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Table of Contents
Vol. 31, No. 4, 2009
Issue release date: June 2009
Free Access
Dev Neurosci 2009;31:332–341
(DOI:10.1159/000216544)

Consequences of Early Experiences and Exposure to Oxytocin and Vasopressin Are Sexually Dimorphic

Carter C.S.a · Boone E.M.a, c · Pournajafi-Nazarloo H.a · Bales K.L.b
aDepartment of Psychiatry, Brain Body Center, University of Illinois at Chicago, Chicago, Ill., bDepartment of Psychology, University of California, Davis, Calif., and cNational Institute on Drug Abuse, NIH, DHHS, Bethesda, Md., USA
email Corresponding Author

Abstract

In the socially monogamous prairie vole, we have observed that small changes in early handling, as well as early hormonal manipulations can have long-lasting and sexually dimorphic effects on behavior. These changes may be mediated in part by changes in parental interactions with their young, acting on systems that rely on oxytocin (OT) and arginine vasopressin (AVP). Knowledge of both endogenous and exogenous influences on systems that rely on OT and AVP may be helpful in understanding sexually dimorphic developmental disorders, such as autism, that are characterized by increased anxiety and deficits in social behavior.


 goto top of outline Key Words

  • Oxytocin
  • Vasopressin
  • Pitocin
  • Sex differences
  • Early experience
  • Prairie voles

 goto top of outline Abstract

In the socially monogamous prairie vole, we have observed that small changes in early handling, as well as early hormonal manipulations can have long-lasting and sexually dimorphic effects on behavior. These changes may be mediated in part by changes in parental interactions with their young, acting on systems that rely on oxytocin (OT) and arginine vasopressin (AVP). Knowledge of both endogenous and exogenous influences on systems that rely on OT and AVP may be helpful in understanding sexually dimorphic developmental disorders, such as autism, that are characterized by increased anxiety and deficits in social behavior.

