Adult Social Behavior With Familiar Partners Following Neonatal Amygdala or Hippocampus Damage

Behavioral Neuroscience

Volumn 129, Issue 3, 2015, Pages 339-350

  Moadab, Gilda ^a   Bliss Moreau, Eliza ^a   Amaral, David G ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Amygdala; Hippocampus; Macaca mulatta; Nonhuman primate; Social behavior

Indexed keywords

ADULT; AGGRESSION; AMYGDALOID NUCLEUS; ANIMAL BEHAVIOR; ANIMAL COMMUNICATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY; ARTICLE; BEHAVIORAL STRESS; BRAIN DAMAGE; CONTROLLED STUDY; EXPLORATORY BEHAVIOR; FEMALE; GROOMING; HIPPOCAMPUS; INFANT; MALE; NEWBORN; NONHUMAN; RHESUS MONKEY; SEXUAL BEHAVIOR; SLEEP QUALITY; SOCIAL BEHAVIOR; SOCIAL INTERACTION; STEREOTYPY; AMYGDALA; ANIMAL; ANIMAL HOUSING; COHORT ANALYSIS; GROWTH, DEVELOPMENT AND AGING; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; RECOGNITION; SLEEP; TIME FACTOR;

IBOTENIC ACID;

AMYGDALA; ANIMALS; ANIMALS, NEWBORN; ANXIETY; BEHAVIOR, ANIMAL; COHORT STUDIES; EXPLORATORY BEHAVIOR; FEMALE; HIPPOCAMPUS; HOUSING, ANIMAL; IBOTENIC ACID; MACACA MULATTA; MAGNETIC RESONANCE IMAGING; MALE; RECOGNITION (PSYCHOLOGY); SLEEP; SOCIAL BEHAVIOR; TIME FACTORS;

EID: 84930401709     PISSN: 07357044     EISSN: 19390084     Source Type: Journal    
DOI: 10.1037/bne0000062     Document Type: Article

References (52)

