Maternal inhibition of infant behavioral response following isolation in novel surroundings and inflammatory challenge

Developmental Psychobiology

Volumn 55, Issue 4, 2013, Pages 395-403

  Hennessy, Michael B ^a   Jacobs, Sarah ^a   Schiml, Patricia A ^a   Hawk, Kiel ^a   Stafford, Nathan ^a   Deak, Terrence ^b  

^a WRIGHT STATE UNIVERSITY   (United States)

^b BINGHAMTON UNIVERSITY   (United States)

Author keywords

Corticotropin releasing factor (CRF); Corticotropin releasing hormone (CRH); Guinea pig; Lipopolysacchride; Maternal separation; Proinflammatory activity; Sickness behavior; Social buffering; Social separation

Indexed keywords

CORTICOTROPIN RELEASING FACTOR; HORMONE; LIPOPOLYSACCHARIDE;

ANIMAL; ANIMAL BEHAVIOR; ARTICLE; DRUG EFFECT; FEMALE; GUINEA PIG; ILLNESS BEHAVIOR; INFLAMMATION; INHIBITION (PSYCHOLOGY); MALE; MATERNAL DEPRIVATION; NEUROPSYCHOLOGICAL TEST; PHYSIOLOGY; PSYCHOLOGICAL ASPECT; SEX DIFFERENCE; SOCIAL ISOLATION;

ANIMALS; BEHAVIOR, ANIMAL; CORTICOTROPIN-RELEASING HORMONE; FEMALE; GUINEA PIGS; HORMONES; ILLNESS BEHAVIOR; INFLAMMATION; INHIBITION (PSYCHOLOGY); LIPOPOLYSACCHARIDES; MALE; MATERNAL DEPRIVATION; NEUROPSYCHOLOGICAL TESTS; SEX FACTORS; SOCIAL ISOLATION;

ANIMALIA; CAVIA;

EID: 84876105547     PISSN: 00121630     EISSN: 10982302     Source Type: Journal    
DOI: 10.1002/dev.21044     Document Type: Article

References (55)

