Sex differences in the parental behavior of rodents

Lonstein, Joseph S.; De Vries, Geert J.

doi:10.1016/s0149-7634(00)00036-1

Cited by 226Neuroendocrine regulation and behaviorAnimal Behavior and ReproductionSexual Differentiation and Disorders

Sex differences in the parental behavior of rodents

Lonstein, Joseph S., De Vries, Geert J.·2000·Neuroscience & Biobehavioral Reviews

DOI 10.1016/s0149-7634(00)00036-1

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Abstract

The reproductive strategy of many mammalian species that give birth to altricial young involves intense and prolonged care of their offspring. In most cases, the mother provides all nurturance, but in some cases fathers, older siblings, or unrelated conspecifics participate in parental care. The display of these behaviors by animals other than mothers is affected by numerous factors, including their sex. We herein review the literature on similarities and/or differences between male and female laboratory rodents (rats, mice, voles, gerbils, and hamsters) in their parental responsiveness and discuss how the parental behavior of males and females is influenced by hormones, developmental processes, and prior social experiences. Understanding the mechanisms that generate sex differences in the parental responsiveness of rodents may indicate how similar sex differences in parental care are generated in other mammals.

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The control and function of maternal scent marking in the Mongolian gerbil
WALLACE, P. M., Owen, K., & Thiessen, D. D. (1973) · Physiology & Behavior · doi:10.1016/0031-9384(73)90206-0 · Cited by 87 · see citing works
Individual differences in the mechanisms underlying the onset and maintenance of paternal behavior and the inhibition of infanticide in the monogamous biparental California mouse, Peromyscus californicus
Gubernick, D. J., Schneider, K. A., & Jeannotte, L. A. (1994) · Behavioral Ecology and Sociobiology · doi:10.1007/bf00167748 · Cited by 86 · see citing works
The influence of reproductive state on infanticide by wild female house mice (Mus musculus)☆
McCarthy, M. J., & VOMSAAL, F. (1985) · Physiology & Behavior · doi:10.1016/0031-9384(85)90248-3 · Cited by 84 · see citing works
Paternal Hamsters Mechanically Assist the Delivery, Consume Amniotic Fluid and Placenta, Remove Fetal Membranes, and Provide Parental Care during the Birth Process
Jones, J. S., & Wynne‐Edwards, K. E. (2000) · Hormones and Behavior · doi:10.1006/hbeh.1999.1563 · Cited by 83 · see citing works
Changes in incidence of infanticidal and parental responses during the reproductive cycle in male and female wild mice Mus musculus
Soroker, V., & Terkel, J. (1988) · Animal Behaviour · doi:10.1016/s0003-3472(88)80196-9 · Cited by 82 · see citing works
Pup-killing in mice: The effects of gonadectomy and testosterone administration☆
GANDELMAN, R., & VOMSAAL, F. (1975) · Physiology & Behavior · doi:10.1016/0031-9384(75)90114-6 · Cited by 81 · see citing works
Perinatal Steroid Treatments Alter Alloparental and Affiliative Behavior in Prairie Voles
Roberts, R. L., Zullo, A. S., Gustafson, E. A., & Carter, C. S. (1996) · Hormones and Behavior · doi:10.1006/hbeh.1996.0060 · Cited by 80 · see citing works
Ontogeny of maternal behavior in the laboratory rat: Early origins in 18‐ to 27‐day‐old young
Mayer, A. D., & Rosenblatt, J. S. (1979) · Developmental Psychobiology · doi:10.1002/dev.420120502 · Cited by 80 · see citing works
The sex hormone-dependent development of opiate receptors in the rat medial preoptic area
Hammer, R. P. (1985) · Brain Research · doi:10.1016/0006-8993(85)91221-1 · Cited by 79 · see citing works
Comparison of parental behavior in male and female prairie voles (Microtus ochrogaster)
Solomon, N. G. (1993) · Canadian Journal of Zoology · doi:10.1139/z93-061 · Cited by 79 · see citing works
Infanticide: Genetic, developmental and hormonal influences in mice
Svare, B. B., & Mann, M. A. (1981) · Physiology & Behavior · doi:10.1016/0031-9384(81)90062-7 · Cited by 78 · see citing works
Postpartum maintenance of paternal behaviour in the biparental California mouse, Peromyscus californicus
Gubernick, D. J., & Alberts, J. R. (1989) · Animal Behaviour · doi:10.1016/0003-3472(89)90044-4 · Cited by 78 · see citing works
Oxytocin Changes in Males over the Reproductive Cycle in the Monogamous, Biparental California Mouse, Peromyscus californicus
Gubernick, D. J., Winslow, J. T., Jensen, P., Jeannotte, L. A., & Bowen, J. (1995) · Hormones and Behavior · doi:10.1006/hbeh.1995.1005 · Cited by 78 · see citing works
Postpartum factors related to mother's attraction to newborn infant odors
Fleming, A. S., Corter, C. M., Franks, P. W., Surbey, M., Schneider, B. A., & Steiner, M. S. (1993) · Developmental Psychobiology · doi:10.1002/dev.420260204 · Cited by 76 · see citing works
