systems therefore not only are found in mammalian brains but also may be a fundamental part of the design of the vertebrate brain.

On the basis of its connections and developmental history IMHV has been compared to the prefrontal and cingulate areas of the primate cerebral cortex (Horn, 1985). Evidence from humans suggests that these regions play an important role in the organization of memory (Janowsky, Shimamura, and Squire, 1989; Tulving et al., 1994).

See also:BIRDSONG LEARNING; GLUTAMATE RECEPTORS AND THEIR CHARACTERIZATION; REINFORCEMENT

Bibliography

Bateson, P. P. G. (1966). The characteristics and context of imprinting. Biological Reviews 41, 177-220.

—— (1978). Sexual imprinting and optimal outbreeding. Nature 273, 659-660.

Bolhuis, J. J. (1991). Mechanisms of avian imprinting: A review. Biological Reviews 66, 303-345.

Bolhuis, J. J., De Vos, G. J., and Kruijt, J. P. (1990). Filial imprinting and associative learning. Quarterly Journal of Experimental Psychology 42B, 313-329.

Bolhuis, J. J., and Honey, R. C. (1998). Imprinting, learning, and development: From behaviour to brain and back. Trends in Neurosciences 21, 306-311.

Gottlieb, G. (1971). Development of species identification in birds. Chicago: University of Chicago Press.

Heinroth, O. (1911). Beiträge zur Biologie, namentlich Ethologie und Psychologie der Anatiden. In Verhandlungen des 5, 589-702. Berlin: Internationaler Ornithologischer Kongress.

Hebb, D. O. (1949). The organization of behavior. New York: Wiley.

Horn, G. (1985). Memory, imprinting, and the brain. Oxford: Clarendon Press.

—— (1998). Visual imprinting and the neural mechanisms of recognition memory. Trends in Neurosciences 21, 300-305.

—— (2000). In memory. In J. J. Bolhuis, ed., Brain, perception, Memory: Advances in cognitive neuroscience. Oxford: Oxford University Press.

Horn, G., Nicol, A. U., and Brown, M. W. (2001). Tracking memory's trace. Proceedings of the National Academy of Sciences of the United States of America 98, 5,282-5,287.

Janowsky, J. S., Shimamura, A. P., and Squire, L. R. (1989). Source and impairment in patients with frontal lobe lesions. Neuropsychologia 27, 1,043-1,056.

Johnson, M. H., and Bolhuis, J. J. (2000). Predispositions in perceptual and cognitive development. In J. J. Bolhuis, ed., Brain, perception, memory. Advances in cognitive neuroscience. Oxford: Oxford University Press.

Lorenz, K. (1935). Der Kumpan in der Umwelt des Vogels. Journal für Ornithologie 83, 137-213, 289-413.

Sluckin, W. (1972). Imprinting and early learning. London: Methuen.

Spalding, D. A. (1873). Instinct, with original observations on young animals. Macmillan's Magazine 27, 282-293.

Tulving, E., Kapur, S., Markowitsch, H. J., Craik, F. I. M., Habib, R. and Houle, S. (1994). Neuroanatomical correlates of retrieval in episodic memory: Auditory sentence recognition. Proceedings of the National Academy of Sciences of the United States of America 91, 2,012-2,015.

Johan J.Bolhuis

G.Horn

Imprinting

Imprinting refers to the chemical modification of the DNA in some genes that affects how or whether those genes are expressed. One particular kind of DNA imprinting found in mammals is known as parental genomic imprinting, in which the sex of the parent from whom a gene is inherited determines how the gene is modified. While imprinting has been found in only about fifty human genes to date, some estimates suggest it may occur in several hundred more, in perhaps up to 1 percent of all genes. Imprinting defects are responsible for several human diseases, including some forms of cancer. Imprinting also occurs in other organisms, from yeast to plants to fruit flies.

Gene Expression in Imprinted and Nonimprinted Genes

Chromosomes, and the genes they contain, are inherited in pairs, with one copy of each supplied from each parent. For most genes, both members of the pair, called the maternal and paternal alleles, are used equally. Both are expressed (read by the transcription machinery to make protein) in roughly equal amounts.

