The impact of early life family structure on adult social attachment, alloparental behavior, and the neuropeptide systems regulating affiliative behaviors in the monogamous prairie vole (Microtus ochrogaster)

Ahern, Todd H

doi:10.3389/neuro.08.017.2009

Cited by 246Neuroendocrine regulation and behaviorAnimal Behavior and ReproductionHuman-Animal Interaction Studies

The impact of early life family structure on adult social attachment, alloparental behavior, and the neuropeptide systems regulating affiliative behaviors in the monogamous prairie vole (Microtus ochrogaster)

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Ahern, Todd H·2009·Frontiers in Behavioral Neuroscience

DOI 10.3389/neuro.08.017.2009PMC PMC2742665

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Abstract

Early social attachments lie at the heart of emotional and social development in many mammals, including humans. In nature, monogamous prairie voles (Microtus ochrogaster) experience considerable natural variation in early social attachment opportunities due to differences in family structure [e.g., single-mothers (SM), solitary breeding pairs, and communal groups]. We exploited some of this natural variation in family structure to examine the influence of early social environment on the development of adult social behavior. First, we characterized the parental care received by pups reared biparentally (BP) or by SM in the laboratory. Second, we examined whether BP- and SM-reared offspring differed in adult nurturing, bonding, and emotional behaviors. Finally, we investigated the effects of rearing condition on neuropeptide systems that regulate adult social behavior [oxytocin (OT), vasopressin, and corticotropin-releasing factor, (CRF)]. Observations revealed that SM-reared pups were exposed more frequently (P < 0.01), licked and groomed less (P < 0.01), and matured more slowly (P < 0.01) than BP-reared pups. In adulthood, there were striking socio-behavioral differences: SM-reared females showed low spontaneous, pup-directed alloparental behavior (P < 0.01) and both males and females from the SM-reared condition showed delayed partner preference formation. While rearing did not impact neuropeptide receptor densities in the ventral forebrain as we predicted, SM-reared animals, particularly females, had increased OT content (P < 0.01) and greater dorsal raphe CRF2 densities (P < 0.05) and both measures correlated with licking and grooming experienced during the first 10 days of life. These results suggest that naturalistic variation in social rearing conditions can introduce diversity into adult nurturing and attachment behaviors.

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Prairie voles raised with biparental care form more pronounced pair bonds in adulthood than those raised by a mother alone.
“As mentioned previously, prairie voles raised with biparental care, compared to those raised by a mother alone, form more pronounced pair bonds in adulthood.”
From The Neurobiology of Love and Pair Bonding from Human and Animal Perspectives (2023) · cites this paper as [64]
The Results (Adult partner preference formation; page unavailable) show that biparentally reared voles of both sexes developed a partner preference after 24 hours, while mother-only-reared voles did not show one until one week. The Discussion describes this as a delayed onset in the mother-only group, not evidence that their eventual pair bonds were less pronounced. (LLM, conf=0.86)
Experimental — accuracy not yet measured
Manipulation of OT/AVP levels via direct exposures to exogenous hormones, agonists, or alteration of the social environment can significantly modify the number of OT, AVP, and TH neurons in the PVN, resulting in anxiety-like behavior and alterations of prototypical male and female sociosexual behavior.
“Manipulation of OT/AVP levels via direct exposures to exogenous hormones, agonists, or alteration of the social environment can significantly modify the number of OT, AVP, and TH neurons in the PVN, thereby resulting in anxiety-like behavior and alterations of prototypical male and female sociosexual behavior (123–127).”
From Endocrine Disruption of Vasopressin Systems and Related Behaviors (2017) · cites this paper as [125]
Split into 2 atoms — 0 confirmed, 2 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.
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In adulthood, voles raised by a single mother are slower to form a preference for their partner despite normal mating behavior.
“In adulthood, these same animals are slower to form a preference for their partner, despite normal mating behavior.”