1. Altmann, J. (1974). Observational study of behavior: Sampling methods. Behaviour, 49, 227-267. http://dx.doi.org/10.1163/156853974X00534
2. Amaral, D. G. (2003). The amygdala, social behavior, and danger detection. Annals of the New York Academy of Sciences, 1000, 337-347. http://dx.doi.org/10.1196/annals.1280.015
3. Bachevalier, J., Alvarado, M. C., Malkova, L. (1999). Memory and socioemotional behavior in monkeys after hippocampal damage incurred in infancy or in adulthood. Biological Psychiatry, 46, 329-339. http://dx.doi.org/10.1016/S0006-3223(99)00123-7
4. Bachevalier, J., Beauregard, M., Alvarado, M. C. (1999). Long-term effects of neonatal damage to the hippocampal formation and amygdaloid complex on object discrimination and object recognition in rhesus monkeys (Macaca mulatta). Behavioral Neuroscience, 113, 1127-1151. http://dx.doi.org/10.1037/0735-7044.113.6.1127
5. Bachevalier, J., Málková, L., Mishkin, M. (2001). Effects of selective neonatal temporal lobe lesions on socioemotional behavior in infant rhesus monkeys (Macaca mulatta). Behavioral Neuroscience, 115, 545- 559. http://dx.doi.org/10.1037/0735-7044.115.3.545
6. Banta Lavenex, P., Amaral, D. G., Lavenex, P. (2006). Hippocampal lesion prevents spatial relational learning in adult macaque monkeys. The Journal of Neuroscience, 26, 4546-4558. http://dx.doi.org/10.1523/JNEUROSCI.5412-05.2006
7. Bauman, M. D., Lavenex, P., Mason, W. A., Capitanio, J. P., Amaral, D. G. (2004a). The development of mother-infant interactions after neonatal amygdala lesions in rhesus monkeys. The Journal of Neuroscience, 24, 711-721. http://dx.doi.org/10.1523/JNEUROSCI.3263-03.2004
8. Bauman, M. D., Lavenex, P., Mason, W. A., Capitanio, J. P., Amaral, D. G. (2004b). The development of social behavior following neonatal amygdala lesions in rhesus monkeys. Journal of Cognitive Neuroscience, 16, 1388-1411.
9. Bauman, M. D., Toscano, J. E., Babineau, B. A., Mason, W. A., Amaral, D. G. (2008). Emergence of stereotypies in juvenile monkeys (Macaca mulatta) with neonatal amygdala or hippocampus lesions. Behavioral Neuroscience, 122, 1005-1015. http://dx.doi.org/10.1037/a0012600
10. Bauman, M. D., Toscano, J. E., Mason, W. A., Lavenex, P., Amaral, D. G. (2006). The expression of social dominance following neonatal lesions of the amygdala or hippocampus in rhesus monkeys (Macaca mulatta). Behavioral Neuroscience, 120, 749-760. http://dx.doi.org/10.1037/0735-7044.120.4.749
11. Beauregard, M., Malkova, L., Bachevalier, J. (1995). Stereotypies and loss of social affiliation after early hippocampectomy in primates. NeuroReport, 6, 2521-2526. http://dx.doi.org/10.1097/00001756-199512150-00018
12. Bliss-Moreau, E., Bauman, M. D., Amaral, D. G. (2011). Neonatal amygdala lesions result in globally blunted affect in adult rhesus macaques. Behavioral Neuroscience, 125, 848 - 858. http://dx.doi.org/10.1037/a0025757
13. Bliss-Moreau, E., Moadab, G., Bauman, M. D., Amaral, D. G. (2013). The impact of early amygdala damage on juvenile rhesus macaque social behavior. Journal of Cognitive Neuroscience, 25, 2124-2140.
14. Bliss-Moreau, E., Toscano, J. E., Bauman, M. D., Mason, W. A., Amaral, D. G. (2010). Neonatal amygdala or hippocampus lesions influence responsiveness to objects. Developmental Psychobiology, 52, 487-503. http://dx.doi.org/10.1002/dev.20451
15. Bliss-Moreau, E., Toscano, J. E., Bauman, M. D., Mason, W. A., Amaral, D. G. (2011). Neonatal amygdala lesions alter responsiveness to objects in juvenile macaques. Neuroscience, 178, 123-132. http://dx.doi.org/10.1016/j.neuroscience.2010.12.038
16. Brown, S., Schafer, E. A. (1888). An investigation into the functions of the occipital and temporal lobes of the monkey's brain. Philosophical Transactions of the Royal Society of London, 179, 303-327. http://dx.doi.org/10.1098/rstb.1888.0011
17. Emery, N. J., Capitanio, J. P., Mason, W. A., Machado, C. J., Mendoza, S. P., Amaral, D. G. (2001). The effects of bilateral lesions of the amygdala on dyadic social interactions in rhesus monkeys (Macaca mulatta). Behavioral Neuroscience, 115, 515-544.
