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Assessing Postpartum Maternal Care, Alloparental Behavior, and Infanticide in Mice: With Notes on Chemosensory Influences

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Part of the book series: Methods in Molecular Biology ((MIMB,volume 1068))

Abstract

Chemosensory signaling influences maternal care and other innate behaviors toward conspecific young animals in rodents. In this chapter, we describe basic protocols for assessment of postpartum maternal behavior and other pup-directed behaviors in laboratory mice. The specific aim of this protocol is to screen out the abnormal phenotypes in parenting of genetic mutant mice under the standard housing condition. The possible underlying mechanisms for a given abnormality in the mother-young interaction are briefly suggested as well.

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References

  1. Krasnegor NA, Bridges RS (1990) Mammalian parenting: biochemical, neurobiological, and behavioral determinants. Oxford University Press, New York, NY

    Google Scholar 

  2. Numan M, Insel TR (2003) The neurobiology of parental behavior. Springer, New York, NY

    Google Scholar 

  3. vom Saal FS, Howard LS (1982) The regulation of infanticide and parental behavior: implications for reproductive success in male mice. Science 215(4537):1270–1272

    Article  PubMed  CAS  Google Scholar 

  4. Priestnall R, Young S (1978) An observational study of caretaking behavior of male and female mice housed together. Dev Psychobiol 11(1):23–30

    Article  PubMed  CAS  Google Scholar 

  5. Rosenblatt JS (1967) Nonhormonal basis of maternal behavior in the rat. Science 156(781):1512–1514

    Article  PubMed  CAS  Google Scholar 

  6. Numan M, McSparren J, Numan MJ (1990) Dorsolateral connections of the medial preoptic area and maternal behavior in rats. Behav Neurosci 104(6):964–979

    Article  PubMed  CAS  Google Scholar 

  7. Brown JR, Ye H, Bronson RT, Dikkes P, Greenberg ME (1996) A defect in nurturing in mice lacking the immediate early gene fosB. Cell 86(2):297–309

    Article  PubMed  CAS  Google Scholar 

  8. Elwood RW (1983) Parental behaviour of rodents. Wiley, New York, NY

    Google Scholar 

  9. Sluckin W, Herbert M (1986) Parental Behaviour. Basil Blackwell, Oxford

    Google Scholar 

  10. Rosenblatt JS, Snowdon CT (eds) (1996) Parental care: evolution, mechanism, and adaptive significance, vol 25, Advances in the study of behavior. Academic, San Diego, CA

    Google Scholar 

  11. Lonstein JS, Fleming AS (2002) Parental behaviors in rats and mice. Curr Protoc Neurosci Chapter 8:8.15.11–18.15.26

    Google Scholar 

  12. Capone F, Bonsignore L, Cirulli F (2005) UNIT 13.9 methods in the analysis of maternal behavior in the rodent. Curr Protoc Toxicol 13(9):1–16

    Google Scholar 

  13. Kuroda KO, Tachikawa K, Yoshida S, Tsuneoka Y, Numan M (2011) Neuromolecular basis of parental behavior in laboratory mice and rats: with special emphasis on technical issues of using mouse genetics. Prog Neuropsychopharmacol Biol Psychiatry 35(5):1205–1231. doi:10.1016/j.pnpbp.2011.02.008, S0278-5846(11)00062-5 [pii]

    Article  PubMed  CAS  Google Scholar 

  14. Levy F, Keller M (2009) Olfactory mediation of maternal behavior in selected mammalian species. Behav Brain Res 200(2):336–345

    Article  PubMed  Google Scholar 

  15. Wong ST, Trinh K, Hacker B, Chan GC, Lowe G, Gaggar A, Xia Z, Gold GH, Storm DR (2000) Disruption of the type III adenylyl cyclase gene leads to peripheral and behavioral anosmia in transgenic mice. Neuron 27(3):487–497, S0896-6273(00)00060-X [pii]

    Article  PubMed  CAS  Google Scholar 

  16. Wang Z, Storm DR (2011) Maternal behavior is impaired in female mice lacking type 3 adenylyl cyclase. Neuropsychopharmacology 36(4):772–781

    Article  PubMed  CAS  Google Scholar 

  17. Belluscio L, Gold GH, Nemes A, Axel R (1998) Mice deficient in G(olf) are anosmic. Neuron 20(1):69–81

    Article  PubMed  CAS  Google Scholar 

  18. Bean NJ, Wysocki CJ (1989) Vomeronasal organ removal and female mouse aggression: the role of experience. Physiol Behav 45(5):875–882

    Article  PubMed  CAS  Google Scholar 

  19. Leypold BG, Yu CR, Leinders-Zufall T, Kim MM, Zufall F, Axel R (2002) Altered sexual and social behaviors in trp2 mutant mice. Proc Natl Acad Sci U S A 99(9):6376–6381. doi:10.1073/pnas.082127599, 082127599 [pii]