Copyright © 2009 S. Karger AG, Basel


 goto top of outline References
  1. Bales KL, Carter CS (2003a): Sex differences and developmental effects of oxytocin on aggression and social behavior in prairie voles (Microtus ochrogaster). Horm Behav 44:178–184.
  2. Bales KL, Carter CS (2003b): Developmental exposure to oxytocin facilitates partner preferences in male prairie voles (Microtus ochrogaster). Behav Neurosci 117:854–859.
  3. Bales KL, Kim AJ, Lewis-Reese AD, Carter CS (2004): Both oxytocin and vasopressin may influence alloparental behavior in male prairie voles. Horm Behav 45:354–361.
  4. Bales KL, Kramer KM, Lewis-Reese AD, Carter CS (2006): Effects of stress on parental care are sexually dimorphic in prairie voles. Physiol Behav 87:424–429.
  5. Bales KL, Lewis-Reese AD, Pfeifer LA, Kramer KM, Carter CS (2007a): Early experience affects the traits of monogamy in a sexually dimorphic manner. Dev Psychobiol 49:335–342.
  6. Bales KL, Plotsky PM, Young LJ, Lim MM, Grotte ND, Ferrer E, Carter CS (2007b): Neonatal oxytocin manipulations have long-lasting, sexually dimorphic effects on vasopressin receptors. Neuroscience 144:38–45.
  7. Barberis C, Tribollet E (1996): Vasopressin and oxytocin receptors in the central nervous system. Crit Rev Neurobiol 10:119–154.
  8. Bester-Meredith JK, Marler CA (2003): Vasopressin and the transmission of paternal behavior across generations in mated, cross-fostered Peromyscus mice. Behav Neurosci 117:455–463.
  9. Bielsky IF, Hu SB, Young LJ (2005): Sexual dimorphism in the vasopressin system: lack of an altered behavioral phenotype in female V1a receptor knockout mice. Behav Brain Res 164:132–136.
  10. Caldwell HK, Wersinger SR, Young WS (2008): The role of vasopressin 1b receptor in aggression and other social behaviors. Prog Brain Res 170:65–72.
  11. Carter CS (1998): Neuroendocrine perspectives on social attachment and love. Psychoneuroendocrinology 23:779–818.
  12. Carter CS (2003): Developmental consequences of oxytocin. Physiol Behav 79:383–397.
  13. Carter CS (2007): Sex differences in oxytocin and vasopressin: implications for autism spectrum disorders? Behav Brain Res 176:170–186.
  14. Carter CS, Altemus M (2004): Oxytocin, vasopressin, and depression; in den Boer JA, George MS, ter Horst GJ (eds): Current and Future Developments in Psychopharmacology. Amsterdam, Benecke, pp 201–216.
  15. Carter, Boone EM, Bales KL (2008): Early experience and the developmental programming of oxytocin and vasopressin; in Bridges RS (ed): Neurobiology of the Parental Brain. San Diego, Elsevier, pp 417–433.
  16. Carter CS, DeVries AC, Getz LL (1995): Physiological substrates of mammalian monogamy: the prairie vole model. Neurosci Biobehav Rev 19:303–314.
  17. Champagne F, Diorio J, Sharma S, Meaney MJ (2001): Naturally occurring variations in maternal behavior in the rat are associated with differences in estrogen-inducible central oxytocin receptors. Proc Natl Acad Sci USA 98:12736–12741.
  18. Champagne FA, Meaney MJ (2006): Stress during gestation alters postpartum maternal care and the development of the offspring in a rodent model. Biol Psychiatr 59:1227–1235.
  19. Cho MM, DeVries AC, Williams JR, Carter CS (1999): The effects of oxytocin and vasopressin on partner preferences in male and female prairie voles (Microtus ochrogaster). Behav Neurosci 113:1071–1079.
  20. Choleris E, Devidze N, Kavaliers M, Pfaff D (2008): Steroidal/neuropeptide interactions in hypothalamus and amygdala related to social anxiety. Prog Brain Res 170:291–303.
  21. Crepel V, Aronov D, Jorquera I, Represa A, Ben-Ari Y, Cossart R (2007): A parturition-associated nonsynaptic coherent activity pattern in the developing hippocampus. Neuron 54:105–120.
  22. Cushing BS, Kramer KM (2005): Mechanisms underlying epigenetic effects of early social experience: the role of neuropeptides and steroids. Neurosci Biobehav Rev 29:1085–1105.

    External Resources

  23. Cushing BS, Okorie U, Young LJ (2003): The effects of neonatal castration on the subsequent behavioural response to centrally administered arginine vasopressin and the expression of V-1a receptors in adult male prairie voles. J Neuroendocrinol 15:1021–1026.
  24. De Vries, Simerly RB (2002): Anatomy, development, and function of sexually dimorphic neural circuits in the mammalian brain; in Pfaff DW (ed): Hormones, Brain, and Behavior. San Diego, Academic Press, vol 4, pp 137–192.
  25. Engelmann M, Landgraf R, Wotjak CT (2004): The hypothalamic-neurohypophysial system regulates the hypothalamic-pituitary adrenal axis under stress: an old concept revisited. Front Neuroendocrinol 25:132–149.
  26. Francis DD, Young LJ, Meaney MJ, Insel TR (2002): Naturally occurring differences in maternal care are associated with the expression of oxytocin and vasopressin (V1a) receptors: gender differences. J Neuroendocrinol 14:349–353.
  27. Getz LL, Carter CS (1996): Prairie vole partnerships. Am Scient 84:56–62.

