Front Endocrinol (Lausanne). 2014 Mar 21;5:33. doi: 10.3389/fendo.2014.00033. eCollection 2014.
Early life trauma and attachment: immediate and enduring effects on neurobehavioral and stress axis development.
Frontiers in endocrinology
Millie Rincón-Cortés, Regina M Sullivan
Affiliations
Affiliations
- Department of Neuroscience and Physiology, Sackler Institute for Graduate Biomedical Sciences, New York University School of Medicine , New York, NY , USA ; Emotional Brain Institute, Nathan Kline Institute for Psychiatric Research , New York, NY , USA ; New York University Child Study Center, Department of Child and Adolescent Psychiatry, New York University School of Medicine , New York, NY , USA.
PMID: 24711804
PMCID: PMC3968754 DOI: 10.3389/fendo.2014.00033
Abstract
Over half a century of converging clinical and animal research indicates that early life experiences induce enduring neuroplasticity of the HPA-axis and the developing brain. This experience-induced neuroplasticity is due to alterations in the frequency and intensity of stimulation of pups' sensory systems (i.e., olfactory, somatosensory, gustatory) embedded in mother-infant interactions. This stimulation provides "hidden regulators" of pups' behavioral, physiological, and neural responses that have both immediate and enduring consequences, including those involving the stress response. While variation in stimulation can produce individual differences and adaptive behaviors, pathological early life experiences can induce maladaptive behaviors, initiate a pathway to pathology, and increase risk for later-life psychopathologies, such as mood and affective disorders, suggesting that infant-attachment relationships program later-life neurobehavioral function. Recent evidence suggests that the effects of maternal presence or absence during this sensory stimulation provide a major modulatory role in neural and endocrine system responses, which have minimal impact on pups' immediate neurobehavior but a robust impact on neurobehavioral development. This concept is reviewed here using two complementary rodent models of infant trauma within attachment: infant paired-odor-shock conditioning (mimicking maternal odor attachment learning) and rearing with an abusive mother that converge in producing a similar behavioral phenotype in later-life including depressive-like behavior as well as disrupted HPA-axis and amygdala function. The importance of maternal social presence on pups' immediate and enduring brain and behavior suggests unique processing of sensory stimuli in early life that could provide insight into the development of novel strategies for prevention and therapeutic interventions for trauma experienced with the abusive caregiver.
Keywords: amygdala; development; infant-attachment; maternal programming; rodent models; social behavior; stress
References
- Am J Physiol. 1978 Nov;235(5):E451-6 - PubMed
- J Clin Psychiatry. 2004;65 Suppl 1:18-28 - PubMed
- J Neurochem. 1988 Jun;50(6):1678-81 - PubMed
- Endocrinology. 1986 Apr;118(4):1445-51 - PubMed
- Dev Psychopathol. 2005 Fall;17(4):1071-89 - PubMed
- Ann N Y Acad Sci. 1997 Apr 24;814:252-65 - PubMed
- Endocr Rev. 2000 Feb;21(1):55-89 - PubMed