In contrast, for most imprinted genes, only one allele is expressed, while the other copy is silenced by imprinting. For some genes it is the maternal copy, for others it is the paternal copy. This is an exception to the Mendelian assumption that the two parents contribute equally to the phenotype controlled by autosomal genes. For some genes, both alleles are expressed, but one copy is expressed much more than the other. For some genes, the silencing occurs in some tissues but not others.

Imprinted genes should not be confused with sex-linked genes, which are carried on the X or Y chromosome. Most imprinted alleles are located on autosomes , but are "stamped" with the sex of the parent that contributed them.

Imprinting should also not be confused with dominant and recessive alleles, in which one allele always controls the phenotype at the expense of the other, because of differences in the alleles themselves. The "dominance" seen in imprinting is determined by the sex of the parent contributing the allele, not any property of the allele itself. Thus, a particular allele will appear to be recessive when inherited from one parent, but dominant when inherited from the other. Such an effect, in which the expression difference is not due to the alleles but to forces acting on them from outside, is termed an "epigenetic effect."

Imprinting is thought to be responsible for many cases of incomplete penetrance, an inheritance pattern in which a dominant gene (as for a genetic disease) is not expressed in some individuals despite being present. Imprinting offers a mechanism by which a particular allele can be turned on or turned off as it is passed down through successive generations.

Timing and Mechanism of Imprinting

Although the details of imprinting are still unknown, it is clear that imprinting must occur either during the formation of the gametes or immediately after fertilization, while the two chromosome sets are still distinct. The imprint must be reliably passed on to each new daughter chromosome during DNA replication.

The exact molecular mechanism of imprinting is also unknown, but it is thought to involve the modification of a gene's promoter. The promoter is the upstream region to which RNA polymerase binds to begin transcription. Imprinting prevents or restricts binding of RNA polymerase, thus preventing gene transcription.

One method by which a gene becomes imprinted is believed to be by the addition of methyl groups (-CH₃) to cytosine nucleotides in the promoter region. The evidence for methylation is strong. Methylation is a common mechanism for gene silencing, because these bulky side groups interfere with the efficient binding of the various transcription factors required to attract the polymerase enzyme. Methylation patterns are known to be altered during gamete formation, and are reliably passed on during replication. Further evidence comes from the observation that altered methylation patterns in some imprinted genes are associated with the aberrant expression of the normally silent allele.

Example of Imprinting: The IGF2 Gene

One of the best-studied imprinted genes is the one that encodes an insulin-like growth factor called growth factor 2 (IGF2). In this gene, the paternal copy is active, whereas the maternal copy is inactive. Imagine that two parents have produced a female child. During egg formation in the mother (or shortly after fertilization), the mother's copy of the IGF2 gene is methylated , rendering it transcriptionally silent. The child uses only the paternal allele to make the growth factor. However, when this child makes her own eggs, neither copy of the gene will remain active, because the alleles will have been "restamped" as coming from a female. The active allele she used throughout life is passed on in an inactive form to her children.

The protein encoded by the IGF2 gene is a growth factor, which stimulates the growth of target cells. Failure to properly imprint the maternal allele, or inheritance of two copies of the male allele, can have important consequences. For example, the expression of two copies of the IGF2 gene is associated with Beckwith-Wiedemann syndrome, a growth disorder, accompanied by an increase in a type of cancer called Wilms tumor . Other human cancers are also associated with improper imprinting (of other genes), causing either too much or too little gene expression.

Uniparental Disomy and Human Disease

Inheritance of two copies of one parent's chromosome (or part of it) is called uniparental disomy, a type of chromosome aberration. Detection of uni-parental disomy in individuals with genetic disorders was one of the first clues that imprinting had important developmental and medical consequences.

Prader-Willi syndrome and Angelman syndrome can both be caused by uniparental disomy of chromosome 15, which carries a maternally expressed, paternally imprinted gene. Two maternal copies of the gene causes Prader-Willi syndrome, which is marked by mild mental retardation, decreased growth of the gonads , and obesity. Two paternal copies of this same gene causes Angelman syndrome, marked by severe mental retardation, small head size, seizures, inappropriate laughter, and distinctive facial features. (The gene itself codes for a protein involved in degrading other proteins.) Imprinting defects can also cause these syndromes in the absence of uniparental disomy, since the result is the same: either zero or two copies of the gene are expressed.

Why Imprint?