From The Neurobiology of Love and Pair Bonding from Human and Animal Perspectives (2023) · cites this paper as [64]
Voles raised by their mother alone receive less parental nurturing in the form of licking/grooming early in development than those raised under biparental care.
“Voles raised by their mother alone, compared to those raised under biparental care, receive less parental nurturing in the form of licking/grooming early in development [64].”
From The Neurobiology of Love and Pair Bonding from Human and Animal Perspectives (2023) · cites this paper as [64]
The quality of early life nurturing received can have life-long consequences on adult social behavioral tendencies.
“There is now growing evidence that the quality of early life nurturing received can have life-long consequences on adult social behavioral tendencies.”
From The prairie vole: An emerging model organism for understanding the social brain (2010) · cites this paper as [39]

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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
The Effects of Mate Removal on Pregnancy Success in Prairie Voles (Microtus Ochrogaster) and Meadow Voles (Microtus Pennsylvanicus)1
McGuire, B., Russell, K., Mahoney, T. P. F., & Novak, M. A. (1992) · Biology of Reproduction · doi:10.1095/biolreprod47.1.37 · Cited by 51 · see citing works
Effects of neonatal oxytocin manipulations on male reproductive potential in prairie voles
BALES, K., ABDELNABI, M., CUSHING, B., OTTINGER, M., & CARTER, C. (2004) · Physiology & Behavior · doi:10.1016/j.physbeh.2004.02.016 · Cited by 47 · see citing works
The Pairbond in the Titi Monkey (Callicebus moloch): Intrinsic versus Extrinsic Contributions of the Pairmates
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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
Attachment, ethology and adult psychotherapy
Sable, P. (2004) · Attachment & Human Development · doi:10.1080/14616730410001663498 · Cited by 33 · see citing works
Sex Differences, Effects of Male Presence and Coordination of Nest Visits in Prairie Voles (Microtus ochrogaster) During the Immediate Postnatal Period
McGuire, B., PARKER, E., & Bemis, W. E. (2007) · The American Midland Naturalist · doi:10.1674/0003-0031(2007)157[187:sdeomp]2.0.co;2 · Cited by 26 · see citing works
Exploratory Behavior Correlates with Social Organization and Is Responsive to Peptide Injections in Prairie Voles
Dharmadhikari, A., LEE, Y. S., Roberts, R. L., & Carter, C. S. (1997) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1997.tb51982.x · Cited by 23 · see citing works
Sex differences in DSM-III-R, Axis II—Personality disorders
Ekselius, L., Bodlund, O., von Knorring, L., Lindström, E., & Kullgren, G. (1996) · Personality and Individual Differences · doi:10.1016/0191-8869(95)00201-4 · Cited by 17 · see citing works
Facilitation of affiliation and pair-bond formation by vasopressin receptor gene transfer into the ventral forebrain of a monogamous vole
(2001) · Nature · doi:10.1038/news010927-4 · Cited by 11 · see citing works
Effect of neonatal handling and paternal care on offspring cognitive development in the monogamous California mouse (Peromyscus californicus)
Bredy, T. W. (2004) · Hormones and Behavior · doi:10.1016/s0018-506x(04)00060-1 · Cited by 5 · see citing works

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Oxytocin-dependent consolation behavior in rodents
Burkett, J. P., Andari, E., Johnson, Z. V., Curry, D. C., de Waal, F. B. M., & Young, L. J. (2016) · Science · doi:10.1126/science.aac4785 · Cited by 692 · see citing works
Natural variations in maternal and paternal care are associated with systematic changes in oxytocin following parent–infant contact