Estradiol and parental experience, but not prolactin are necessary for ultrasound recognition and pup-retrieving in the mouse
Koch, M., & Ehret, G. (1989) · Physiology & Behavior · doi:10.1016/0031-9384(89)90293-x · Cited by 76 · see citing works
Personality characteristics and platelet MAO activity in women with congenital adrenal hyperplasia (CAH)
Helleday, J., Edman, G., Ritzén, E. M., & Siwers, B. (1993) · Psychoneuroendocrinology · doi:10.1016/0306-4530(93)90010-i · Cited by 74 · see citing works
Social and hormonal factors influencing infanticide and its suppression in adult male Long-Evans rats (Rattus norvegicus).
Brown, R. E. (1986) · Journal of comparative psychology · doi:10.1037/0735-7036.100.2.155 · Cited by 72 · see citing works
Prenatal stress and maternal behavior in intact virgin rats: Response latencies are decreased in males and increased in females
Kinsley, C. H. (1988) · Hormones and Behavior · doi:10.1016/0018-506x(88)90032-3 · Cited by 72 · see citing works
A comparative systems model of the regulation of maternal motivation in mammals
Pryce, C. R. (1992) · Animal Behaviour · doi:10.1016/s0003-3472(05)80102-2 · Cited by 71 · see citing works
The development, inhibition and disinhibition of pup-cannibalism in the Mongolian gerbil
Elwood, R. W. (1980) · Animal Behaviour · doi:10.1016/s0003-3472(80)80107-2 · Cited by 71 · see citing works
Pup cannibalism: One aspect of maternal behavior in golden hamsters.
Day, C. S., & Galef, B. G. (1977) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0077386 · Cited by 70 · see citing works
Behavioural similarities between mother rats and benzodiazepine-treated non-meternal animals
Hansen, S., Ferreira, A., & Selart, M. E. (1985) · Psychopharmacology · doi:10.1007/bf00432226 · Cited by 67 · see citing works
Importance of mother/young contact at parturition and across lactation for the expression of maternal behavior in rabbits
González‐Mariscal, G., Melo, Á. I., Chirino, R., Jim�nez, P., Beyer, C., & Rosenblatt, J. S. (1998) · Developmental Psychobiology · doi:10.1002/(sici)1098-2302(199803)32:2 · Cited by 67 · see citing works
Inhibition of infanticide after mating by wild male house mice
McCarthy, M. M., & Saal, F. S. V. (1986) · Physiology & Behavior · doi:10.1016/0031-9384(86)90004-1 · Cited by 67 · see citing works
Parent-Young Contact in Prairie and Meadow Voles
Wilson, S. C. (1982) · Journal of Mammalogy · doi:10.2307/1380642 · Cited by 67 · see citing works
Changes in responsiveness to young in the adult mouse. I. The problematical effect of hormones
Noirot, É. (1964) · Animal Behaviour · doi:10.1016/0003-3472(64)90102-2 · Cited by 66 · see citing works
The effect of gonadal hormones in infancy on maternal behavior in the adult rat*1
Quadagno, D. M. (1972) · Hormones and Behavior · doi:10.1016/0018-506x(72)90007-4 · Cited by 66 · see citing works
Effects of neonatal castration and testosterone on the rat's pup-killing behavior and activity
Rosenberg, K. M., Denenberg, V. H., ZARROW, M. X., & Frank, B. L. (1971) · Physiology & Behavior · doi:10.1016/0031-9384(71)90315-5 · Cited by 65 · see citing works
Sexually dimorphic aspects of spontaneous activity in meadow voles (Microtus pennsylvanicus): Effects of exposure to fox odor.
Perrot-Sinal, T. S., Heale, V. R., Ossenkopp, K., & Kavaliers, M. (1996) · Behavioral Neuroscience · doi:10.1037/0735-7044.110.5.1126 · Cited by 64 · see citing works
Developmental changes in pre‐adult behavior in confined colonies of golden hamsters
Goldman, L., & Swanson, H. H. (1975) · Developmental Psychobiology · doi:10.1002/dev.420080206 · Cited by 64 · see citing works
Postpartum and lactational estrus: A comparative analysis in rodentia.
Gilbert, A. N. (1984) · Journal of comparative psychology · doi:10.1037/0735-7036.98.3.232 · Cited by 64 · see citing works
Nursing posture is elicited rapidly in maternally naive, haloperidol-treated female and male rats in response to ventral trunk stimulation from active pups
Stern, J. M. (1991) · Hormones and Behavior · doi:10.1016/0018-506x(91)90017-c · Cited by 63 · see citing works
The Relationships between Mammalian Young and Conspecifics other than Mothers and Peers: A Review
Spencer‐Booth, Y. (1971) · Advances in the study of behavior · doi:10.1016/s0065-3454(08)60156-4 · Cited by 62 · see citing works
Postpartum and lactational estrus: A comparative analysis in rodentia.
Gilbert, A. N. (1984) · Journal of comparative psychology · doi:10.1037//0735-7036.98.3.232 · Cited by 62 · see citing works
Communal nesting in prairie voles (Microtus ochrogaster): formation, composition, and persistence of communal groups
Getz, L. L., & McGuire, B. (1997) · Canadian Journal of Zoology · doi:10.1139/z97-065 · Cited by 62 · see citing works