The evolutionary reason for imprinting is not yet clear, although some scientists propose that, at least in mammals, it arose from an evolutionary tug of war between males and females. In this scheme, fathers (who contribute only sperm) benefit when the embryo grows as fast as possible. Thus, silencing genes that slow down embryonic growth is in their interest, even if it depletes resources from the mother. Mothers, on the other hand, need to conserve their resources. Silencing genes that promote rapid growth is therefore in their interest. Supporting this hypothesis is the fact that many of the known imprinted genes regulate growth. Paternally expressed (maternally imprinted) genes such as IGF2 tend to promote growth, whereas maternally expressed (paternally imprinted) genes tend to inhibit it.

see also Chromosomal Aberrations; Fertilization; Inheritance Patterns; Methylation; RNA Polymerases.

Richard Robinson

Bibliography

Everman, David B., and Suzanne B. Cassidy. "Genomic Imprinting: Breaking the Rules." Journal of the American Academy of Child and Adolescent Psychiatry 39, no. 3 (March 2000): 386-389.

Greally, John M., and Matthew W. State. "Genomic Imprinting: The Indelible Mark of the Gamete." Journal of the American Academy of Child and Adolescent Psychiatry 39, no. 4 (April 2000): 532-535.

Paulsen, Martina, and Anne C. Ferguson-Smith. "DNA Methylation in Genomic Imprinting, Development, and Disease." Journal of Pathology 195, no. 1 (2001): 97-110.

Internet Resources

Geneimprint.com. <http://www.geneimprint.com/>.

Yale University School of Medicine and Yale-New Haven Hospital. <http://info.med.yale.edu>.

Imprinting

Definition

Genetic imprinting is the differential expression of a gene depending on whether it was maternally or paternally inherited. It is a method by which the gene expression can be silenced, and made nonfunctional. Imprinting is believed to play a critical role in fetal growth and development, but the exact purpose for imprinting has not been determined.

Description

Normal genetic imprinting process

A gene is made up of long sequences of DNA . When DNA is changed into RNA and then into protein, the processes involved are known as transcription and translation. For a gene to exert an effect on the individual's system, it has to be transcribed and translated. Some genes are constitutively (consistently) transcribed. Others are only transcribed when their products are needed.

Genetic imprinting is a natural phenomenon that does not follow the pattern of traditional Mendelian genetics. Mendelian genetics demonstrate that an individual inherits two functional copies (alleles) of every non-sex linked gene. One copy is paternally inherited, and the other is maternally inherited. When genes follow the Mendelian inheritance pattern, both the paternal and maternal copies are functionally expressed, regardless of which parent it came from. Imprinting, however, demonstrates that the expression of some genes is affected by which parent they originated from. A gene is imprinted when the expression of its activity depends on the sex of the parent that transmitted the copy of the gene. The activity of these genes is specifically regulated based on whether it is maternally or paternally marked with a signal sequence. Usually, one allele is silenced so that only one parental copy is active. The silenced copy is the imprinted copy. An imprinted gene is temporarily silenced. Genes that are silenced are not transcribed and translated, and so exert no effect on the system. There are no expression products from an imprinted gene. An individual with a maternally imprinted gene will only have expression products from the paternal allele. An individual with a paternally imprinted gene will only have expression products from the maternal allele. The result is only one functional copy of the gene that came from the parent with the normal, non-imprinted chromosome .

The imprinted chromosome was silenced during the formation of parental egg or sperm, before the offspring ever inherited it. Imprinting occurs in each generation when new egg and sperm cells are produced. A female that inherits a paternally imprinted gene will maintain the paternal imprint during the embryonic stage. However, the female will eventually form her own egg cells that may be used to reproduce. In her new egg cells (gametes), the original paternal imprint will be erased, and replaced with her own imprinted patterns. The same is true for males that inherit maternally imprinted genes. The imprinting is not permanent in that it will be erased when gametes, or sperm, are formed. This germline conversion process is regulated by the imprinting center, a piece of DNA located within the imprinted chromosome. Relatively few human genes are imprinted. Imprinted genes tend to cluster together in the same genomic regions. A maternally imprinted gene has a signal on it, often a chemical methyl group, which causes it to be silenced. Imprinted genes are referred to as "epigenetic," because the alterations that silence them do not involve actual mutations to the DNA sequence.