- Front Hum Neurosci. 2010 Jan 08;3:68 - PubMed
- Dev Psychobiol. 1975 Mar;8(2):151-64 - PubMed
- Dev Psychopathol. 2006 Summer;18(3):651-77 - PubMed
- Physiol Behav. 1999 Jun;66(4):627-37 - PubMed
- Life Sci. 1982 Jun 21;30(25):2207-14 - PubMed
- Front Neuroendocrinol. 2003 Jul;24(3):151-80 - PubMed
- Proc Natl Acad Sci U S A. 1998 Apr 28;95(9):5335-40 - PubMed
- Horm Behav. 2006 Nov;50(4):623-31 - PubMed
- J Neurobiol. 1999 Feb 5;38(2):259-69 - PubMed
- Biol Psychiatry. 2000 Oct 15;48(8):778-90 - PubMed
- Science. 1967 Apr 14;156(3772):258-60 - PubMed
- Dev Cogn Neurosci. 2011 Jan;1(1):77-87 - PubMed
- Int J Dev Neurosci. 2004 Aug-Oct;22(5-6):415-22 - PubMed
- J Am Acad Child Adolesc Psychiatry. 2009 Feb;48(2):114-27 - PubMed
- Physiol Behav. 2001 Jun;73(3):255-60 - PubMed
- Biol Psychiatry. 2000 Dec 15;48(12):1164-74 - PubMed
- Child Dev. 1994 Oct;65(5):1491-502 - PubMed
- Neurosci Biobehav Rev. 2003 Jan-Mar;27(1-2):73-82 - PubMed
- Brain Res. 1986 Jan;389(1-2):271-7 - PubMed
- J Neuroendocrinol. 2001 Sep;13(9):799-807 - PubMed
- Dev Psychobiol. 1998 Jul;33(1):5-20 - PubMed
- Ann N Y Acad Sci. 1999 Jun 29;877:756-9 - PubMed
- Dev Neurosci. 2012;34(2-3):101-14 - PubMed
- Brain Res Dev Brain Res. 1992 Dec 18;70(2):279-82 - PubMed
- Ann N Y Acad Sci. 2003 Dec;1008:22-30 - PubMed
- Dev Psychobiol. 1984 Jul;17(4):407-22 - PubMed
- J Neurosci. 1987 Sep;7(9):2837-43 - PubMed
- Dev Psychobiol. 1990 Jul;23(5):411-26 - PubMed
- J Neurochem. 1999 Mar;72(3):1088-94 - PubMed
- Neurosci Biobehav Rev. 1999 May;23(5):743-60 - PubMed
- Neurotox Res. 2002 Aug-Sep;4(5-6):557-564 - PubMed
- J Comp Neurol. 2002 Nov 11;453(2):116-30 - PubMed
- Nat Rev Neurosci. 2009 Jun;10(6):397-409 - PubMed
- Horm Behav. 2007 Sep;52(3):391-400 - PubMed
- Dev Neurosci. 2013;35(4):306-16 - PubMed
- JAMA. 2000 Aug 2;284(5):592-7 - PubMed
- Dev Psychobiol. 2010 Nov;52(7):638-50 - PubMed
- Behav Brain Res. 2013 Mar 1;240:46-51 - PubMed
- Psychol Bull. 2014 Jan;140(1):256-82 - PubMed
- Eur J Neurosci. 2004 Apr;19(7):1863-74 - PubMed
- Pediatr Neurol. 1996 Sep;15(2):114-9 - PubMed
- Public Health Rev. 1999;27(4):279-93 - PubMed
- Brain Res. 2008 Mar 20;1200:58-65 - PubMed
- Child Adolesc Psychiatr Clin N Am. 2003 Apr;12(2):271-92 - PubMed
- Life Sci. 1991;48(16):1537-46 - PubMed
- Cell Mol Neurobiol. 1996 Jun;16(3):345-56 - PubMed
- Neuron. 2012 Sep 6;75(5):747-61 - PubMed
- Nat Rev Neurosci. 2001 Feb;2(2):129-36 - PubMed
- Psychoneuroendocrinology. 2000 Nov;25(8):819-36 - PubMed
- Science. 1984 Dec 14;226(4680):1342-4 - PubMed
- Brain Res. 2000 Dec 15;886(1-2):172-189 - PubMed
- Prog Brain Res. 1990;85:367-402; discussion 402-3 - PubMed
- Child Dev. 1996 Apr;67(2):508-22 - PubMed
- J Comp Neurol. 1987 Sep 1;263(1):113-25 - PubMed
- Neuroscience. 1995 Feb;64(3):619-28 - PubMed
- Dev Med Child Neurol. 1980 Dec;22(6):800-15 - PubMed
- Proc Natl Acad Sci U S A. 1996 Feb 20;93(4):1619-23 - PubMed
- Biol Psychiatry. 2007 Nov 15;62(10):1070-9 - PubMed
- Brain Res Dev Brain Res. 1995 Apr 18;85(2):187-91 - PubMed
- Dev Psychopathol. 2001 Summer;13(3):473-89 - PubMed
- J Pers Soc Psychol. 2008 Jul;95(1):197-211 - PubMed
- J Child Psychol Psychiatry. 2000 Jan;41(1):97-116 - PubMed
- Dev Psychobiol. 1980 Jan;13(1):77-84 - PubMed