    External Resources

  28. Gimpl G, Fahrenholz F (2001): The oxytocin receptor system: structure, function, and regulation. Physiol Rev 81:629–683.
  29. Glynn LM, Davis EP, Schetter CD, Chicz-Demet A, Hobel CJ, Sandman CJ (2007): Postnatal maternal cortisol levels predict temperament in healthy breastfed infants. Early Human Devel 83:675–681.
  30. Grosvenor CE, Picciano MT, Baumrucker CR (1993): Hormones and growth factors in milk. Endocr Rev 14:710–728.
  31. Hammock EA, Young LJ (2005): Microsatellite instability generates diversity in brain and sociobehavioral traits. Science 308:1630–1634.
  32. Husslein P (2002): Development and clinical experience with the new evidence-based tocolytic atosiban. Acta Obst Gynecol Scand 81:633–641.
  33. Insel TR, Shapiro LE (1992): Oxytocin receptor distribution reflects social organization in monogamous and polygamous voles. PNAS 89:5981–5985.
  34. Khazipov R, Tyzio R, Ben-Ari Y (2008): Effects of oxytocin on GABA signalling in the fetal brain during delivery. Prog Brain Res 170:243–254.
  35. Kimura T, Saji F, Nishimori K, Ogita K, Nakamura H, Koyama M, Murata Y (2003): Molecular regulation of the oxytocin receptor in peripheral organs. J Mol Endocrinol 30:109–115.
  36. Kramer KM, Yoshida S, Papademitriou E, Cushing BS (2007): The organizational effects of oxytocin on the central expression of estrogen receptor alpha and oxytocin in adulthood. BMC Neurosci 8:71.
  37. Landgraf R, Neumann ID (2004): Vasopressin and oxytocin release within the brain: a dynamic concept of multiple and variable modes of neuropeptide communication. Front Neuroendocrinol 25:150–176.
  38. Leake RD, Weitzman RE, Fisher DA (1981): Oxytocin concentrations during the neonatal period. Biol Neonate 39:127–131.
  39. Lim MM, Hammock EA, Young LJ (2004a): The role of vasopressin in the genetic and neural regulation of monogamy. J Neuroendocrinol 16:325–332.
  40. Lim MM, Hammock EAD, Young LJ (2004b): The role of vasopressin in the genetic and neural regulation of monogamy. J Neuroendocrinol 16:325–332.
  41. Ophir AG, Wolff JO, Phelps SM (2008): Variation in neural V1aR predicts sexual fidelity and space use among male prairie voles in semi-natural settings. Proc Natl Acad Sci USA 105:1249–1254.
  42. Phelps SM, Young LJ (2003): Extraordinary diversity in vasopressin (V1a) receptor distributions among wild prairie voles (Microtus ochrogaster): patterns of variation and covariation. J Comp Neurol 466:564–576.
  43. Porges SW (1998): Love: an emergent property of the mammalian autonomic nervous system. Psychoneuroendocrinology 23:837–861.
  44. Pournajafi-Nazarloo H, Carr MS, Papademetriou E, Schmidt JV, Cushing BS (2007a): Oxytocin increases ERalpha mRNA expression in the hypothalamus and hippocampus of neonatal female voles. Neuropeptides 41:39–44.
  45. Pournajafi-Nazarloo H, Perry A, Papademetriou E, Parloo L, Carter CS (2007b): Neonatal oxytoin treatment modulates oxytocin receptor, atrial natriuretic peptide, nitric oxide synthase, and estrogen receptor mRNA expression in rat heart. Peptides 28:1170–1177.
  46. Stribley JM, Carter CS (1999): Developmental exposure to vasopressin increases aggression in adult prairie voles. Proc Natl Acad Sci USA 96:12601–12604.
  47. Szyf M, Weaver ICG, Champagne FA, Diorio J, Meaney MJ (2005): Maternal programming of steroid receptor expression and phenotype through DNA methylation in the rat. Front Neuroendocrinol 26:139–162.
  48. Theodosis DT (2002): Oxytocin-secreting neurons: a physiological model of morphological neuronal and glial plasticity in the adult hypothalamus. Front Neuroendocrinol 23:101–135.
  49. Tyzio R, Cossart R, Khalilov I, Minlebaev M, Hubner CA, Represa A, Ben-Ari Y, Khazipov R (2006): Maternal oxytocin triggers a transient inhibitory switch in GABA signaling in the fetal brain during delivery. Science 314:1788–1792.
  50. Vivani D, Stoop R (2008): Opposite effects of oxytocin and vasopressin on the emotional expression of the fear response. Prog Brain Res 170:207–218.
  51. Wang ZX, Young LJ, De Vries GJ, Insel TR (1998): Voles and vasopressin: a review of molecular, cellular, and behavioral studies of pair bonding and paternal behaviors. Prog Brain Res 119:483–499.
  52. Weiser MJ, Foradori CD, Handa RJ (2008): Estrogen receptor beta in the brain: from form to function. Brain Res Rev 57:309–320.
  53. Williams JR, Insel TR, Harbaugh CR, Carter CS (1994): Oxytocin centrally administered facilitates formation of a partner preference in female prairie voles (Microtus ochrogaster). J Neuroendocrinol 6:247–250.
  54. Winslow JT, Hastings N, Carter CS, Harbaugh CR, Insel TR (1993): A role for central vasopressin in pair bonding in monogamous prairie voles. Nature 365:545–548.
  55. Witt DM, Carter CS, Insel TR (1991): Oxytocin receptor binding in female prairie voles: endogenous and exogenous estradiol stimulation. J Neuroendocrinol 3:155–161.
  56. Yamamoto Y, Carter CS, Cushing BS (2006): Neonatal manipulation of oxytocin affects expression of estrogen receptor alpha. Neuroscience 137:157–164.
  57. Yamamoto Y, Cushing BS, Kramer KM, Epperson PD, Hoffman GE, Carter CS (2004): Neonatal manipulations of oxytocin alter expression of oxytocin and vasopressin immunoreactive cells in the paraventricular nucleus of the hypothalamus in a gender specific manner. Neuroscience 125:947–955.
  58. Young LJ, Murphy Young AZ, Hammock EA (2005): Anatomy and neurochemistry of the pair bond. J Comp Neurol 493:51–57.