Genetic imprinting is a normal process that occurs in several dozen mammalian genes. It is thought to play a role in the transmission of nutrients from the mother to the fetus and to the newborn. Imprinted genes tend to impact fetal growth and the behavior of the newborn infant. Abnormalities involving imprinting patterns may result in many different diseases.

Complications in the genetic imprinting process

Multiple types of complications may arise involving imprinted genes. Normally, if there is a mutation in one of a pair of chromosomes that deletes its function, the other copy still functions and expresses a gene product. With an imprinted gene, if the one normal, functional gene is deleted or mutated, there is no back-up functionality on the imprinted chromosome. In this manner, the mutation of the normal, active copy of an imprinted gene may result in disease. Another complication may occur if, as a result of an error, cells receive all or part of a pair of chromosomes from a single parent. This is known as uniparental disomy. With imprinted genes, the cell receives either two imprinted copies or two active copies. If both copies are imprinted, there are no functional genes present.

Loss of activity and gain of inappropriate activity can both be harmful. A mutation in a gene that is imprinted may also activate the gene. This loss of imprinting leads to two active copies of a gene where neither copy is silenced. Too many active copies of a gene may result in overexpression, which can result in disease. Some types of cancer are associated with failure to imprint genes that encode for growth factors. Overexpression of these growth factors contributes to uncontrolled cell growth and the development of cancer. Environmental factors such as exposure to toxins may sometimes cause changes in DNA that alter imprinted gene expression, resulting in genetic diseases such as cancer and behavioral disorders.

Two of the best-studied diseases caused by genomic imprinting are Prader-Willi syndrome (PWS) and Angelman syndrome (AS). Both syndromes are caused by alterations in chromosome 15. Many different genes within this chromosomal region express different products based on whether they were inherited maternally or paternally. A paternally imprinted chromosome 15 with a deletion causes approximately 70% of cases of PWS. Approximately 29% of cases are caused by inheriting both maternal copies of chromosome 15, with a rare 1% involving a mutation in the imprinting center itself. All of these alterations lead to PWS, a neurobehavioral disorder characterized by excessive eating habits, obesity, short stature, mental retardation, and small hands and feet. Approximately 70% of cases of AS are caused by a deletion within the same region of chromosome 15, but on the maternal copy. Various other types of alterations cause the remaining 30%. Although AS involves the same chromosomal region, the impact of a functional paternal chromosome as opposed to a maternal chromosome, is profoundly different. Angelman syndrome is characterized by hyperactivity, an unusual facial appearance, short stature, mental retardation, spasticity, inappropriate laughter, and seizures. While PWS affects approximately one in every 10,000–15,000 live births, AS is relatively rare.

As of 2005, the National Institutes of Health (NIH) is in the process of assessing preliminary evidence that suggests assisted reproduction techniques such as in vitro fertilization (IVF) may be interfering with the imprinting process and lead to increased risk for related congenital abnormalities in offspring. These techniques may interfere with genetic processing that takes place during early embryogenesis. An increased incidence in genetic disorders involving imprinting has been found in children conceived by IVF. There may be an increased incidence of Beckwith Wiedemann syndrome (BWS), a disorder associated with overgrowth and malformations due to an imprinting defect in chromosome 11. An increase in BWS has also been reported in monozygotic twin gestations, increasing the evidence that disturbances occurring during the preimplantation stage may affect imprinting.

Resources

BOOKS

Lewin, Benjamin. Genes, Fifth Edition. Oxford: Oxford University Press, 1994.

Moore, Keith L., and T. V. N. Persaud. The Developing Human, Clinically Oriented Embryology, Seventh Edition. St. Louis, MO: Elsevier Science, 2003.

Thompson & Thompson Genetics in Medicine, Sixth Edition. St. Louis, MO: Elsevier Science, 2004.

PERIODICALS

Reik, W., and J. Walter. "Genomic Imprinting: Parental Influence on the Genome." Nature Reviews Genetics 2 2001: 21–32.

WEBSITES

Genomic Imprinting and Assisted Reproduction: Is There a Cause for Concern? NIH. (April 5, 2005.) <http://www.nichd.nih.gov/cdbpm/pp/fetalGrowth/wilkins_haug1.htm>.