    Article  PubMed  CAS  Google Scholar 

  20. Del Punta K, Leinders-Zufall T, Rodriguez I, Jukam D, Wysocki CJ, Ogawa S, Zufall F, Mombaerts P (2002) Deficient pheromone responses in mice lacking a cluster of vomeronasal receptor genes. Nature 419(6902):70–74

    Article  PubMed  Google Scholar 

  21. Mennella JA, Moltz H (1988) Infanticide in the male rat: the role of the vomeronasal organ. Physiol Behav 42(3):303–306

    Article  PubMed  CAS  Google Scholar 

  22. Fleming AS, Gavarth K, Sarker J (1992) Effects of transections to the vomeronasal nerves or to the main olfactory bulbs on the initiation and long-term retention of maternal behavior in primiparous rats. Behav Neural Biol 57(3):177–188

    Article  PubMed  CAS  Google Scholar 

  23. Yagi T, Aizawa S, Tokunaga T, Shigetani Y, Takeda N, Ikawa Y (1993) A role for Fyn tyrosine kinase in the suckling behaviour of neonatal mice. Nature 366(6457):742–745. doi:10.1038/366742a0

    Article  PubMed  CAS  Google Scholar 

  24. Hamaguchi-Hamada K, Sanbo C, Hamada S, Yagi T (2004) Exposure to hexanal odor influences maternal behavior and induces neonatal death in Fyn tyrosine kinase-deficient mice. Neurosci Res 48(3):259–267

    Article  PubMed  CAS  Google Scholar 

  25. Kuroda KO, Meaney MJ, Uetani N, Kato T (2008) Neurobehavioral basis of the impaired nurturing in mice lacking the immediate early gene FosB. Brain Res 1211:57–71

    Article  PubMed  CAS  Google Scholar 

  26. Deacon RM (2006) Assessing nest building in mice. Nat Protoc 1(3):1117–1119

    Article  PubMed  Google Scholar 

  27. Doetschman T (2009) Influence of genetic background on genetically engineered mouse phenotypes. Methods Mol Biol 530:423–433

    Article  PubMed  CAS  Google Scholar 

  28. Brown RE, Mathieson WB, Stapleton J, Neumann PE (1999) Maternal behavior in female C57BL/6J and DBA/2J inbred mice. Physiol Behav 67(4):599–605

    Article  PubMed  CAS  Google Scholar 

  29. Shoji H, Kato K (2006) Maternal behavior of primiparous females in inbred strains of mice: a detailed descriptive analysis. Physiol Behav 89(3):320–328

    Article  PubMed  CAS  Google Scholar 

  30. Wolfer DP, Crusio WE, Lipp HP (2002) Knockout mice: simple solutions to the problems of genetic background and flanking genes. Trends Neurosci 25(7):336–340

    Article  PubMed  CAS  Google Scholar 

  31. Hess SE, Rohr S, Dufour BD, Gaskill BN, Pajor EA, Garner JP (2008) Home improvement: C57BL/6J mice given more naturalistic nesting materials build better nests. J Am Assoc Lab Anim Sci 47(6):25–31

    PubMed  CAS  Google Scholar 

  32. Moltz H, Lubin M, Leon M, Numan M (1970) Hormonal induction of maternal behavior in the ovariectomized nulliparous rat. Physiol Behav 5(12):1373–1377

    Article  PubMed  CAS  Google Scholar 

  33. Pedersen CA, Prange AJ Jr (1979) Induction of maternal behavior in virgin rats after intracerebroventricular administration of oxytocin. Proc Natl Acad Sci U S A 76(12):6661–6665

    Article  PubMed  CAS  Google Scholar 

  34. Bridges RS, DiBiase R, Loundes DD, Doherty PC (1985) Prolactin stimulation of maternal behavior in female rats. Science 227(4688):782–784

    Article  PubMed  CAS  Google Scholar 

  35. Noirot E (1972) The onset of maternal behavior in rats, hamsters, and mice a selective review. In: Lehrman DS, Hinde RA, Shaw E (eds) Advances in the study of behavior, vol 4. Elsevier, New York, NY, pp 107–145

    Google Scholar 

  36. Lonstein JS, De Vries GJ (2000) Sex differences in the parental behavior of rodents. Neurosci Biobehav Rev 24(6):669–686

