Elsevier

Neuroscience

Volume 162, Issue 4, 15 September 2009, Pages 881-891
Neuroscience

Behavioural Neuroscience
Research Paper
Interest in infants by female rhesus monkeys with neonatal lesions of the amygdala or hippocampus

https://doi.org/10.1016/j.neuroscience.2009.05.056Get rights and content

Abstract

Previous research in our laboratory has shown that damage to the amygdala in neonatal rhesus monkeys profoundly alters behaviors associated with fear processing, while leaving many aspects of social development intact. Little is known, however, about the impact of neonatal lesions of the amygdala on later developing aspects of social behavior. A well-defined phenomenon in the development of young female rhesus monkeys is an intense interest in infants that is typically characterized by initiating proximity or attempting to hold them. The extent to which young females are interested in infants may have important consequences for the development of species-typical maternal behavior. Here we report the results of a study that was designed to assess interest in infants by female rhesus monkeys that received neonatal lesions to the amygdala, hippocampus or a sham surgical procedure. Subjects were first paired with pregnant “stimulus” females to assess social interactions with them prior to the birth of the infants. There were few behavioral differences between lesion groups when interacting with the pregnant females. However, following the birth of the infants, the amygdala-lesioned females showed significantly less interest in the infants than did control or hippocampus-lesioned females. They directed fewer affiliative vocalizations and facial expressions to the mother–infant pair compared to the hippocampus-lesioned and control females. These findings suggest that neonatal damage to the amygdala, but not the hippocampus, impairs important precursors of non-human primate maternal behavior.

Section snippets

Experimental procedures

All experimental procedures were carried out in accordance with the National Institutes of Health Guide for the Care and Use of Laboratory Animals and developed through consultation with the veterinary staff at the California National Primate Research Center (CNPRC). All protocols were also approved by the University of California, Davis, Institutional Animal Care and Use Committee. Group sizes chosen represent the minimum required to achieve adequate statistical power. All efforts were made to

MRI and histological evaluation of lesions

T2-weighted images of coronal sections are illustrated in previous publications, providing substantial reassurance that the ibotenic acid was injected and was focused in the amygdaloid complex or hippocampal formation (Bauman et al 2004a, Bauman et al 2004b). The extent of the targeted lesion was confirmed in one amygdala-lesioned subject that died due to an unrelated illness and whose brain was subjected to histological evaluation of the lesion (see Fig. 2 in Bauman et al., 2004b). Analysis of

Discussion

The present study provides evidence that monkeys that received lesions to the amygdala in early infancy displayed significantly decreased species-typical interest in infants, as compared to monkeys that received lesions to the hippocampus or a control sham surgical procedure. Lesion groups differed very little in their reactions to the stimulus females prior to the birth of the infant. There were few differences between groups for the majority of behavioral measures assessed during the

Conclusion

In sum, rhesus female monkeys that sustained amygdala lesions as neonates, but not those with neonatal lesions to the hippocampus, demonstrate less species-typical interest in infants of other mothers later in life. Positioning this work within a broader picture of amygdala function is an experimental challenge for the future. One of the hallmark findings in lesion work in non-human primates and rodents is that removal of the amygdala compromises fear processing. In the present study, however,

Acknowledgments

This research was supported by a grant from the National Institute of Mental Health (R37MH57502) and by the base grant of the CNPRC (RR00169). This work was also supported through the Early Experience and Brain Development Network of the Macarthur Foundation. We thank the veterinary and husbandry staff of the CNPRC for excellent care of the animal subjects. We also thank Jeffrey Bennett and Pamela Tennant for assistance with surgical procedures, Melissa Marcucci for assistance with behavioral

References (45)

  • J.B. Silk

    Why are infants so attractive to others?The form and function of infant handling in bonnet macaques

    Anim Behav

    (1999)
  • K. Slater et al.

    Embraces for infant handling in spider monkeys: evidence for a biological market?

    Anim Behav

    (2007)
  • Y. Spencer-Booth

    The behaviour of group companions towards rhesus monkey infants

    Anim Behav

    (1968)
  • H.D. Steklis et al.

    Neurobiology of affiliative behavior in nonhuman primates

  • K. Wallen

    Hormonal influences on sexually differentiated behavior in nonhuman primates

    Front Neuroendocrinol

    (2005)
  • R. Adolphs et al.

    Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala

    Nature

    (1994)
  • D.G. Amaral et al.

    The amygdala and autism: implications from non-human primate studies

    Genes Brain Behav

    (2003)
  • M.D. Bauman et al.

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

    J Neurosci

    (2004)
  • M.D. Bauman et al.

    The development of social behavior following neonatal amygdala lesions in rhesus monkeys

    J Cogn Neurosci

    (2004)
  • M.D. Bauman et al.

    Emergence of stereotypies in juvenile monkeys (Macaca mulatta) with neonatal amygdala or hippocampus lesions

    Behav Neurosci

    (2008)
  • M.D. Bauman et al.

    The expression of social dominance following neonatal lesions of the amygdala or hippocampus in rhesus monkeys (Macaca mulatta)

    Behav Neurosci

    (2006)
  • R.S. Bridges et al.

    Hypothalamic involvement in the regulation of maternal behaviour in the rat: inhibitory roles for the ventromedial hypothalamus and the dorsal/anterior hypothalamic areas

    J Neuroendocrinol

    (1999)
  • Cited by (0)

    View full text