Feldman, R., Gordon, I., Schneiderman, I., Weisman, O., & Zagoory-Sharon, O. (2010) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2010.01.013 · Cited by 638 · see citing works
Maternal and paternal plasma, salivary, and urinary oxytocin and parent–infant synchrony: considering stress and affiliation components of human bonding
Feldman, R., Gordon, I., & Zagoory‐Sharon, O. (2011) · Developmental Science · doi:10.1111/j.1467-7687.2010.01021.x · Cited by 486 · see citing works
Oxytocin and the development of parenting in humans
Gordon, I., Zagoory-Sharon, O., Leckman, J. F., & Feldman, R. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.02.005 · Cited by 469 · see citing works
Exogenous and evoked oxytocin restores social behavior in the Cntnap2 mouse model of autism
Peñagarikano, O., Lázaro, M. T., Lu, X.-H., Gordon, A., Dong, H., Lam, H. A., Peles, E., Maidment, N. T., Murphy, N. P., Yang, X. W., et al. (2015) · Science Translational Medicine · doi:10.1126/scitranslmed.3010257 · Cited by 378 · see citing works
The neurobiology of pair bonding: Insights from a socially monogamous rodent
Young, K. A., Gobrogge, K. L., Liu, Y., & Wang, Z. (2011) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2010.07.006 · Cited by 389 · see citing works
Stress, social behavior, and resilience: Insights from rodents
Beery, A. K., & Kaufer, D. (2014) · Neurobiology of Stress · doi:10.1016/j.ynstr.2014.10.004 · Cited by 373 · see citing works
The prairie vole: An emerging model organism for understanding the social brain
McGraw, L. A., & Young, L. J. (2010) · Trends in Neurosciences · doi:10.1016/j.tins.2009.11.006 · Cited by 276 · see citing works
Chronic intranasal oxytocin causes long-term impairments in partner preference formation in male prairie voles
Bales, K. L., Perkeybile, A. M., Conley, O. G., Lee, M. H., Guoynes, C. D., Downing, G. M., Yun, C. R., Solomon, M., Jacob, S., & Mendoza, S. P. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.08.025 · Cited by 265 · see citing works
Towards a neuroscience of empathy: Ontogeny, phylogeny, brain mechanisms, context and psychopathology
Gonzalez-Liencres, C., Shamay‐Tsoory, S., & Brüne, M. (2013) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2013.05.001 · Cited by 264 · see citing works
Influence of maternal care on the developing brain: Mechanisms, temporal dynamics and sensitive periods
Curley, J. P., & Champagne, F. A. (2015) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2015.11.001 · Cited by 257 · see citing works
The cross-generation transmission of oxytocin in humans
Feldman, R., Gordon, I., & Zagoory-Sharon, O. (2010) · Hormones and Behavior · doi:10.1016/j.yhbeh.2010.06.005 · Cited by 256 · see citing works
Constraints and flexibility in mammalian social behaviour: introduction and synthesis
Kappeler, P. M., Barrett, L., Blumstein, D. T., & Clutton-Brock, T. H. (2013) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2012.0337 · Cited by 206 · see citing works
Social influences on neurobiology and behavior: Epigenetic effects during development
Curley, J. P., Jensen, C. L., Rahia Mashoodh, A., & Champagne, F. A. (2010) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2010.06.005 · Cited by 195 · see citing works
Neurobiological mechanisms of social attachment and pair bonding
Johnson, Z. V., & Young, L. J. (2015) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2015.01.009 · Cited by 169 · see citing works
Fathering in rodents: Neurobiological substrates and consequences for offspring
Bales, K. L., & Wendy Saltzman, A. (2015) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.05.021 · Cited by 167 · see citing works
Increasing oxytocin receptor expression in the nucleus accumbens of pre-pubertal female prairie voles enhances alloparental responsiveness and partner preference formation as adults