 goto top of outline Author Contacts

Sue Carter
Department of Psychiatry, Brain Body Center
University of Illinois at Chicago
Chicago, IL 60612 (USA)
Tel. +1 312 355 1593, Fax +1 312 996 7658, E-Mail scarter@psych.uic.edu


 goto top of outline Article Information

Received: December 16, 2008
Accepted: December 29, 2008
Published online: June 17, 2009
Number of Print Pages : 10
Number of Figures : 0, Number of Tables : 2, Number of References : 58


 goto top of outline Publication Details

Developmental Neuroscience

Vol. 31, No. 4, Year 2009 (Cover Date: June 2009)

Journal Editor: Levison S.W. (Newark, N.J.)
ISSN: 0378-5866 (Print), eISSN: 1421-9859 (Online)

For additional information: http://www.karger.com/DNE


Copyright / Drug Dosage / Disclaimer

Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher or, in the case of photocopying, direct payment of a specified fee to the Copyright Clearance Center.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in goverment regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.

Abstract

In the socially monogamous prairie vole, we have observed that small changes in early handling, as well as early hormonal manipulations can have long-lasting and sexually dimorphic effects on behavior. These changes may be mediated in part by changes in parental interactions with their young, acting on systems that rely on oxytocin (OT) and arginine vasopressin (AVP). Knowledge of both endogenous and exogenous influences on systems that rely on OT and AVP may be helpful in understanding sexually dimorphic developmental disorders, such as autism, that are characterized by increased anxiety and deficits in social behavior.



 goto top of outline Author Contacts

Sue Carter
Department of Psychiatry, Brain Body Center
University of Illinois at Chicago
Chicago, IL 60612 (USA)
Tel. +1 312 355 1593, Fax +1 312 996 7658, E-Mail scarter@psych.uic.edu


 goto top of outline Article Information

Received: December 16, 2008
Accepted: December 29, 2008
Published online: June 17, 2009
Number of Print Pages : 10
Number of Figures : 0, Number of Tables : 2, Number of References : 58


 goto top of outline Publication Details

Developmental Neuroscience

Vol. 31, No. 4, Year 2009 (Cover Date: June 2009)

Journal Editor: Levison S.W. (Newark, N.J.)
ISSN: 0378-5866 (Print), eISSN: 1421-9859 (Online)

For additional information: http://www.karger.com/DNE


Copyright / Drug Dosage

Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher or, in the case of photocopying, direct payment of a specified fee to the Copyright Clearance Center.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in goverment regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.