1. Aubert, A., Goodall, G., Danzer, R., & Gheusi, G. (1997). Differential effects of lipopolysacchride on pup retrieving and nest building in lactating mice. Brain, Behavior, and Immunity, 11, 107-118.
2. Aubert, A. (1999). Sickness and behaviour in animals: A motivational hypothesis. Neuroscience and Biobehavioral Reviews, 23, 1029-1036.
3. Bagot, R. C., van Hasselt, F. N., Champagne, D. L., Meaney, M. J., Krugers, H. J., & Joels, M. (2009). Maternal care determines rapid effects of stress mediators on dynamic synaptic plasticity in adult rat hippocampal dentate gyrus. Neurobiology of Learning and Memory, 92, 292-300.
4. Baker, C., Richards, L. J., Dayan, C. M., & Jessop, D. S. (2003). Corticotropin-releasing hormone immunoreactivity in human T and B cells and macrophages: Colocalization with arginine vasopressin. Journal of Neuroendocrinology, 15, 1070-1074.
5. Becker, L. A., & Hennessy, M. B. (1993). Further characterization of the behavioral effects of peripherally administered corticotropin-releasing factor in guinea pigs. Pharmacology, Biochemistry and Behavior, 44, 925-930.
6. Belay, H., Burton, C. L., Lovic, V., Meaney, M. J., Sokolowski, M., & Flemming, A. S. (2011). Early adversity and serotonin transporter genotype interact with hippocampal glucocorticoid receptor mRNA expression, corticosterone, and behavior in adult rats. Behavioral Neuroscience, 125, 150-160.
7. Black-Rubio, C. M., Cibils, A. F., & Gould, W. R. (2007). Maternal influence on feeding site avoidance behavior of lambs. Applied Animal Behaviour Science, 105, 122-139.
8. Blatteis, C. M. (1975). Postnatal development of pyrogenic sensitivity in guinea pigs. Journal of Applied Physiology, 39, 251-257.
9. Cameron, N. M. (2011). Maternal programming of reproductive function and behavior in the female rat. Frontiers in Evolutionary Neuroscience, 3, 1-10.
10. Champagne, F. A., & Curley, J. P. (2005). How social experiences influence the brain. Current Opinion in Neurobiology, 15, 1-6.
11. Chowdrey, H. S., Lightman, S. L., Harbuz, M. S., Larsen, P. J., & Jessop, D. S. (1984). Contents of corticotropin-releasing hormone and arginine vasopressin immunoreactivity in the spleen and thymus during a chronic inflammatory stress. Journal of Neuroimmunology, 53, 17-21.
12. Colonnello, V., Iacobucci, P., Fuchs, T., Newberry, R., & Panksepp, J. (2011). Octodon degus. A useful animal model for social-affective neuroscience research: Basic description of separation distress, social attachments and play. Neuroscience and Biobehavioral Reviews, 35, 1854-1863.
13. Friedman, E. M., Reyes, T. M., & Coe, C. L. (1996). Context-dependent behavioral effects of interleukin-1 in the rhesus monkey, Macaca mulatta. Psychoneuroendocrinology, 21, 455-468.
14. Galef, B. G., & Clark, M. M. (1972). Mother's milk and adult presence: Two factors determining initial dietary selection by weanling rats. Journal of Comparative and Physiological Psychology, 78, 220-225.
15. Hagen, P. M., Poole, S., & Bristow, A. F. (1993). Corticotropin-releasing factor as a mediator of the acute-phase response in rats, mice, and rabbits. Journal of Endocrinology, 136, 207-216.
16. Harlow, H. F. (1962). The heterosexual affectional system in monkeys. American Psychologist, 17, 1-9.
17. Hart, B. L. (1988). Biological basis of the behavior of sick animals. Neuroscience and Biobehavioral Reviews, 12, 123-137.
18. Hennessy, M. B., Deak, T., Schiml-Webb, P. A., Wilson, S. E., Greenlee, T. M., & McCall, E. (2004). Responses of guinea pig pups during isolation in a novel environment may represent stress-induced sickness behaviors. Physiology and Behavior, 81, 5-13.
19. Hennessy, M. B., Fitch, C., Jacobs, S., Deak, T., & Schiml, P. A. (2011). Behavioral effects of peripheral corticotropin-releasing factor during maternal separation may be mediated by proinflammatory activity. Psychoneuroendocrinology, 36, 996-1004.
20. Hennessy, M. B., & Jenkins, R. (1994). A descriptive analysis of nursing behavior in the guinea pig (Cavia porcellus). Journal of Comparative Psychology, 108, 23-28.
21. Hennessy, M. B., Maken, D. S., & Graves, F. C. (2002). Presence of mother and unfamiliar female alters levels of testosterone, progesterone, cortisol, adrenocorticotropin, and behavior in maturing guinea pigs. Hormones and Behavior, 42, 42-52.
22. Hennessy, M. B., & Morris, A. (2005). Passive responses of young guinea pigs during exposure to a novel environment: Influences of social partners and age. Developmental Psychobiology, 46, 86-96.
23. Hennessy, M. B., Long, S. J., Nigh, C. K., Williams, W. T., & Nolan, D. J. (1995). Effects of peripherally administered corticotropin-releasing factor (CRF) and a CRF antagonist: Does peripheral CRF activity mediate behavior of guinea pig pups during isolation? Behavioral Neuroscience, 109, 1137-1145.
24. Hennessy, M. B., Schiml-Webb, P. A., Miller, E. E., Maken, D. S., Bullinger, K. L., & Deak, T. (2007). Anti-inflammatory agents attenuate the passive responses of guinea pig pups: Evidence for stress-induced sickness behavior during maternal separation. Psychoneuroendocrinology, 32, 508-515.
25. Hennessy, M. B., Young, T. L., O'Leary, S. K., & Maken, D. S. (2003). Social preferences of developing guinea pigs (Cavia porcellus) from the preweaning to the periadolescent period. Journal of Comparative Psychology, 117, 406-413.
26. Hofer, M. A. (1987). Shaping forces within early social relationships. In N. A. Krasnegor, E. M. Blass, M. A. Hofer, & W. P. Smotherman (Eds.), Perinatal development: A psychobiological perspective (pp. 251-274). Orlando: Academic Press.
27. Hofer, M. A. (2006). Psychobiological roots of early attachment. Current Directions in Psychological Science, 15, 84-88.