Keebaugh, A. C., & Young, L. J. (2011) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.07.018 · Cited by 154 · see citing works
Oxytocin and Social Relationships: From Attachment to Bond Disruption
Bosch, O. J., & Young, L. J. (2017) · Current Topics in Behavioral Neurosciences · doi:10.1007/7854_2017_10 · Cited by 162 · see citing works
Oxytocin, cortisol, and triadic family interactions
Gordon, I., Zagoory-Sharon, O., Leckman, J. F., & Feldman, R. (2010) · Physiology & Behavior · doi:10.1016/j.physbeh.2010.08.008 · Cited by 158 · see citing works
RNAi knockdown of oxytocin receptor in the nucleus accumbens inhibits social attachment and parental care in monogamous female prairie voles
Keebaugh, A. C., Barrett, C. E., Laprairie, J. L., Jenkins, J. J., & Young, L. J. (2015) · Social Neuroscience · doi:10.1080/17470919.2015.1040893 · Cited by 150 · see citing works
Epigenetics for behavioral ecologists
Ledón‐Rettig, C. C., Richards, C. L., & Martin, L. B. (2012) · Behavioral Ecology · doi:10.1093/beheco/ars145 · Cited by 156 · see citing works
Toward understanding how early-life social experiences alter oxytocin- and vasopressin-regulated social behaviors
Veenema, A. H. (2011) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.12.002 · Cited by 157 · see citing works
Paternal Influences on Offspring Development: Behavioural and Epigenetic Pathways
Braun, K., & Champagne, F. A. (2014) · Journal of Neuroendocrinology · doi:10.1111/jne.12174 · Cited by 157 · see citing works
Individual differences underlying susceptibility to addiction: Role for the endogenous oxytocin system
Buisman‐Pijlman, F. T. A., Sumracki, N. M., Gordon, J. J., Hull, P. R., Carter, C. S., & Mattie Tops, A. (2013) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2013.09.005 · Cited by 143 · see citing works
Developmental experiences and the oxytocin receptor system
Bales, K. L., & Perkeybile, A. M. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.12.013 · Cited by 142 · see citing works
Oxytocin in the nucleus accumbens shell reverses CRFR2-evoked passive stress-coping after partner loss in monogamous male prairie voles
Bosch, O. J., Dabrowska, J., Modi, M. E., Johnson, Z. V., Keebaugh, A. C., Barrett, C. E., Ahern, T. H., Guo, J., Grinevich, V., Rainnie, D. G., et al. (2016) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2015.11.011 · Cited by 140 · see citing works
Long-term exposure to intranasal oxytocin in a mouse autism model
Bales, K. L., Solomon, M., Jacob, S., Crawley, J. N., Silverman, J. L., Larke, R. H., Sahagún, E., Puhger, K. R., Pride, M. C., & Mendoza, S. P. (2014) · Translational Psychiatry · doi:10.1038/tp.2014.117 · Cited by 131 · see citing works
Ontogenesis of oxytocin pathways in the mammalian brain: late maturation and psychosocial disorders
Grinevich, V., Desarménien, M. G., Chini, B., Tauber, M., & Muscatelli, F. (2015) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2014.00164 · Cited by 121 · see citing works
The neurobiological causes and effects of alloparenting
Kenkel, W. M., Perkeybile, A. M., & Carter, C. S. (2016) · Developmental Neurobiology · doi:10.1002/dneu.22465 · Cited by 120 · see citing works
Oxytocin receptor is not required for social attachment in prairie voles
Berendzen, K. M., Sharma, R., Alvarado, M., Wei, Y., Rogers, F. D., Simmons, T. C., Seelke, A. M. H., Bond, J. M., Larios, R., Goodwin, N. L., et al. (2023) · Neuron · doi:10.1016/j.neuron.2022.12.011 · Cited by 120 · see citing works
The oxytocin system promotes resilience to the effects of neonatal isolation on adult social attachment in female prairie voles
Barrett, C. E., Arambula, S. E., & Young, L. J. (2015) · Translational Psychiatry · doi:10.1038/tp.2015.73 · Cited by 115 · see citing works