References

  1. Bales KL, Carter CS (2003a): Sex differences and developmental effects of oxytocin on aggression and social behavior in prairie voles (Microtus ochrogaster). Horm Behav 44:178–184.
  2. Bales KL, Carter CS (2003b): Developmental exposure to oxytocin facilitates partner preferences in male prairie voles (Microtus ochrogaster). Behav Neurosci 117:854–859.
  3. Bales KL, Kim AJ, Lewis-Reese AD, Carter CS (2004): Both oxytocin and vasopressin may influence alloparental behavior in male prairie voles. Horm Behav 45:354–361.
  4. Bales KL, Kramer KM, Lewis-Reese AD, Carter CS (2006): Effects of stress on parental care are sexually dimorphic in prairie voles. Physiol Behav 87:424–429.
  5. Bales KL, Lewis-Reese AD, Pfeifer LA, Kramer KM, Carter CS (2007a): Early experience affects the traits of monogamy in a sexually dimorphic manner. Dev Psychobiol 49:335–342.
  6. Bales KL, Plotsky PM, Young LJ, Lim MM, Grotte ND, Ferrer E, Carter CS (2007b): Neonatal oxytocin manipulations have long-lasting, sexually dimorphic effects on vasopressin receptors. Neuroscience 144:38–45.
  7. Barberis C, Tribollet E (1996): Vasopressin and oxytocin receptors in the central nervous system. Crit Rev Neurobiol 10:119–154.
  8. Bester-Meredith JK, Marler CA (2003): Vasopressin and the transmission of paternal behavior across generations in mated, cross-fostered Peromyscus mice. Behav Neurosci 117:455–463.
  9. Bielsky IF, Hu SB, Young LJ (2005): Sexual dimorphism in the vasopressin system: lack of an altered behavioral phenotype in female V1a receptor knockout mice. Behav Brain Res 164:132–136.
  10. Caldwell HK, Wersinger SR, Young WS (2008): The role of vasopressin 1b receptor in aggression and other social behaviors. Prog Brain Res 170:65–72.
  11. Carter CS (1998): Neuroendocrine perspectives on social attachment and love. Psychoneuroendocrinology 23:779–818.
  12. Carter CS (2003): Developmental consequences of oxytocin. Physiol Behav 79:383–397.
  13. Carter CS (2007): Sex differences in oxytocin and vasopressin: implications for autism spectrum disorders? Behav Brain Res 176:170–186.
  14. Carter CS, Altemus M (2004): Oxytocin, vasopressin, and depression; in den Boer JA, George MS, ter Horst GJ (eds): Current and Future Developments in Psychopharmacology. Amsterdam, Benecke, pp 201–216.
  15. Carter, Boone EM, Bales KL (2008): Early experience and the developmental programming of oxytocin and vasopressin; in Bridges RS (ed): Neurobiology of the Parental Brain. San Diego, Elsevier, pp 417–433.
  16. Carter CS, DeVries AC, Getz LL (1995): Physiological substrates of mammalian monogamy: the prairie vole model. Neurosci Biobehav Rev 19:303–314.
  17. Champagne F, Diorio J, Sharma S, Meaney MJ (2001): Naturally occurring variations in maternal behavior in the rat are associated with differences in estrogen-inducible central oxytocin receptors. Proc Natl Acad Sci USA 98:12736–12741.
  18. Champagne FA, Meaney MJ (2006): Stress during gestation alters postpartum maternal care and the development of the offspring in a rodent model. Biol Psychiatr 59:1227–1235.
  19. Cho MM, DeVries AC, Williams JR, Carter CS (1999): The effects of oxytocin and vasopressin on partner preferences in male and female prairie voles (Microtus ochrogaster). Behav Neurosci 113:1071–1079.
  20. Choleris E, Devidze N, Kavaliers M, Pfaff D (2008): Steroidal/neuropeptide interactions in hypothalamus and amygdala related to social anxiety. Prog Brain Res 170:291–303.
  21. Crepel V, Aronov D, Jorquera I, Represa A, Ben-Ari Y, Cossart R (2007): A parturition-associated nonsynaptic coherent activity pattern in the developing hippocampus. Neuron 54:105–120.
  22. Cushing BS, Kramer KM (2005): Mechanisms underlying epigenetic effects of early social experience: the role of neuropeptides and steroids. Neurosci Biobehav Rev 29:1085–1105.