18. Goursaud, A. P., Bachevalier, J. (2007). Social attachment in juvenile monkeys with neonatal lesion of the hippocampus, amygdala and orbital frontal cortex. Behavioural Brain Research, 176, 75-93. http://dx.doi.org/10.1016/j.bbr.2006.09.020
19. Goursaud, A. P., Wallen, K., Bachevalier, J. (2014). Mother recognition and preference after neonatal amygdala lesions in rhesus macaques (Macaca mulatta) raised in a semi-naturalistic environment. Developmental Psychobiology, 56, 1723-1734. http://dx.doi.org/10.1002/dev.21233
20. Heuer, E., Bachevalier, J. (2011). Neonatal hippocampal lesions in rhesus macaques alter the monitoring, but not maintenance, of information in working memory. Behavioral Neuroscience, 125, 859 - 870. http://dx.doi.org/10.1037/a0025541
21. Izquierdo, A., Suda, R. K., Murray, E. A. (2005). Comparison of the effects of bilateral orbital prefrontal cortex lesions and amygdala lesions on emotional responses in rhesus monkeys. The Journal of Neuroscience, 25, 8534-8542. http://dx.doi.org/10.1523/JNEUROSCI.1232-05.2005
22. Kling, A. (1968). Effects of amygdalectomy and testosterone on sexual behavior of male juvenile macaques. Journal of Comparative and Physiological Psychology, 65, 466-471. http://dx.doi.org/10.1037/h0025804
23. Kling, A. (1974). Differential effects of amygdalectomy in male and female nonhuman primates. Archives of Sexual Behavior, 3, 129-134. http://dx.doi.org/10.1007/BF01540996
24. Kling, A., Cornell, R. (1971). Amygdalectomy and social behavior in the caged stump-tailed macaque (Macaca speciosa). Folia Primatologica, 14, 190-208. http://dx.doi.org/10.1159/000155350
25. Kling, A., Lancaster, J., Benitone, J. (1970). Amygdalectomy in the free-ranging vervet (Cercopithecus aethiops). Journal of Psychiatric Research, 7, 191-199. http://dx.doi.org/10.1016/0022-3956(70)90006-3
26. Klüver, H., Bucy, P. C. (1939). Preliminary analysis of functions of the temporal loves in monkeys. Archives of Neurology & Psychiatry, 42, 979 -1000. http://dx.doi.org/10.1001/archneurpsyc.1939.02270240017001
27. Lavenex, P., Banta Lavenex, P., Amaral, D. G. (2007). Spatial relational learning persists following neonatal hippocampal lesions in macaque monkeys. Nature Neuroscience, 10, 234-239. http://dx.doi.org/10.1038/nn1820
28. Leuner, B., Gould, E. (2010). Structural plasticity and hippocampal function. Annual Review of Psychology, 61, 111-140. http://dx.doi.org/10.1146/annurev.psych.093008.100359
29. Machado, C. J., Bachevalier, J. (2006). The impact of selective amygdala, orbital frontal cortex, or hippocampal formation lesions on established social relationships in rhesus monkeys (Macaca mulatta). Behavioral Neuroscience, 120, 761-786. http://dx.doi.org/10.1037/0735-7044.120.4.761
30. Machado, C. J., Emery, N. J., Capitanio, J. P., Mason, W. A., Mendoza, S. P., Amaral, D. G. (2008). Bilateral neurotoxic amygdala lesions in rhesus monkeys (Macaca mulatta): Consistent pattern of behavior across different social contexts. Behavioral Neuroscience, 122, 251-266. http://dx.doi.org/10.1037/0735-7044.122.2.251
31. Machado, C. J., Snyder, A. Z., Cherry, S. R., Lavenex, P., Amaral, D. G. (2008). Effects of neonatal amygdala or hippocampus lesions on resting brain metabolism in the macaque monkey: A microPET imaging study. NeuroImage, 39, 832-846. http://dx.doi.org/10.1016/j.neuroimage.2007.09.029
32. Málková, L., Mishkin, M., Suomi, S. J., Bachevalier, J. (2010). Longterm effects of neonatal medial temporal ablations on socioemotional behavior in monkeys (Macaca mulatta). Behavioral Neuroscience, 124, 742-760. http://dx.doi.org/10.1037/a0021622
33. Mason, W. A., Capitanio, J. P., Machado, C. J., Mendoza, S. P., Amaral, D. G. (2006). Amygdalectomy and responsiveness to novelty in rhesus monkeys (Macaca mulatta): Generality and individual consistency of effects. Emotion, 6, 73-81. http://dx.doi.org/10.1037/1528-3542.6.1.73
34. Meunier, M., Nalwa, V., Bachevalier, J. (2003). Reactions to familiar and novel objects in infant monkeys with neonatal temporal lesions. Hippocampus, 13, 489-493. http://dx.doi.org/10.1002/hipo.10143
35. Mirsky, A. F. (1960). Studies of the effects of brain lesions on social behavior in Macaca mulatta: Methodological and theoretical considerations. Annals of the New York Academy of Sciences, 85, 785-794. http://dx.doi.org/10.1111/j.1749-6632.1960.tb50000.x