Parental division of labor, coordination, and the effects of family structure on parenting in monogamous prairie voles ( Microtus ochrogaster )
Ahern, T. H., Hammock, E. A. D., & Young, L. J. (2011) · Developmental Psychobiology · doi:10.1002/dev.20498 · Cited by 113 · see citing works
Natural variation in early parental care correlates with social behaviors in adolescent prairie voles (Microtus ochrogaster)
Perkeybile, A. M., Griffin, L. L., & Bales, K. L. (2013) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2013.00021 · Cited by 114 · see citing works
The CRF system and social behavior: a review
Hostetler, C. M., & Ryabinin, A. E. (2013) · Frontiers in Neuroscience · doi:10.3389/fnins.2013.00092 · Cited by 105 · see citing works
Effects of continuously enhanced corticotropin releasing factor expression within the bed nucleus of the stria terminalis on conditioned and unconditioned anxiety
Sink, K. S., Walker, D. L., Freeman, S. M., Flandreau, E. I., Ressler, K. J., & Davis, M. (2012) · Molecular Psychiatry · doi:10.1038/mp.2011.188 · Cited by 108 · see citing works
Variation in vasopressin receptor (Avpr1a) expression creates diversity in behaviors related to monogamy in prairie voles
Barrett, C. E., Keebaugh, A. C., Ahern, T. H., Bass, C. E., Terwilliger, E. F., & Young, L. J. (2013) · Hormones and Behavior · doi:10.1016/j.yhbeh.2013.01.005 · Cited by 100 · see citing works
Associations among oxytocin receptor gene (OXTR) DNA methylation in adulthood, exposure to early life adversity, and childhood trajectories of anxiousness
Gouin, J.-P., Zhou, Q. Q., Booij, L., Boivin, M., Côté, S. M., Hébert, M., Ouellet‐Morin, I., Moshe Szyf, A., Tremblay, R. E., Turecki, G., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-07950-x · Cited by 102 · see citing works
CD38 and its role in oxytocin secretion and social behavior
Higashida, H., Yokoyama, S., Kikuchi, M., & Munesue, T. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.12.011 · Cited by 98 · see citing works
μ-Opioid receptors within subregions of the striatum mediate pair bond formation through parallel yet distinct reward mechanisms
Resendez, S. L., Dome, M., Gormley, G., Franco, D., Nevárez, N., Hamid, A. A., & Aragona, B. J. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.4123-12.2013 · Cited by 93 · see citing works
Why and how the early-life environment affects development of coping behaviours
Langenhof, M. R., & Komdeur, J. (2018) · Behavioral Ecology and Sociobiology · doi:10.1007/s00265-018-2452-3 · Cited by 90 · see citing works
Early adverse experience and substance addiction: Dopamine, oxytocin, and glucocorticoid pathways
Kim, S., Kwok, S., Mayes, L. C., Potenza, M. N., Rutherford, H. J. V., & Strathearn, L. (2017) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.13140 · Cited by 85 · see citing works
Lost connections: Oxytocin and the neural, physiological, and behavioral consequences of disrupted relationships
Pohl, T. T., Young, L. J., & Bosch, O. J. (2019) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2017.12.011 · Cited by 83 · see citing works
Local oxytocin expression and oxytocin receptor binding in the male rat brain is associated with aggressiveness
Calcagnoli, F., de Boer, S. F., Beiderbeck, D. I., Althaus, M., Koolhaas, J. M., & Neumann, I. D. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.12.050 · Cited by 84 · see citing works
Neonatal paternal deprivation impairs social recognition and alters levels of oxytocin and estrogen receptor α mRNA expression in the MeA and NAcc, and serum oxytocin in mandarin voles
Cao, Y., Wu, R., Tai, F., Zhang, X., Yu, P., An, X., Qiao, X., & Hao, P. (2013) · Hormones and Behavior · doi:10.1016/j.yhbeh.2013.11.005 · Cited by 82 · see citing works