    External Resources

  23. Cushing BS, Okorie U, Young LJ (2003): The effects of neonatal castration on the subsequent behavioural response to centrally administered arginine vasopressin and the expression of V-1a receptors in adult male prairie voles. J Neuroendocrinol 15:1021–1026.
  24. De Vries, Simerly RB (2002): Anatomy, development, and function of sexually dimorphic neural circuits in the mammalian brain; in Pfaff DW (ed): Hormones, Brain, and Behavior. San Diego, Academic Press, vol 4, pp 137–192.
  25. Engelmann M, Landgraf R, Wotjak CT (2004): The hypothalamic-neurohypophysial system regulates the hypothalamic-pituitary adrenal axis under stress: an old concept revisited. Front Neuroendocrinol 25:132–149.
  26. Francis DD, Young LJ, Meaney MJ, Insel TR (2002): Naturally occurring differences in maternal care are associated with the expression of oxytocin and vasopressin (V1a) receptors: gender differences. J Neuroendocrinol 14:349–353.
  27. Getz LL, Carter CS (1996): Prairie vole partnerships. Am Scient 84:56–62.

    External Resources

  28. Gimpl G, Fahrenholz F (2001): The oxytocin receptor system: structure, function, and regulation. Physiol Rev 81:629–683.
  29. Glynn LM, Davis EP, Schetter CD, Chicz-Demet A, Hobel CJ, Sandman CJ (2007): Postnatal maternal cortisol levels predict temperament in healthy breastfed infants. Early Human Devel 83:675–681.
  30. Grosvenor CE, Picciano MT, Baumrucker CR (1993): Hormones and growth factors in milk. Endocr Rev 14:710–728.
  31. Hammock EA, Young LJ (2005): Microsatellite instability generates diversity in brain and sociobehavioral traits. Science 308:1630–1634.
  32. Husslein P (2002): Development and clinical experience with the new evidence-based tocolytic atosiban. Acta Obst Gynecol Scand 81:633–641.
  33. Insel TR, Shapiro LE (1992): Oxytocin receptor distribution reflects social organization in monogamous and polygamous voles. PNAS 89:5981–5985.
  34. Khazipov R, Tyzio R, Ben-Ari Y (2008): Effects of oxytocin on GABA signalling in the fetal brain during delivery. Prog Brain Res 170:243–254.
  35. Kimura T, Saji F, Nishimori K, Ogita K, Nakamura H, Koyama M, Murata Y (2003): Molecular regulation of the oxytocin receptor in peripheral organs. J Mol Endocrinol 30:109–115.
  36. Kramer KM, Yoshida S, Papademitriou E, Cushing BS (2007): The organizational effects of oxytocin on the central expression of estrogen receptor alpha and oxytocin in adulthood. BMC Neurosci 8:71.
  37. Landgraf R, Neumann ID (2004): Vasopressin and oxytocin release within the brain: a dynamic concept of multiple and variable modes of neuropeptide communication. Front Neuroendocrinol 25:150–176.
  38. Leake RD, Weitzman RE, Fisher DA (1981): Oxytocin concentrations during the neonatal period. Biol Neonate 39:127–131.
  39. Lim MM, Hammock EA, Young LJ (2004a): The role of vasopressin in the genetic and neural regulation of monogamy. J Neuroendocrinol 16:325–332.
  40. Lim MM, Hammock EAD, Young LJ (2004b): The role of vasopressin in the genetic and neural regulation of monogamy. J Neuroendocrinol 16:325–332.
  41. Ophir AG, Wolff JO, Phelps SM (2008): Variation in neural V1aR predicts sexual fidelity and space use among male prairie voles in semi-natural settings. Proc Natl Acad Sci USA 105:1249–1254.