Roles of the main olfactory and vomeronasal systems in the response of the female hamster to young
Marques, D. M. (1979) · Behavioral and Neural Biology · doi:10.1016/s0163-1047(79)91300-1 · Cited by 60 · see citing works
Maternal behaviour in non-maternal golden hamsters (Mesocricetus auratus)
Rowell, T. E. (1961) · Animal Behaviour · doi:10.1016/0003-3472(61)90043-4 · Cited by 60 · see citing works
Effects of the Selective Serotonin Reuptake Inhibitor Fluoxetine on Social Behaviors in Male and Female Prairie Voles (Microtus ochrogaster)
Villalba, C., Boyle, P. A., Caliguri, E. J., & Vries, G. J. D. (1997) · Hormones and Behavior · doi:10.1006/hbeh.1997.1420 · Cited by 59 · see citing works
Infanticide and parental behavior in wild female house mice: Effects of ovariectomy, adrenalectomy and administration of oxytocin and prostaglandin F2α
McCarthy, M. M., Bare, J. E., & Saal, F. S. V. (1986) · Physiology & Behavior · doi:10.1016/0031-9384(86)90066-1 · Cited by 58 · see citing works
Sexually dimorphic behavior in group-housed rhesus monkeys (Macaca mulatta) at 1 year of age
Lovejoy, J. C., & Wallen, K. (1988) · Psychobiology · doi:10.3758/bf03327332 · Cited by 57 · see citing works
Maternal behaviour in the golden hamster: responsiveness to young in virgin, pregnant, and lactating females
Richards, M. P. M. (1966) · Animal Behaviour · doi:10.1016/s0003-3472(66)80088-x · Cited by 57 · see citing works
Neonatal gonadal hormones: Effect on maternal and sexual behavior in the female rat☆
Quadagno, D. M., MCCULLOUGH, J., KANHWAHO, G., & Spevak, A. M. (1973) · Physiology & Behavior · doi:10.1016/0031-9384(73)90357-0 · Cited by 56 · see citing works
MATERNAL BEHAVIOR IN HYPOPHYSECTOMIZED MALE AND FEMALE MICE
Leblond, C. P., & Nelson, W. O. (1937) · American Journal of Physiology-Legacy Content · doi:10.1152/ajplegacy.1937.120.1.167 · Cited by 56 · see citing works
The preoptic area/anterior hypothalamus of different strains of mice: sex differences and development
Brown, A. E., Mani, S. K., & Tobet, S. A. (1999) · Developmental Brain Research · doi:10.1016/s0165-3806(99)00061-9 · Cited by 55 · see citing works
Maternal behavior priming in virgin and caesarean-delivered Long-Evans rats: Effects of brief contact or continuous exteroceptive pup stimulation☆
STERN, J. (1983) · Physiology & Behavior · doi:10.1016/0031-9384(83)90271-8 · Cited by 55 · see citing works
Social influences on parental and nonparental responses toward pups in virgin female prairie voles (Microtus ochrogaster).
Lonstein, J. S., & Vries, G. J. D. (2001) · Journal of comparative psychology · doi:10.1037/0735-7036.115.1.53 · Cited by 55 · see citing works
Nest attendance in male meadow voles: the role of the female in regulating male interactions with pups
Storey, A. E., Bradbury, C. G. J., & Joyce, T. L. (1994) · Animal Behaviour · doi:10.1006/anbe.1994.1142 · Cited by 55 · see citing works
Effects of maternal diet, body weight and body composition on infanticide in Syrian hamsters
Schneider, J. E., & Wade, G. N. (1989) · Physiology & Behavior · doi:10.1016/0031-9384(89)90042-5 · Cited by 53 · see citing works
Social Learning of a Food Preference in Male and Female Mongolian Gerbils is Facilitated by the Anxiolytic, Chlordiazepoxide
Choleris, E. (1998) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(98)00005-7 · Cited by 53 · see citing works
Influence of gonadal hormones on the development of parental behavior in adult virgin prairie voles (Microtus ochrogaster)
Lonstein, J. S., & Vries, G. J. D. (2000) · Behavioural Brain Research · doi:10.1016/s0166-4328(00)00192-3 · Cited by 52 · see citing works
Genetic mediation of infanticide and parental behavior in male and female domestic and wild stock house mice
Perrigo, G. H., Belvin, L., Quindry, P., Kadir, T., Becker, J. A., van Look, C., Niewoehner, J., & Saal, F. S. V. (1993) · Behavior Genetics · doi:10.1007/bf01068143 · Cited by 52 · see citing works
Male identity and enclosure size affect paternal attendance of meadow voles, Microtus pennsylvanicus
Storey, A. E., & Snow, D. T. (1987) · Animal Behaviour · doi:10.1016/s0003-3472(87)80265-8 · Cited by 52 · see citing works
Infanticide in the male rat: the role of the vomeronasal organ.
Mennella, J., & Moltz, H. (1988) · Physiology and Behavior · doi:10.1016/0031-9384(88)90087-x · Cited by 52 · see citing works
Parenting and potency: alternative routes to reproductive success in male Mongolian gerbils
Clark, M. M., DeSousa, D., Vonk, J. M., & Galef, B. G. (1997) · Animal Behaviour · doi:10.1006/anbe.1997.0468 · Cited by 52 · see citing works
Experiential Factors in Postpartum Regulation of Maternal Care
Fleming, A. S., Morgan, H. D., & Walsh, C. J. (1996) · Advances in the study of behavior · doi:10.1016/s0065-3454(08)60336-8 · Cited by 51 · see citing works
Infanticide: Accounting for genetic variation in mice