Melanocortin receptor agonists facilitate oxytocin-dependent partner preference formation in the Prairie Vole
Modi, M. E., Inoue, K., Barrett, C. E., Kittelberger, K. A., Smith, D. G., Landgraf, R., & Young, L. J. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.35 · Cited by 82 · see citing works
Increased anxiety and decreased sociability induced by paternal deprivation involve the PVN-PrL OTergic pathway
He, Z., Young, L., Ma, X.-M., Guo, Q., Wang, L., Yang, Y., Luo, L., Yuan, W., Li, L., Zhang, J., et al. (2019) · eLife · doi:10.7554/elife.44026 · Cited by 81 · see citing works
Intergenerational transmission of alloparental behavior and oxytocin and vasopressin receptor distribution in the prairie vole
Perkeybile, A. M., Delaney-Busch, N., Hartman, S., Grimm, K. J., & Bales, K. L. (2015) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2015.00191 · Cited by 76 · see citing works
Early-life sleep disruption increases parvalbumin in primary somatosensory cortex and impairs social bonding in prairie voles
Jones, C. E., Opel, R. A., Kaiser, M. E., Chau, A. Q., Quintana, J., Nipper, M. A., Finn, D. A., Hammock, E. A. D., & Lim, M. M. (2019) · Science Advances · doi:10.1126/sciadv.aav5188 · Cited by 72 · see citing works
A novel model for neuroendocrine toxicology: neurobehavioral effects of BPA exposure in a prosocial species, the prairie vole (Microtus ochrogaster)
Sullivan, A. W., Beach, E. C., Stetzik, L. A., Perry, A., D'Addezio, A. S., Cushing, B. S., & Patisaul, H. B. (2014) · Endocrinology · doi:10.1210/en.2014-1379 · Cited by 79 · see citing works
Social memory, amnesia, and autism: Brain oxytocin secretion is regulated by NAD+ metabolites and single nucleotide polymorphisms of CD38
Higashida, H., Yokoyama, S., Huang, J., Liu, L., Ma, W., Akther, S., Higashida, C., Kikuchi, M., Minabe, Y., & Munesue, T. (2012) · Neurochemistry International · doi:10.1016/j.neuint.2012.01.030 · Cited by 74 · see citing works
Pathways Relating the Neurobiology of Attachment to Drug Addiction
Strathearn, L., Mertens, C. E., Mayes, L. C., Rutherford, H. J. V., Rajhans, P., Xu, G., Potenza, M. N., & Kim, S. (2019) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2019.00737 · Cited by 71 · see citing works
The Parental Brain
Numan, M. (2020) · doi:10.1093/oso/9780190848675.001.0001 · Cited by 101 · see citing works
Paternal deprivation affects social behaviors and neurochemical systems in the offspring of socially monogamous prairie voles
Tabbaa, M., Lei, K., Liu, Y., & Wang, Z. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2016.12.011 · Cited by 68 · see citing works
The effects of neonatal paternal deprivation on pair bonding, NAcc dopamine receptor mRNA expression and serum corticosterone in mandarin voles
Yu, P., An, S.-C., Tai, F., Zhang, X., He, F., Wang, J., An, X., & Wu, R. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2012.02.028 · Cited by 65 · see citing works
The association between observed non-verbal maternal responses at 12 months and later infant development at 18 months and IQ at 4 years: A longitudinal study
Pearson, R. M., Heron, J., Melotti, R., Joinson, C., Stein, A., Ramchandani, P. G., & Evans, J. (2011) · Infant Behavior and Development · doi:10.1016/j.infbeh.2011.07.003 · Cited by 60 · see citing works
The Neurobiology of Love and Pair Bonding from Human and Animal Perspectives
Blumenthal, S. A., & Young, L. J. (2023) · Biology · doi:10.3390/biology12060844 · Cited by 59 · see citing works
“Furthermore, voles raised by a single mother display decreased turnover of DA in the NAc following cohabitation and mating with an opposite-sex conspecific, suggesting less activity in reward regions during sexual contact [64,65].”
