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WIREs Cogn Sci
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Imprinting

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Abstract Imprinting is a type of learning by which an animal restricts its social preferences to an object after exposure to that object. Filial imprinting occurs shortly after birth or hatching and sexual imprinting, around the onset of sexual maturity; both have sensitive periods. This review is concerned mainly with filial imprinting. Filial imprinting in the domestic chick is an effective experimental system for investigating mechanisms underlying learning and memory. Extensive evidence implicates a restricted part of the chick forebrain, the intermediate and medial mesopallium (IMM), as a memory store for visual imprinting. After imprinting to a visual stimulus, neuronal responsiveness in IMM is specifically biased toward the imprinting stimulus. Both this bias and the strength of imprinting measured behaviorally depend on uninterrupted sleep shortly after training. When learning‐related changes in IMM are lateralized they occur predominantly or completely on the left side. Ablation experiments indicate that the left IMM is responsible for long‐term storage of information about the imprinting stimulus; the right side is also a store but additionally is necessary for extra storage outside IMM, in a region necessary for flexible use of information acquired through imprinting. Auditory imprinting gives rise to biochemical, neuroanatomical, and electrophysiological changes in the medio‐rostral nidopallium/mesopallium, anterior to IMM. Auditory imprinting has not been shown to produce learning‐related changes in IMM. Imprinting may be facilitated by predispositions. Similar predispositions for faces and biological motion occur in domestic chicks and human infants. WIREs Cogn Sci 2013, 4:375–390. doi: 10.1002/wcs.1231 This article is categorized under: Psychology > Memory Psychology > Learning Neuroscience > Behavior

Plot illustrating learning‐relatedness of a physiological measurement in the brain after imprinting. The number of Fos‐positive nuclei (square root‐ transformed to normalize the data) are plotted against preference score, a measure of preference for the imprinting stimulus and thus of the strength of imprinting/learning. Nuclei were counted in a standard sampling frame placed over the IMM region in histological sections. Each point represents data from one chick. The least squares regression line has been fitted. The lower horizontal dashed line estimates the value of the ordinate corresponding to the ‘no preference’ score of 50 (characteristic of chicks showing no learning). This estimate was not significantly different from the mean value for untrained chicks, which is represented by the open circle (the error bars represent ±1 SEM, n = 16). The upper horizontal dashed line gives the estimated value of the ordinate corresponding to the maximum preference score attained in the experiment (characteristic of strongly imprinted chicks). This estimate was significantly greater than the mean value for untrained chicks. The estimates shown by the horizontal dashed lines are based on interpolation of the regression line. The thick bars on the Y axis depict ± one standard error of each estimated value. (Reprinted with permission from Ref . Copyright 1988 National Academy of Sciences)

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Experiment demonstrating the mediational function of region S′ in the chick brain. On Day 1, all chicks received a total of 100 presentations of imprinting stimulus A and 100 presentations of imprinting stimulus B during two 53‐min sessions of imprinting training. In the Mixed training condition, both sessions contained 50 presentations of each of the stimuli, A and B, in a quasi‐random order. For chicks in the Separate training condition, one session contained 100 presentations of A and the remaining session contained 100 presentations of B. For half of these chicks, A was presented in Session 1 and B in Session 2; for the remaining chicks, B was presented in Session 1 and A in Session 2. Chicks then received lesions, either unilaterally in the right IMM ≤1 h after training (Group R‐IMM, preventing storage in S′) or bilaterally in the IMM 4–6 h after training (Group Bil‐IMM, allowing storage in S′). On the next day, all chicks received visual discrimination training in which they were rewarded for approaching stimulus A. Chicks in Group Bil‐IMM receiving Mixed training (framed) learned the discrimination significantly slower than the other three groups, whose acquisition rates did not differ significantly from each other. Thus, learning during the Mixed training session impaired subsequent discrimination learning if S′ remained intact. This impairment was interpreted as S′ mediating the classification together of A and B following Mixed training and thereby interfering with the acquisition of a discrimination between A and B. (Reprinted with permission from Ref . Copyright 1995 American Psychological Association)