Svare, B. B., Kinsley, C. H., Mann, M. A., & Broida, J. P. (1984) · Physiology & Behavior · doi:10.1016/0031-9384(84)90024-6 · Cited by 51 · see citing works
An observational study of caretaking behavior of male and female mice housed together
Priestnall, R., & Young, S. M. (1978) · Developmental Psychobiology · doi:10.1002/dev.420110107 · Cited by 50 · see citing works
Changes in responsiveness to young in the adult mouse: V. Priming
Noirot, É. (1969) · Animal Behaviour · doi:10.1016/0003-3472(69)90161-4 · Cited by 50 · see citing works
Distribution of small vasopressinergic neurons in golden hamsters
Ferris, C. F., Delville, Y., MILLER, M. A., Dorsa, D. M., & Vries, G. J. D. (1995) · The Journal of Comparative Neurology · doi:10.1002/cne.903600404 · Cited by 50 · see citing works
Effects of neonatal RU486 on adult sexual, parental, and fearful behaviors in rats.
Lonstein, J. S., Quadros, P. S., & Wagner, C. K. (2001) · Behavioral Neuroscience · doi:10.1037/0735-7044.115.1.58 · Cited by 49 · see citing works
Care of young under communal conditions in the mouse (MUS MUSCULUS)
Gandelman, R. J., Paschke, R. E., ZARROW, M. X., & Denenberg, V. H. (1970) · Developmental Psychobiology · doi:10.1002/dev.420030405 · Cited by 49 · see citing works
The Family Group in Golden Hamsters: Its Formation and Break-Up
Rowell, T. E. (1961) · Behaviour · doi:10.1163/156853961x00015 · Cited by 49 · see citing works
Maternal behaviour in virgin female golden hamsters (Mesocricetus auratus waterhouse): the role of the age of the test pup
Richards, M. P. M. (1966) · Animal Behaviour · doi:10.1016/s0003-3472(66)80087-8 · Cited by 49 · see citing works
Individual differences in aggressiveness of female hamsters: Response to intact and castrated males and to females
Marques, D. M., & Valenstein, E. S. (1977) · Animal Behaviour · doi:10.1016/0003-3472(77)90075-6 · Cited by 48 · see citing works
Facial Receptive Fields of Trigeminal Neurons: Increased Size Following Estrogen Treatment in Female Rats
Bereiter, D. A., & Barker, D. J. (2008) · Neuroendocrinology · doi:10.1159/000122389 · Cited by 48 · see citing works
Hormones and maternal behavior in the male rat*1
Lubin, M. (1972) · Hormones and Behavior · doi:10.1016/0018-506x(72)90026-8 · Cited by 48 · see citing works
Incidence of pup killing and parental behavior in virgin female and male rats (Rattus norvegicus): differences between Wistar and Sprague-Dawley stocks.
Jakubowski, M., & Terkel, J. (1985) · PubMed · Cited by 47 · see citing works
A neuroanatomical correlate of paternal and maternal behavior in the biparental California mouse (Peromyscus californicus).
Gubernick, D. J., Sengelaub, D. R., & Kurz, E. M. (1993) · Behavioral Neuroscience · doi:10.1037//0735-7044.107.1.194 · Cited by 47 · see citing works
The ontogeny of maternal responsiveness in female Rockland-Swiss albino mice
Gandelman, R. J. (1973) · Hormones and Behavior · doi:10.1016/0018-506x(73)90010-x · Cited by 46 · see citing works
Suppression of Infanticide in Mother Rats.
Peters, L. C., & Kristal, M. B. (1983) · Journal of comparative psychology · doi:10.1037/0735-7036.97.2.167 · Cited by 46 · see citing works
Maternal behaviour in virgin female golden hamsters: Changes consequent upon initial contact with pups
Noirot, É., & Richards, M. (1966) · Animal Behaviour · doi:10.1016/s0003-3472(66)80003-9 · Cited by 46 · see citing works
The role of neonatal androgen in the expression of hormonally induced maternal responsiveness in the adult rat
Bridges, R. S., ZARROW, M. X., & Denenberg, V. H. (1973) · Hormones and Behavior · doi:10.1016/0018-506x(73)90031-7 · Cited by 46 · see citing works
Development of maternal behavior in nulliparous rats (Rattus norvegicus): Effects of sex and early maternal experience.
Gray, P., & Chesley, S. (1984) · Journal of comparative psychology · doi:10.1037//0735-7036.98.1.91 · Cited by 46 · see citing works
The development of cannibalism in male Rockland‐Swiss mice and the influence of olfactory bulb removal
Gandelman, R. J. (1973) · Developmental Psychobiology · doi:10.1002/dev.420060210 · Cited by 46 · see citing works
Incidence of pup killing and parental behavior in virgin female and male rats (Rattus norvegicus): Differences between Wistar and Sprague-Dawley stocks.
Jakubowski, M., & Terkel, J. (1985) · Journal of comparative psychology · doi:10.1037/0735-7036.99.1.93 · Cited by 45 · see citing works
Role of social and endocrine factors in alloparental behavior of prairie voles (Microtus ochrogaster)
Roberts, R. L., Miller, A. K., Taymans, S. E., & Carter, C. S. (1998) · Canadian Journal of Zoology · doi:10.1139/cjz-76-10-1862 · Cited by 44 · see citing works
Neuronal and behavioral differences between Mus musculus domesticus (C57BL/6JBy) and Mus musculus castaneus (CAST/Ei)