    Article  PubMed  CAS  Google Scholar 

  37. Leblond CP (1940) Extra-hormonal factors in maternal behavior. Proc Soc Exp Biol Med 38:66–70

    Google Scholar 

  38. Leblond CP, Nelson WO (1937) Maternal behavior in hypophysectomized male and female mice. Am J Physiol 120:167–172

    Google Scholar 

  39. Perrigo G, Belvin L, Quindry P, Kadir T, Becker J, van Look C, Niewoehner J, vom Saal FS (1993) Genetic mediation of infanticide and parental behavior in male and female domestic and wild stock house mice. Behav Genet 23(6):525–531

    Article  PubMed  CAS  Google Scholar 

  40. Trivers RL (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man 1871-1971. Aldine-Atherton, Chicago, IL, pp 136–172

    Google Scholar 

  41. Hrdy SB (1974) Male-male competition and infanticide among the langurs (Presbytis entellus) of Abu, Rajasthan. Folia Primatol (Basel) 22(1):19–58

    Article  CAS  Google Scholar 

  42. Parmigiani S, Vom Saal FS (eds) (1990) Infanticide and parental care. Harwood academic publishers, London

    Google Scholar 

  43. Beach FA, Jaynes J (1956) Studies of Maternal Retrieving in Rats: III. Sensory cues involved in the lactating female’s response to her young. Behavior 10:104–125

    Article  Google Scholar 

  44. Herrenkohl LR, Rosenberg PA (1972) Exteroceptive stimulation of maternal behavior in the naive rat. Physiol Behav 8(4):595–598

    Article  PubMed  CAS  Google Scholar 

  45. Tasaki T, Sohr R, Xia Z, Hellweg R, Hortnagl H, Varshavsky A, Kwon YT (2007) Biochemical and genetic studies of UBR3, a ubiquitin ligase with a function in olfactory and other sensory systems. J Biol Chem 282(25):18510–18520

    Article  PubMed  CAS  Google Scholar 

  46. Kimchi T, Xu J, Dulac C (2007) A functional circuit underlying male sexual behaviour in the female mouse brain. Nature 448(7157):1009–1014. doi:10.1038/nature06089, nature06089 [pii]

    Article  PubMed  CAS  Google Scholar 

  47. Crawley JN (2007) Whats wrong with my mouse? Behavioral phenotyping of trangenic and knockout mice, 2nd edn. Wiley-Liss, New York, NY

    Book  Google Scholar 

  48. Francis D, Diorio J, Liu D, Meaney MJ (1999) Nongenomic transmission across generations of maternal behavior and stress responses in the rat. Science 286(5442):1155–1158

    Article  PubMed  CAS  Google Scholar 

  49. Crawley JN (2008) Behavioral phenotyping strategies for mutant mice. Neuron 57(6):809–818

    Article  PubMed  CAS  Google Scholar 

  50. Hedrich H (ed) (2004) The laboratory mouse, The hand book of experimental animals. Elsevier, Amsterdam

    Google Scholar 

  51. Gandelman R (1973) Induction of maternal nest building in virgin female mice by the presentation of young. Horm Behav 4(3):191–197

    Article  PubMed  CAS  Google Scholar 

  52. Slotnick BM, Nigrosh BJ (1975) Maternal behavior of mice with cingulate cortical, amygdala, or septal lesions. J Comp Physiol Psychol 88(1):118–127

    Article  PubMed  CAS  Google Scholar 

  53. Numan M, Callahan EC (1980) The connections of the medial preoptic region and maternal behavior in the rat. Physiol Behav 25(5):653–665

    Article  PubMed  CAS  Google Scholar 

  54. Mann PE (1993) Measurement of maternal behavior. Methods Neurosci 14:343–358

    Google Scholar 

  55. Manning CJ, Wakeland EK, Potts WK (1992) Communal nesting patterns in mice implicate MHC genes in kin recognition. Nature 360(6404):581–583

    Article  PubMed  CAS  Google Scholar 

  56. Valzelli L, Bernasconi S, Gomba P (1974) Effect of isolation on some behavioral characteristics in three strains of mice. Biol Psychiatry 9(3):329–334

    PubMed  CAS  Google Scholar 

  57. Liu D, Diorio J, Tannenbaum B, Caldji C, Francis D, Freedman A, Sharma S, Pearson D, Plotsky PM, Meaney MJ (1997) Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science 277(5332):1659–1662

    Article  PubMed  CAS  Google Scholar 

  58. Perrigo G, Belvin L, vom Saal F (1990) Humane behavioral assays in the laboratory: an alternative test for assessing how rodents behave toward young. Humane Innov Alternat Anim Experiment 4:208–209

    Google Scholar 

  59. Perrigo G, Bryant W, vom Saal F (1989) The use of live pups in a humane, injury-free test for infanticidal behaviour in male mice. Anim Behav 38:897–904

    Article  Google Scholar 

  60. Stern JM, Lonstein JS (2001) Neural mediation of nursing and related maternal behaviors. Prog Brain Res 133(64):263–278