Maria Basile, PhD

Imprinting

Imprinting is a term used to describe two very distinct processes. Genomic imprinting is an epigenetic chromosomal modification that describes the preferential expression of a specific parental form of a gene (allele). Imprinting is also a term used in the behavioral science to describe a learning process during which a younger animal identifies with, and adopts behaviors exhibited by, other animals, usually of the same species .

Genomic imprinting

Genomic imprinting is a normal but complex genetic phenomenon, that is difficult to define. As of March, 2003, no adequate explanation has been found for why genomic imprinting exists.

With genomic imprinting only one type of gene (allele) is expressed while the other allele remains genetically silent. Which allele is expressed and which remains silent depends on from which parent the genes are inherited.

A small subset of approximately 50 genes exhibit characteristics of genomic imprinting.

Following fertilization of a mammalian embryo most of the genes contributed by each parent begin to function equally. When a gene is expressed, the copy inherited from the mother (maternal allele), and the copy inherited from the father (paternal allele), are transcribed equally (bi-alleleic expression) and the RNA is translated into the protein product.

In contrast, with imprinting one allele is transcribed while the other is silent (i.e., imprinted). For example, in humans the insulin-like growth factor 2 gene (IGF2), which is an important fetal growth factor, is only expressed from the paternally inherited allele while the maternal allele is imprinted and never normally expressed. Similarly, the H19 gene, which is located adjacent to IGF2, is normally only expressed from the maternally inherited allele, while the paternal allele is silent.

The genetic mechanism of genomic imprinting remains uncertain but research indicates that some form of reversible genetic modification (epigenetic modification) such as DNA methylation is involved.

Impact of genomic imprinting

In most cases genomic imprinting is a normal process and has no affect on the normal individual . However, imprinted genes are involved in the development of some genetic disorders and in cancer .

Imprinted genes are involved in the development of some cancers. The imprinted fetal growth factor gene, IGF2, is commonly expressed in cancers such as Wilms tumor of the kidney, and cancers of the breast, lung, liver, and colon. In these cancers the maternal IGF2 imprint has been lost and both gene alleles are expressed (bi-allelic expression), this is termed "relaxation of imprinting."

There are many theories for why genomic imprinting exists. One of the most favored (in accord with the most current data), proposed by David Haig (the Haig Hypothesis), suggests that imprinting is a form of genetic reproductive conflict between the sexes each vying for a different reproductive outcome. Males desire large offspring males, so they over-express growth factors such as the paternally expressed fetal growth factor IGF2. However, females needing to limit fetal growth to ensure their successful birth have repressed growth factor expression by imprinting the gene.

Behavioral imprinting

With behavioral imprinting—a form of which is termed parental imprinting—a newly hatched or newborn animal is able to recognize its own parents from among other individuals of the same species. This process helps to ensure that the young will not become separated from their parents, even among large flocks or herds of similar animals.

Imprinting occurs during a sensitive period shortly after hatching, corresponding to a time when the chicks are near the nest and unlikely to encounter adults other than their parents. Many behavioral scientists assert that once an animal has imprinted on an object, it is never forgotten and the animal cannot imprint on any other object. Thus even when the chicks begin to encounter other animals they remain with their parents.

Imprinting was first studied in depth by Austrian zoologist Konrad Lorenz (1903–1989), who observed the process in ducks and geese . Lorenz found that a chick will learn to follow the first conspicuous moving object it sees after hatching. Normally, this object would be the mother bird, but in various experiments, ducklings and goslings have imprinted on artificial models of birds , bright red balls, and even human beings. In 1973, Lorenz's work earned a share of the Nobel Prize for Physiology and Medicine.

The effects of the imprinting process carry over into the adult life of the animal as well. In many cases it has been shown that the object imprinted upon as a hatchling determines the mating and courtship behaviors of the adult. Many species will avoid social contact with animals dissimilar to the one to which they have imprinted. Under normal circumstances, this helps prevent breeding between different species. Under artificial conditions, an animal which has imprinted on an individual of a different species will often attempt to court a member of that species later in life.

Imprinting in animals is most thoroughly studied in birds, although it is believed to be especially important in the hoofed mammals , which tend to congregate in large herds in which a young animal could easily be separated from its mother. Imprinting also occurs in humans to at least some extent. An infant separated from its mother for a prolonged period during its first year may develop serious mental retardation. Irreparable damage and even death may result from a separation of several months.

See also Behavior; Genetics.