Roy, I. L., Roubertoux, P. L., Jamot, L., Maarouf, F., Tordjman, S., Mortaud, S., Blanchard, C., Martin, B., Guillot, P. V., & Duquenne, V. (1998) · Behavioural Brain Research · doi:10.1016/s0166-4328(97)00218-0 · Cited by 44 · see citing works
Infanticide in the meadow vole, Microtus pennsylvanicus: Significance in relation to social system and population cycling
Webster, A. B., Gartshore, R. G., & Brooks, R. J. (1981) · Behavioral and Neural Biology · doi:10.1016/s0163-1047(81)91394-7 · Cited by 44 · see citing works
Development of maternal behaviors in prepubertal rats at three ages: Age‐characteristic patterns of responses
Brunelli, S. A., Shindledecker, R. D., & Hofer, M. A. (1985) · Developmental Psychobiology · doi:10.1002/dev.420180404 · Cited by 44 · see citing works
Induction of pup killing in female mice by androgenization
Gandelman, R. J. (1972) · Physiology & Behavior · doi:10.1016/0031-9384(72)90273-9 · Cited by 43 · see citing works
Resource Partitioning During Reproduction in the Norway Rat
Woodside, B. C., Wilson, R., Chee, P., & Leon, M. (1981) · Science · doi:10.1126/science.7444451 · Cited by 43 · see citing works
Plasma Prolactin Concentrations in Parental Male and Female Rats: Effects of Exposure to Rat Young*
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Paternal Care Reduces Maternal Hyperthermia in Djungarian Hamsters (Phodopus campbelli)
Walton, J. (1997) · Physiology & Behavior · doi:10.1016/s0031-9384(97)00385-5 · Cited by 43 · see citing works
Another hamster paradox: More males carry pups and fewer kill and cannibalize young than do females.
Marques, D. M., & Valenstein, E. S. (1976) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0077229 · Cited by 42 · see citing works
ON THE RETRIEVING OF YOUNG AND OTHER BEHAVIOUR IN LACTATING GOLDEN HAMSTERS
Rowell, T. E. (1960) · Proceedings of the Zoological Society of London · doi:10.1111/j.1469-7998.1960.tb05845.x · Cited by 42 · see citing works
A comparison of hypothalami of rats and mice: lack of gross sexual dimorphism in the mouse
Young, J. K. (1982) · Brain Research · doi:10.1016/0006-8993(82)90844-7 · Cited by 42 · see citing works
Paternal Care in Canids
Malcolm, J. (1985) · American Zoologist · doi:10.1093/icb/25.3.853 · Cited by 41 · see citing works
Hormonal influences during the ontogeny of maternal behavior in female rats.
Mayer, A. D., & Rosenblatt, J. S. (1979) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0077622 · Cited by 41 · see citing works
Development of maternal behavior in nulliparous rats (Rattus norvegicus): Effects of sex and early maternal experience.
Gray, P., & Chesley, S. (1984) · Journal of comparative psychology · doi:10.1037/0735-7036.98.1.91 · Cited by 41 · see citing works
Stimulus control of cannibalism and maternal behavior in anosmic mice
Gandelman, R. J., ZARROW, M. X., & Denenberg, V. H. (1971) · Physiology & Behavior · doi:10.1016/0031-9384(71)90112-0 · Cited by 40 · see citing works
Sex Differences in Function of a Pheromonally Stimulated Pathway: Role of Steroids and the Main Olfactory System
Swann, J. M., & Fiber, J. M. (1997) · Brain Research Bulletin · doi:10.1016/s0361-9230(97)00220-7 · Cited by 39 · see citing works
Some effects of strain differences in the maternal behavior of inbred mice
Ward, R. M. (1980) · Developmental Psychobiology · doi:10.1002/dev.420130209 · Cited by 39 · see citing works
Transition from pup killing to parental behavior in male and virgin female albino rats
Jakubowski, M., & Terkel, J. (1985) · Physiology & Behavior · doi:10.1016/0031-9384(85)90364-6 · Cited by 39 · see citing works
Intrauterine position modulates maternal behaviors in female mice
Kinsley, C. H., Konen, C., Miele, J., Ghiraldi, L. L., & Svare, B. B. (1986) · Physiology & Behavior · doi:10.1016/0031-9384(86)90434-8 · Cited by 39 · see citing works
Sexual Differentiation of Behavior in the Context of Developmental Psychobiology
Yahr, P. (1988) · Handbook of behavioral neurobiology · doi:10.1007/978-1-4684-5421-5_6 · Cited by 38 · see citing works
Mother-weanling interactions in norway rats in the presence of a successive litter produced by postpartum mating☆
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Effects of oestrogen and progesterone on nest building in the golden hamster
Richards, M. P. M. (1969) · Animal Behaviour · doi:10.1016/0003-3472(69)90022-0 · Cited by 37 · see citing works
Changes in Responsiveness To Young in the Adult Mouse Iii. the Effect of Immediately Preceding Performances
Noirot, É. (1965) · Behaviour · doi:10.1163/156853965x00084 · Cited by 37 · see citing works
A neuroanatomical correlate of paternal and maternal behavior in the biparental California mouse (Peromyscus californicus).
Gubernick, D. J., Sengelaub, D. R., & Kurz, E. M. (1993) · Behavioral Neuroscience · doi:10.1037/0735-7044.107.1.194 · Cited by 37 · see citing works