Dynamic modulation of sociality and aggression: an examination of plasticity within endocrine and neuroendocrine systems
Kelly, A. M., & Vitousek, M. N. (2017) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2016.0243 · Cited by 57 · see citing works
The oxytocin system and early‐life experience‐dependent plastic changes
Onaka, T., & Takayanagi, Y. (2021) · Journal of Neuroendocrinology · doi:10.1111/jne.13049 · Cited by 60 · see citing works
Variation, plasticity, and alternative mating tactics: Revisiting what we know about the socially monogamous prairie vole
Madrid, J. E., Parker, K. J., & Ophir, A. G. (2020) · Advances in the study of behavior · doi:10.1016/bs.asb.2020.02.001 · Cited by 55 · see citing works
Endocrine Disruption of Vasopressin Systems and Related Behaviors
Patisaul, H. B. (2017) · Frontiers in Endocrinology · doi:10.3389/fendo.2017.00134 · Cited by 54 · see citing works
A Neuroscientist’s Guide to the Vole
Kenkel, W. M., Gustison, M. L., & Beery, A. K. (2021) · Current Protocols · doi:10.1002/cpz1.175 · Cited by 52 · see citing works
Early life adversity and adult social behavior: focus on arginine vasopressin and oxytocin as potential mediators
Kompier, N. F., Keysers, C., Gazzola, V., Lucassen, P. J., & Krugers, H. J. (2019) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2019.00143 · Cited by 53 · see citing works
Paternal deprivation impairs social behavior putatively via epigenetic modification to lateral septum vasopressin receptor
Kelly, A. M., Ong, J. Y., Witmer, R. A., & Ophir, A. G. (2020) · Science Advances · doi:10.1126/sciadv.abb9116 · Cited by 53 · see citing works
Paternal Deprivation Affects the Development of Corticotrophin‐Releasing Factor‐Expressing Neurones in Prefrontal Cortex, Amygdala and Hippocampus of the BiparentalOctodon degus
Seidel, K., Poeggel, G., Holetschka, R., Helmeke, C., & Braun, K. (2011) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2011.02208.x · Cited by 51 · see citing works
On the role of oxytocin in borderline personality disorder
Brüne, M. (2015) · British Journal of Clinical Psychology · doi:10.1111/bjc.12100 · Cited by 50 · see citing works
Early Social Environment Affects the Endogenous Oxytocin System: A Review and Future Directions
Alves, E., Fielder, A. L., Ghabriel, N., Sawyer, M., & Buisman‐Pijlman, F. T. A. (2015) · Frontiers in Endocrinology · doi:10.3389/fendo.2015.00032 · Cited by 48 · see citing works
Neuropeptide Regulation of Social Attachment: The Prairie Vole Model
Tabbaa, M., Paedae, B., Liu, Y., & Wang, Z. (2016) · Comprehensive physiology · doi:10.1002/cphy.c150055 · Cited by 53 · see citing works
Paraventricular nucleus oxytocin subsystems promote active paternal behaviors in mandarin voles
He, Z., Zhang, L., Hou, W., Zhang, X., Young, L. J., Li, L., Liu, L., Ma, H., Xun, Y., Lv, Z., et al. (2021) · The Journal of Neuroscience · doi:10.1523/jneurosci.2864-20.2021 · Cited by 45 · see citing works
Compositional variation in early‐life parenting structures alters oxytocin and vasopressin 1a receptor development in prairie voles (Microtus ochrogaster)
Rogers, F. D., Freeman, S. M., Anderson, M., Palumbo, M. C., & Bales, K. L. (2021) · Journal of Neuroendocrinology · doi:10.1111/jne.13001 · Cited by 44 · see citing works
Perinatal and juvenile social environments interact to shape cognitive behaviour and neural phenotype in prairie voles
Prounis, G. S., Foley, L., Rehman, A., & Ophir, A. G. (2015) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2015.2236 · Cited by 44 · see citing works
Biopossibility: A Queer Feminist Materialist Science Studies Manifesto, with Special Reference to the Question of Monogamous Behavior
Willey, A. (2016) · Signs · doi:10.1086/684238 · Cited by 44 · see citing works