  42. Phelps SM, Young LJ (2003): Extraordinary diversity in vasopressin (V1a) receptor distributions among wild prairie voles (Microtus ochrogaster): patterns of variation and covariation. J Comp Neurol 466:564–576.
  43. Porges SW (1998): Love: an emergent property of the mammalian autonomic nervous system. Psychoneuroendocrinology 23:837–861.
  44. Pournajafi-Nazarloo H, Carr MS, Papademetriou E, Schmidt JV, Cushing BS (2007a): Oxytocin increases ERalpha mRNA expression in the hypothalamus and hippocampus of neonatal female voles. Neuropeptides 41:39–44.
  45. Pournajafi-Nazarloo H, Perry A, Papademetriou E, Parloo L, Carter CS (2007b): Neonatal oxytoin treatment modulates oxytocin receptor, atrial natriuretic peptide, nitric oxide synthase, and estrogen receptor mRNA expression in rat heart. Peptides 28:1170–1177.
  46. Stribley JM, Carter CS (1999): Developmental exposure to vasopressin increases aggression in adult prairie voles. Proc Natl Acad Sci USA 96:12601–12604.
  47. Szyf M, Weaver ICG, Champagne FA, Diorio J, Meaney MJ (2005): Maternal programming of steroid receptor expression and phenotype through DNA methylation in the rat. Front Neuroendocrinol 26:139–162.
  48. Theodosis DT (2002): Oxytocin-secreting neurons: a physiological model of morphological neuronal and glial plasticity in the adult hypothalamus. Front Neuroendocrinol 23:101–135.
  49. Tyzio R, Cossart R, Khalilov I, Minlebaev M, Hubner CA, Represa A, Ben-Ari Y, Khazipov R (2006): Maternal oxytocin triggers a transient inhibitory switch in GABA signaling in the fetal brain during delivery. Science 314:1788–1792.
  50. Vivani D, Stoop R (2008): Opposite effects of oxytocin and vasopressin on the emotional expression of the fear response. Prog Brain Res 170:207–218.
  51. Wang ZX, Young LJ, De Vries GJ, Insel TR (1998): Voles and vasopressin: a review of molecular, cellular, and behavioral studies of pair bonding and paternal behaviors. Prog Brain Res 119:483–499.
  52. Weiser MJ, Foradori CD, Handa RJ (2008): Estrogen receptor beta in the brain: from form to function. Brain Res Rev 57:309–320.
  53. Williams JR, Insel TR, Harbaugh CR, Carter CS (1994): Oxytocin centrally administered facilitates formation of a partner preference in female prairie voles (Microtus ochrogaster). J Neuroendocrinol 6:247–250.
  54. Winslow JT, Hastings N, Carter CS, Harbaugh CR, Insel TR (1993): A role for central vasopressin in pair bonding in monogamous prairie voles. Nature 365:545–548.
  55. Witt DM, Carter CS, Insel TR (1991): Oxytocin receptor binding in female prairie voles: endogenous and exogenous estradiol stimulation. J Neuroendocrinol 3:155–161.
  56. Yamamoto Y, Carter CS, Cushing BS (2006): Neonatal manipulation of oxytocin affects expression of estrogen receptor alpha. Neuroscience 137:157–164.
  57. Yamamoto Y, Cushing BS, Kramer KM, Epperson PD, Hoffman GE, Carter CS (2004): Neonatal manipulations of oxytocin alter expression of oxytocin and vasopressin immunoreactive cells in the paraventricular nucleus of the hypothalamus in a gender specific manner. Neuroscience 125:947–955.
  58. Young LJ, Murphy Young AZ, Hammock EA (2005): Anatomy and neurochemistry of the pair bond. J Comp Neurol 493:51–57.