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Oxytocin and social affiliation in humans
Feldman, R. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2012.01.008 · Cited by 767 · see citing works
Galanin neurons in the medial preoptic area govern parental behaviour
Wu, Z., Autry, A. E., Bergan, J. F., Watabe‐Uchida, M., & Dulac, C. G. (2014) · Nature · doi:10.1038/nature13307 · Cited by 593 · see citing works
Sexual selection and animal personality
Schuett, W., Tregenza, T., & Dall, S. R. X. (2009) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/j.1469-185x.2009.00101.x · Cited by 549 · see citing works
Oxytocin, motivation and the role of dopamine
Love, T. M. (2014) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2013.06.011 · Cited by 369 · see citing works
Developmental consequences of oxytocin
Carter, C. S. (2003) · Physiology & Behavior · doi:10.1016/s0031-9384(03)00151-3 · Cited by 367 · see citing works
From house mouse to mouse house: the behavioural biology of free-living Mus musculus and its implications in the laboratory
Latham, N., & Mason, G. J. (2004) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2004.02.006 · Cited by 338 · see citing works
Comparing postnatal development of gonadal hormones and associated social behaviors in rats, mice, and humans
Bell, M. R. (2018) · Endocrinology · doi:10.1210/en.2018-00220 · Cited by 308 · see citing works
Sensory, hormonal, and neural control of maternal aggression in laboratory rodents
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Parental Behaviour
Luis, J., & Romero‐Morales, L. (2022) · Routledge eBooks · doi:10.4324/9781003091868-18

