The development of mother-infant interactions after neonatal amygdala lesions in rhesus monkeys

Abstract

As part of ongoing studies on the neurobiology of socioemotional behavior in the nonhuman primate, we examined the development of mother-infant interactions in 24 macaque monkeys who received either bilateral amygdala or hippocampus ibotenic acid lesions, or a sham surgical procedure at 2 weeks of age. After surgery, the infants were returned to their mothers and reared with daily access to small social groups. Behavioral observations of the infants in dyads (mother-infant pairs alone), tetrads (two mother-infant pairs), and social groups (six mother-infant pairs and one adult male) revealed species-typical mother-infant interactions for all lesion conditions, with the exception of increased physical contact time between the amygdala-lesioned infants and their mothers. Immediately after permanent separation from their mothers at 6 months of age, the infants were tested in a mother preference test that allowed the infants to choose between their mother and another familiar adult female. Unlike control and hippocampus-lesioned infants, the amygdala-lesioned infants did not preferentially seek proximity to their mother, nor did they produce distress vocalizations. Given the normal development of mother-infant interactions observed before weaning, we attribute the behavior of the amygdala-lesioned infants during the preference test to an impaired ability to perceive potential danger (i.e., separation from their mother in a novel environment), rather than to a disruption of the mother-infant relationship. These results are consistent with the view that the amygdala is not essential for fundamental aspects of social behavior but is necessary to evaluate potentially dangerous situations and to coordinate appropriate behavioral responses.

Figure 1.

Schematic representations of the experimental test cages. a, Test cage used for dyadic, tetradic, and group observations (2.13 × 3.35 × 2.44 m). b, Novel test cage used for the mother preference test (5.56 × 1.91 × 2.13 m). Holding cages for the mother and the stimulus female are shown in solid gray. The arrow indicates the position of the portable infant release box placed in the center of the cage at the onset of each trial.

Figure 2.

T2-weighted MR images of sections through the amygdala from infants that received injections of IBO 10 d earlier. Overlaid outlines represent the approximate boundary of the amygdaloid complex. The T2-hyperintense signal was used to confirm that IBO was injected and that the lesion target (amygdala or hippocampus) was in the central region of the edema. a, T2-weighted MR image of the same subject from which the Nissl-stained sections shown in Figure 3 is taken.

Figure 5.

Amygdala-lesioned infants failed to demonstrate a species-typical preference for their mother after separation from their mother, as indicated by measure of proximity duration, distance, and distress responses. a, Bars represent the average time ± SEM (per 120 sec trial) spent in a 1 m semicircle “proximity zone” in front of the holding cages that contain either their mother (M) or the stimulus female (S). Proximity duration was scored only when the infant stayed within the proximity zone for at least 3 consecutive seconds. Asterisks denote significant paired t tests (p < 0.05). b, Bars represent the average distance from the mother (meters) ± SEM. Spacing data were collected every 15 sec during the 120 sec trial, noting the location of the infant on a 27 quadrant floor grid. Asterisks denote significant post hoc Fisher's PLSD tests (significance set at p < 0.05). c, Bars represent the average scream frequency ± SEM per 120 sec trial. The frequency of scream data were not normally distributed and contained a number of zero values. Therefore, a ln(scream + 1) transformation was used. For display purposes, the nontransformed scream data are shown. Asterisks denote significant post hoc Fisher's PLSD tests (significance set at p < 0.05).

Figure 3.

Nissl-stained coronal sections through two levels in an amygdala-lesioned subject's anterior temporal lobe. The amygdala in this subject was substantially damaged, whereas adjacent structures, including the entorhinal cortex, were primarily intact. a, Rostral level showing an expanded ventricle and substantial amygdala damage on the right side and cell damage to the rostral portion of the amygdala on the left side. The asterisk indicates sparing in the medial portion of the accessory basal nucleus and the periamygdaloid cortex. b, Caudal level of the amygdala showing expanded ventricle and nearly complete cell loss on the right side and substantial cell damage on the left side. The asterisk indicates sparing in a small, ventomedial medial portion of the parvicellular division of the basal nucleus on the left side.

Figure 4.

Amygdala-lesioned infants do not differ from controls during dyads (one mother-infant pair) but do spend significantly more time in contact with their mothers than both controls and hippocampus-lesioned infants during tetrads (two mother-infant pairs) and social group interaction (six mother-infant pairs plus one adult male). Each bar represents the average percentage of time ± SEM (per 300 sec observation period) spent in physical contact with their mothers. Asterisks denote significant post hoc Fisher's PLSD tests (p < 0.05).

Figure 6.

Amygdala-lesioned infants are capable of visually identifying their mother, as indicated by their preference to approach their mother (M) as opposed to the stimulus female (S). a, Bars represent the group average for the number of first approaches ± SEM (scored when an infant moves into the proximity zone within the first 15 sec of the trial) of twenty trials. Asterisks denote significant one-tailed paired t tests (p < 0.05). b, Bars represent the group average frequency of approaches ± SEM per 120 sec trial. Asterisks denote significant one-tailed paired t tests (p < 0.05)