Intergenerational transmission of sociality: the role of parents in shaping social behavior in monogamous and non-monogamous species
Perkeybile, A. M., & Bales, K. L. (2017) · Journal of Experimental Biology · doi:10.1242/jeb.142182 · Cited by 42 · see citing works
Paternal Care in Biparental Rodents: Intra- and Inter-individual Variation
Wendy Saltzman, A., Harris, B. N., A, T. R. D. J., Perea-Rodríguez, J. P., Horrell, N. D., Zhao, M., & Andrew, J. R. (2017) · Integrative and Comparative Biology · doi:10.1093/icb/icx047 · Cited by 44 · see citing works
Raised without a father: monoparental care effects over development, sexual behavior, sexual reward, and pair bonding in prairie voles
Valera-Marín, G., Young, L. J., Camacho, F., Paredes, R. G., Rodríguez, V. M., Díaz, N. F., & Portillo, W. (2021) · Behavioural Brain Research · doi:10.1016/j.bbr.2021.113264 · Cited by 42 · see citing works
Neuroanatomical distribution of oxytocin receptor binding in the female rabbit forebrain: Variations across the reproductive cycle
Jiménez, A., Young, L. J., Río, R. T.-D., LaPrairie, J. L., & González‐Mariscal, G. (2015) · Brain Research · doi:10.1016/j.brainres.2015.10.043 · Cited by 41 · see citing works
Long-term dysregulation of brain corticotrophin and glucocorticoid receptors and stress reactivity by single early-life pain experience in male and female rats
Victoria, N. C., Inoue, K., Young, L. J., & Murphy, A. Z. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.08.013 · Cited by 39 · see citing works
Neuropeptides as mediators of the early-life impact on the brain; implications for alcohol use disorders
Nylander, I., & Roman, E. (2012) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2012.00077 · Cited by 40 · see citing works
Developmental trajectories and influences of environmental complexity on oxytocin receptor and vasopressin 1A receptor expression in male and female prairie voles
Prounis, G. S., Thomas, K., & Ophir, A. G. (2018) · The Journal of Comparative Neurology · doi:10.1002/cne.24450 · Cited by 36 · see citing works
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Authors: Ahern, T. H.
Affiliations: Emory University (US)
Corresponding author: Ahern, Todd H
ORCID: Ahern, Todd H
Venue: Frontiers in Behavioral Neuroscience
Publisher: Frontiers Media SA
Published: 2009
Volume: 3
Pages: 17-17
ISSN: 1662-5153 (ISSN-L)
DOI: 10.3389/neuro.08.017.2009
PMC: PMC2742665
OpenAlex: W1991733912
Cited by: 239
References: 86
Citations by year: 2026: 9 · 2025: 6 · 2024: 7 · 2023: 18 · 2022: 30 · 2021: 14 · 2020: 21 · 2019: 13 · 2018: 13 · 2017: 15 · 2016: 13 · 2015: 22 · 2014: 10 · 2013: 13 · 2012: 11
FWCI: 15.17
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
Locations: Frontiers in Behavioral Neuroscience (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders: National Science Foundation (9876754)
National Institutes of Health (IBN-9876754, RR‐00165)
National Institute of Mental Health (K02MH064692, MH064692, MH77776, MH0732505, R01MH077776)
National Center for Research Resources (P51RR000165)
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 › Genetics › Human-Animal Interaction Studies
Keywords: Microtus ochrogaster, family structure, social attachment, parental care, oxytocin, vasopressin, corticotropin-releasing factor, mate preferences, social bonding, licking and grooming, neuropeptide receptors, dorsal raphe nucleus, monogamy, early life experience, social development (developmental psychology)

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The impact of early life family structure on adult social attachment, alloparental behavior, and the neuropeptide systems regulating affiliative behaviors in the monogamous prairie vole (Microtus ochrogaster)

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