Authors: Lonstein, J. S., & De Vries, G. J.
Affiliations: University of Massachusetts Amherst (US)
Corresponding author: Lonstein, Joseph S.
ORCID: Lonstein, Joseph S.
Venue: Neuroscience & Biobehavioral Reviews
Publisher: Elsevier BV
Published: 2000-08
Volume: 24
Issue: 6
Pages: 669-686
ISSN: 0149-7634 (ISSN-L)
DOI: 10.1016/s0149-7634(00)00036-1
OpenAlex: W2035785773
Cited by: 226
References: 264
Citations by year: 2026: 5 · 2025: 9 · 2024: 9 · 2023: 13 · 2022: 10 · 2021: 9 · 2020: 11 · 2019: 6 · 2018: 9 · 2017: 11 · 2016: 15 · 2015: 11 · 2014: 9 · 2013: 12 · 2012: 8
FWCI: 1.65
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Neuroscience & Biobehavioral Reviews (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health
U.S. Public Health Service (08392, 47538)
National Institute of Mental Health
National Institute of Child Health and Human Development
Topics: Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Sexual Differentiation and Disorders
Keywords: sex differences, parental care, paternal behavior, rodents, rats, mice, voles, gerbils, hamster, hormones, developmental processes, social experience
MeSH terms: Animals, Female, Male, Maternal Behavior, Paternal Behavior, Rodentia, Sex Characteristics

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Sex differences in the parental behavior of rodents

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