    Article  PubMed  CAS  Google Scholar 

  61. Lonstein JS, Wagner CK, De Vries GJ (1999) Comparison of the “nursing” and other parental behaviors of nulliparous and lactating female rats. Horm Behav 36(3):242–251

    Article  PubMed  CAS  Google Scholar 

  62. Wiesner BP, Sheard NM (1933) Maternal behaviour in the Rat. Oliver and Boyd, London

    Google Scholar 

  63. Bridges RS, Zarrow MX, Goldman BD, Denenberg VH (1974) A developmental study of maternal responsiveness in the rat. Physiol Behav 12(1):149–151

    Article  PubMed  CAS  Google Scholar 

  64. Fahrbach SE, Morrell JI, Pfaff DW (1984) Oxytocin induction of short-latency maternal behavior in nulliparous, estrogen-primed female rats. Horm Behav 18(3):267–286, 0018-506X(84)90016-3 [pii]

    Article  PubMed  CAS  Google Scholar 

  65. Kinsley CH, Bridges RS (1988) Parity-associated reductions in behavioral sensitivity to opiates. Biol Reprod 39(2):270–278

    Article  PubMed  CAS  Google Scholar 

  66. Moore CL (1992) The role of maternal stimulation in the development of sexual behavior and its neural basis. Ann N Y Acad Sci 662:160–177

    Article  PubMed  CAS  Google Scholar 

  67. Gubernick DJ, Alberts JR (1985) Maternal licking by virgin and lactating rats: water transfer from pups. Physiol Behav 34(4):501–506

    Article  PubMed  CAS  Google Scholar 

  68. Ambrose A (ed) (1969) Stimulation in early infancy. Academic, New York, NY

    Google Scholar 

  69. Rosenberg KM, Denenberg VH, Zarrow MX (1970) Mice (Mus musculus) reared with rat aunts: the role of rat-mouse contact in mediating behavioural and physiological changes in the mouse. Anim Behav 18(1):138–143

    Article  PubMed  CAS  Google Scholar 

  70. Kristal MB (1980) Placentophagia: a biobehavioral enigma (or De gustibus non disputandum est). Neurosci Biobehav Rev 4(2):141–150

    Article  PubMed  CAS  Google Scholar 

  71. Kristal MB (1991) Enhancement of opioid-mediated analgesia: a solution to the enigma of placentophagia. Neurosci Biobehav Rev 15(3):425–435, S0149-7634(05)80035-1 [pii]

    Article  PubMed  CAS  Google Scholar 

  72. Kristal MB, Graber GC (1976) Placentophagia in nonpregnant rats: influence of estrous cycle stage and birthplace. Physiol Behav 17(4):599–605

    Article  PubMed  CAS  Google Scholar 

  73. Kristal MB, Eleftheriou BE (1975) Placentophagia in nonpregnant nulliparous mice: a genetic investigation. Behav Biol 13(1):113–119

    Article  PubMed  CAS  Google Scholar 

  74. Koller G (1952) Der Nestbau der Weissen Maus und seine hormonale Auslosung. Zool Anz Suppl 17:160–168

    Google Scholar 

  75. Denenberg VH, Taylor RE, Zarrow MX (1969) Maternal behavior in the rat: an investigation and quantification of nest building. Behaviour 34(1):1–16

    Article  PubMed  CAS  Google Scholar 

  76. Lonstein JS, Gammie SC (2002) Sensory, hormonal, and neural control of maternal aggression in laboratory rodents. Neurosci Biobehav Rev 26(8):869–888

    Article  PubMed  Google Scholar 

  77. Gammie SC (2005) Current models and future directions for understanding the neural circuitries of maternal behaviors in rodents. Behav Cogn Neurosci Rev 4(2):119–135

    Article  PubMed  Google Scholar 

  78. Svare B, Gandelman R (1976) Suckling stimulation induces aggression in virgin female mice. Nature 260(5552):606–608

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Kashiko Tachikawa and Yoshihiro Yoshihara for helpful discussion and comments on this topic. This work was supported by RIKEN, the Uehara Memorial Foundation, and the JSPS Grant-in-Aid programs. We would appreciate if the readers kindly let us know if any corrections or comments on this article at: oyako@brain.riken.jp.

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Kuroda, K.O., Tsuneoka, Y. (2013). Assessing Postpartum Maternal Care, Alloparental Behavior, and Infanticide in Mice: With Notes on Chemosensory Influences. In: Touhara, K. (eds) Pheromone Signaling. Methods in Molecular Biology, vol 1068. Humana Press, Totowa, NJ. https://doi.org/10.1007/978-1-62703-619-1_25

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  • DOI: https://doi.org/10.1007/978-1-62703-619-1_25

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