28. Hrdy, S. B. (1979). Infanticide among animals: A review, classification, and examination of the implications for the reproductive strategies of females. Ethology and Sociobiology, 1, 13-40.
29. Karalis, K., Muglia, L. J., Bae, D., Hilderbrand, H., & Majzoub, J. A. (1997). CRH and the immune system. Journal of Neuroimmology, 72, 131-136.
30. Karelina, K., Norman, G. J., Zhang, N., Morris, J. S., Peng, H., & DeVries, A. C. (2009). Social isolation alters neuroinflammatory response to stroke. Proceedings of National Academy of Sciences, USA, 106, 5895-5900.
31. Kaufman, I. C., & Rosenblum, L. A. (1967). The reaction to separation in infant monkeys: Anaclitic depression and conservation withdrawal. Psychosomatic Medicine, 29, 648-675.
32. König, B. (1985). Maternal activity budget during lactation in two species of Caviidae (Cavia porcellus and Galea musteloides). Zeitschrift für Tierpsychologie, 68, 215-230.
33. Leu, S. J., & Singh, L. K. (1992). Stimulation of interleukin-6 production by corticotrophin-releasing hormone. Cellular Immunology, 143, 220-227.
34. Levine, S. (2001). Primary social relationships influence the development of the hypothalamic-pituitary-adrenal axis in the rat. Physiology and Behavior, 73, 255-260.
35. MacLean, P. D. (1985). Brain evolution relating to family, play, and the separation call. Archives of General Psychiatry, 42, 405-417.
36. Maier, S. F., & Watkins, L. R. (1998). Cytokines for psychologists: Implications of bidirectional immune-to-brain communication for understanding behavior, mood, and cognition. Psychological Review, 105, 83-107.
37. Mason, W. A. (1978). Social experience and primate cognitive development. In G. M. Burghardt & M. Beckoff (Eds.), The development of behavior: Comparative and evolutionary aspects (pp. 233-251), New York: Garland STPM Press.
38. Mateo, J. M. (2009). Maternal influences on habitat selection, social relationships, and survival behaviors. In D. Maestripieri & J. M. Mateo (Eds.), Maternal effects in mammals (pp. 133-158), Chicago, IL: University of Chicago Press.
39. Moore, C. L., Dou, H., & Juraska, J. M. (1992). Maternal stimulation affects the number of motor neurons in a sexually dimorphic nucleus of the lumbar spinal cord. Brain Research, 572, 52-56.
40. Paschos, K. A., Kolios, G., & Chatzaki, E. (2009). The corticotropin-releasing factor system in inflammatory bowel disease: Prospects for new therapeutic approaches. Drug Discovery Today, 14, 713-720.
41. Perkeybile, A. M., Schiml-Webb, P. A., O'Brien, E., Deak, T., & Hennessy, M. B. (2009). Anti-inflammatory influences on behavioral, but not cortisol, responses during maternal separation. Psychoneuroendocrinology, 34, 1101-1108.
42. Sachser, N., Hennessy, M. B., & Kaiser, S. (2011). Adaptive modulation of behavioural profiles by social stress during early phases of life and adolescence. Neuroscience and Biobehavioral Reviews, 35, 1518-1533.
43. Schanberg, S. M., Ingledue, V. F., Lee, Y., Hannun, Y. A., & Bartolome, J. V. (2003). PKC alpha mediates maternal touch regulation of growth-related gene expression in infant rats. Neuropsychopharmacology, 28, 1026-1030.
44. Schiml, P. A., & Hennessy, M. B. (1990). Light-dark variation and changes across the lactational period in the behaviors of undisturbed mother and infant guinea pigs. Journal of Comparative Psychology, 104, 283-288.
45. Schiml-Webb, P. A., Deak, T., Greenlee, T. M., Maken, D. S., & Hennessy, M. B. (2006). Alpha-melanocyte stimulating hormone reduces putative stress-induced sickness behaviors in isolated guinea pig pups. Behavioural Brain Research, 168, 326-330.
46. Schiml-Webb, P. A., Miller, E. E., Deak, T., & Hennessy, M. B. (2009). Alpha-melanocyte-stimulating hormone attenuates behavioral effects of corticotropin-releasing factor in isolated guinea pig pups. Developmental Psychobiology, 51, 399-407.
47. Sevelinges, Y., Mouly, A. M., Raineki, C., Moriceau, S., Forest, C., & Sullivan, R. M. (2011). Adult depression-like behavior, amygdala and olfactory cortex functions are restored by odor previously paired with shock during infant's sensitive period attachment learning. Developmental Cognitive Neuroscience, 1, 77-87.
48. Shair, H. N. (2007). Acquisition and expression of a socially mediated separation response. Behavioural Brain Research, 182, 180-192.
49. Singh L. K., & Leu, S. J. (1990). Enhancing effect of corticotropin-releasing neurohormone on the production of interleukin-1 and interleukin-2. Neuroscience Letters, 120, 151-154.
50. Stengel, A., & Taché, Y. (2009). Neuroendocrine control of the gut during stress: Corticotropin-releasing factor signaling pathways in the spotlight. Annual Review of Physiology, 71, 219-239.
51. Stucky, N. L., Gregory, E., Winter, M. K., He, Y. Y., Hamilton, E. S., McCarson, K. E., & Berman, N. E. (2011). Sex differences in behavior and expression of CGRP-related genes in a rodent model of chronic migraine. Headache, 51, 674-692.
52. Webster, E. L., Elenkov, I. J., & Chrousos, G. P. (1997). The role of corticotropin-releasing hormone in neuroendocrine-immune interactions. Molecular Psychiatry, 2, 368-372.
53. Willette, A. A., Lubach, G. R., & Coe, C. L. (2007). Environmental context differentially affects behavioral, leukocyte, cortisol, and interleukin-6 responses to low dose of endotoxin in the rhesus monkey. Brain, Behavior, and Immunity, 21, 807-815.
54. Yee, J. R., & Prendergast, B. J. (2010). Sex-specific social regulation of inflammatory responses and sickness behaviors. Brain, Behavior, and Immunity, 24, 942-951.
55. Yirmiya, R., Avitsur, R., Donchin, O., & Cohen, E. (1995). Interleukin-I inhibits sexual behevior in female but not in male rats. Brain, Behavior, and Immunity, 9, 220-233.