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Summary of the results of experiments in which the IMM was ablated either unilaterally or bilaterally after imprinting training. Lesions in the IMM are represented as oval shaded areas and the left and right forebrain hemispheres are denoted by ‘L’ and ‘R’, respectively. ‘Result 1’ gives the result of a preference test following IMM ablation under general anaesthesia ≤3 h after training. ‘Result 2’ is derived from a preference test after ablation under general anaesthesia ∼24 h after training. (a) Bilateral ablation of the IMM ≤3 h after training results in amnesia for the imprinting stimulus. (b) Ablation of first the right IMM and then the left IMM gives amnesia after the second lesion. (c) In contrast, ablation of the left and right IMM in the reverse order results in retention of the preference acquired through imprinting. (d) If both the left and the right IMM are intact for ∼24 h after training, the preference acquired through imprinting is retained after subsequent ablation. In summary, if the right IMM is intact for a sufficient time after training, storage of information about the imprinting stimulus occurs outside the IMM, in a region termed S′. If the right IMM is lesioned ≤3 h after training, retention is dependent on the remaining left IMM and there is no evidence of S′ being functional.

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(a) Mean proportions of neurons ± SEM in the IMM of domestic chicks that were responsive to a visual imprinting stimulus (IS—a red box), plotted against time since the start of the experiment. Chicks were exposed to the IS for two 1‐h periods, denoted by Train1 and Train2. Neuronal responsiveness to the IS was tested by neuronal tests NT1–NT4. Chicks remained in running wheels throughout the experiment. Filled squares represent data from chicks (Rest‐First group) that were allowed to rest in darkness during the 6‐h period labeled ‘Session 1’. Open circles represent data from chicks (Disturbed‐First group) that were prevented from sleeping continuously during Session 1 by a single revolution of the running wheel (duration one minute) delivered at random every 30 min during Session 1. During Session 2, which was also 6 h in duration, the Rest‐First chicks were disturbed as described above and the Disturbed‐First chicks were allowed to rest. At test NT4, neuronal responsiveness to the IS in the Rest‐First group had risen significantly to a maximum value that was significantly higher than neuronal responsiveness to the IS in the Disturbed‐First group; in this latter group, the responsiveness had collapsed at NT4. The high level of responsiveness in the Rest‐First group was due to the fact that this group was rested during Session 1 rather than disturbed during Session 2, since a high level of responsiveness at NT4 was also found if chicks were rested during Session 2. (b) Neuronal responsiveness to a novel stimulus (a blue cylinder) in the Rest‐First and Disturbed‐First groups that contributed data to panel A. In both groups, only approximately 10% of neurons in the IMM responded to the imprinting stimulus during all of the neuronal tests NT1–NT4. (c) Mean preference scores ± SEM for the Rest‐First and Disturbed‐First chicks measured at the end of the experiment. The Rest‐First chicks had a preference score significantly (P = 0.03) greater than 50, indicating that they had become imprinted. In contrast, the Disturbed‐First chicks had a mean preference score that was not significantly different from the ‘no preference’ level of 50. Disturbance during Session 1, as well as causing a drastic reduction of neuronal responsiveness to the imprinting stimulus at NT4 (panel A, filled squares), also reduced the mean preference score to a level at which no evidence of memory for the imprinting stimulus remained. (Reprinted with permission from Ref . Copyright 2008 Elsevier)

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Summary of learning‐related biochemical changes in the IMM and the times after the end of imprinting training at which they were detected. In some cases the changes were lateralized and when this was the case, the learning‐related effect was always stronger in the left IMM. An effect is reported as lateralized if either (1) there was a significant interaction between the side of the IMM and strength of learning (measured either by regression of the biochemical change on preference score, or by a difference between good and poor learners); or (2) there was a significant effect of training on one side of the IMM but not on the other.

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