36. Moadab, G., Bliss-Moreau, E., Bauman, M. D., Amaral, D. G. (2015). Early amygdala or hippocampus damage impacts social behavior at the transition to sexual maturity. Manuscript submitted for publication.
37. Noldus, L. P. J. J. (1991). The observer: A software system for collection and analysis of observational data. Behavior Research Methods, Instruments & Computers, 23, 415-429.
38. Raper, J., Bachevalier, J., Wallen, K., Sanchez, M. (2013). Neonatal amygdala lesions alter basal cortisol levels in infant rhesus monkeys. Psychoneuroendocrinology, 38, 818-829. http://dx.doi.org/10.1016/j.psyneuen.2012.09.004
39. Raper, J., Stephens, S. B., Henry, A., Villarreal, T., Bachevalier, J., Wallen, K., Sanchez, M. M. (2014). Neonatal amygdala lesions lead to increased activity of brain CRF systems and hypothalamic-pituitaryadrenal axis of juvenile rhesus monkeys. The Journal of Neuroscience, 34, 11452-11460. http://dx.doi.org/10.1523/JNEUROSCI.0269-14.2014
40. Raper, J., Stephens, S. B., Sanchez, M., Bachevalier, J., Wallen, K. (2014). Neonatal amygdala lesions alter mother-infant interactions in rhesus monkeys living in a species-typical social environment. Developmental Psychobiology, 56, 1711-1722. http://dx.doi.org/10.1002/dev.21234
41. Raper, J., Wallen, K., Sanchez, M. M., Stephens, S. B., Henry, A., Villareal, T., Bachevalier, J. (2013). Sex-dependent role of the amygdala in the development of emotional and neuroendocrine reactivity to threatening stimuli in infant and juvenile rhesus monkeys. Hormones and Behavior, 63, 646-658. http://dx.doi.org/10.1016/j.yhbeh.2013.01.010
42. Raper, J., Wilson, M., Sanchez, M., Machado, C. J., Bachevalier, J. (2013). Pervasive alterations of emotional and neuroendocrine responses to an acute stressor after neonatal amygdala lesions in rhesus monkeys. Psychoneuroendocrinology, 38, 1021-1035. http://dx.doi.org/10.1016/j.psyneuen.2012.10.008
43. Schreiner, L., Kling, A. (1956). Rhinencephalon and behavior. The American Journal of Physiology, 184, 486-490.
44. Stefanacci, L., Clark, R. E., Zola, S. M. (2003). Selective neurotoxic amygdala lesions in monkeys disrupt reactivity to food and object stimuli and have limited effects on memory. Behavioral Neuroscience, 117, 1029-1043.
45. Stephens, S. B., Raper, J., Bachevalier, J., Wallen, K. (2014). Neonatal amygdala lesions advance pubertal timing in female rhesus macaques. Psychoneuroendocrinology, 51, 307-317.
46. Thompson, C. I. (1969). Time in test cage and behavior after amygdalectomy in infant rhesus monkeys. Physiology & Behavior, 4, 1027-1029. http://dx.doi.org/10.1016/0031f-9384(69)90061-4
47. Thompson, C. I., Bergland, R. M., Towfighi, J. T. (1977). Social and nonsocial behaviors of adult rhesus monkeys after amygdalectomy in infancy or adulthood. Journal of Comparative and Physiological Psychology, 91, 533-548. http://dx.doi.org/10.1037/h0077352
48. Thompson, C. I., Schwartzbaum, J. S., Harlow, H. F. (1969). Development of social fear after amygdalectomy in infant rhesus monkeys. Physiology & Behavior, 4, 249-254. http://dx.doi.org/10.1016/0031-9384(69)90088-2
49. Thompson, C. I., Towfighi, J. T. (1976). Social behavior of juvenile rhesus monkeys after amygdalectomy in infancy. Physiology & Behavior, 17, 831-836. http://dx.doi.org/10.1016/0031-9384(76)90049-4
50. Toscano, J. E., Bauman, M. D., Mason, W. A., Amaral, D. G. (2009). Interest in infants by female rhesus monkeys with neonatal lesions of the amygdala or hippocampus. Neuroscience, 162, 881-891. http://dx.doi.org/10.1016/j.neuroscience.2009.05.056
51. Tseng, K. Y., Chambers, R. A., Lipska, B. K. (2009). The neonatal ventral hippocampal lesion as a heuristic neurodevelopmental model of schizophrenia. Behavioural Brain Research, 204, 295-305. http://dx.doi.org/10.1016/j.bbr.2008.11.039
52. Zeamer, A., Heuer, E., Bachevalier, J. (2010). Developmental trajectory of object recognition memory in infant rhesus macaques with and without neonatal hippocampal lesions. The Journal of Neuroscience, 30, 9157-9165. http://dx.doi.org/10.1523/JNEUROSCI.0022-10.2010