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The Journal of Neuroscience, January 21, 2004, 24(3):711-721; doi:10.1523/JNEUROSCI.3263-03.2004

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Development/Plasticity/Repair
The Development of Mother-Infant Interactions after Neonatal Amygdala Lesions in Rhesus Monkeys

M. D. Bauman,^1,3 P. Lavenex,^1,3 W. A. Mason,^2,3 J. P. Capitanio,^2,3 and D. G. Amaral^1,3,4

¹Department of Psychiatry and Behavioral Sciences, and Center for Neuroscience, ²Department of Psychology, ³California National Primate Research Center, and ⁴The Medical Investigation of Neurodevelopmental Disorders Institute, University of California at Davis, Davis, California 95616

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.

Key words: amygdaloid complex; social behavior; filial bond; fear; hippocampus; macaque monkey

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Received July 9, 2003; revised October 20, 2003; accepted November 19, 2003.

This article has been cited by other articles:

				G. G. Berntson, A. Bechara, H. Damasio, D. Tranel, and J. T. Cacioppo Amygdala contribution to selective dimensions of emotion Soc Cogn Affect Neurosci, June 1, 2007; 2(2): 123 - 129. [Abstract] [Full Text] [PDF]

				P. Lavenex and P. B. Lavenex Spatial relational memory in 9-month-old macaque monkeys Learn. Mem., January 1, 2006; 13(1): 84 - 96. [Abstract] [Full Text] [PDF]

				M. D. Bauman, P. Lavenex, W. A. Mason, J. P. Capitanio, and D. G. Amaral The Development of Social Behavior Following Neonatal Amygdala Lesions in Rhesus Monkeys J. Cogn. Neurosci., September 1, 2004; 16(8): 1388 - 1411. [Abstract] [Full Text] [PDF]

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