- J Public Health Policy. 1988 Summer;9(2):167-76 - PubMed
- Dev Psychobiol. 1986 Nov;19(6):615-23 - PubMed
- Eur Arch Psychiatry Clin Neurosci. 2006 Apr;256(3):174-86 - PubMed
- Ann N Y Acad Sci. 2003 Dec;1008:122-31 - PubMed
- Psychosom Med. 1995 Jan-Feb;57(1):23-31 - PubMed
- Endocr Rev. 1984 Winter;5(1):25-44 - PubMed
- Endocrinology. 1991 Sep;129(3):1505-12 - PubMed
- J Neurochem. 1989 May;52(5):1655-8 - PubMed
- Physiol Behav. 1984 Nov;33(5):693-8 - PubMed
- J Neurosci. 2006 Jun 21;26(25):6737-48 - PubMed
- J Neuroendocrinol. 1996 Jan;8(1):1-8 - PubMed
- Biol Psychiatry. 2004 Jul 15;56(2):72-9 - PubMed
- Brain Res. 2000 Mar 24;859(2):249-54 - PubMed
- J Am Acad Child Adolesc Psychiatry. 2000 Jun;39(6):703-12 - PubMed
- Brain Res. 1985 Mar 11;329(1-2):294-9 - PubMed
- J Child Psychol Psychiatry. 2007 Mar-Apr;48(3-4):224-44 - PubMed
- Dev Psychobiol. 1991 Dec;24(8):547-58 - PubMed
- J Neurosci. 1999 May 15;19(10):3982-91 - PubMed
- Neuropsychopharmacology. 1989 Sep;2(3):175-89 - PubMed
- Neuroscience. 2003;117(3):707-13 - PubMed
- Endocrinology. 1980 Mar;106(3):991-4 - PubMed
- Dev Psychobiol. 2010 Jul;52(5):453-64 - PubMed
- Behav Brain Res. 2001 Nov 29;126(1-2):147-57 - PubMed
- Behav Neural Biol. 1980 May;29(1):132-6 - PubMed
- Psychol Bull. 1998 May;123(3):211-23 - PubMed
- Curr Psychiatry Rep. 2013 Apr;15(4):352 - PubMed
- Ann N Y Acad Sci. 1997 Jun 21;821:194-207 - PubMed
- Int J Psychoanal. 1958 Sep-Oct;39(5):350-73 - PubMed
- Dialogues Clin Neurosci. 2005;7(2):103-23 - PubMed
- Dev Psychobiol. 1987 Mar;20(2):131-45 - PubMed
- Dev Psychobiol. 1985 May;18(3):215-27 - PubMed
- Front Neuroendocrinol. 2009 Oct;30(4):470-482 - PubMed
- J Neuroendocrinol. 2000 Aug;12(8):709-10 - PubMed
- Psychopharmacology (Berl). 2011 Mar;214(1):55-70 - PubMed
- Physiol Behav. 1975 Mar;14(3):311-9 - PubMed
- Adolescence. 1997 Summer;32(126):381-94 - PubMed
- Ann N Y Acad Sci. 1994 Nov 30;746:275-88; discussion 289-93 - PubMed
- Prog Brain Res. 2000;122:81-103 - PubMed
- Brain Res Dev Brain Res. 1990 May 1;53(2):243-7 - PubMed
- Psychoneuroendocrinology. 2005 Nov;30(10):939-46 - PubMed
- Front Behav Neurosci. 2009 Sep 01;3:22 - PubMed
- NIDA Res Monogr. 1995;158:172-201 - PubMed
- Brain Res Dev Brain Res. 1994 Aug 12;81(1):121-7 - PubMed
- Ment Retard Dev Disabil Res Rev. 2003;9(3):149-54 - PubMed
- Proc Natl Acad Sci U S A. 2013 Nov 5;110(45):18274-8 - PubMed
- Dev Psychobiol. 2008 Sep;50(6):554-65 - PubMed
- J Neurophysiol. 1987 Sep;58(3):510-24 - PubMed
- Behav Neurosci. 2006 Oct;120(5):1017-24 - PubMed
- Psychol Sci. 2006 Jun;17(6):550-6 - PubMed
- J Neurosci. 2009 Dec 16;29(50):15745-55 - PubMed
- Int J Dev Neurosci. 1998 Jun-Jul;16(3-4):149-64 - PubMed
- Child Maltreat. 2005 May;10(2):150-72 - PubMed
- J Neurosci. 2012 May 30;32(22):7758-65 - PubMed
- Dev Psychobiol. 2010 Nov;52(7):651-60 - PubMed
- Physiol Behav. 1988;42(3):265-70 - PubMed
- Science. 1979 Aug 31;205(4409):927-9 - PubMed
- Mol Cell Biol. 2006 Oct;26(19):7236-45 - PubMed
- Dev Psychobiol. 2009 Jan;51(1):95-105 - PubMed
- Child Psychiatry Hum Dev. 1999 Spring;29(3):189-208 - PubMed
- Nat Neurosci. 2006 Aug;9(8):1004-6 - PubMed
- Psychobiology (Austin, Tex). 1991;19(4):308-312 - PubMed
- Endocrinology. 1991 Mar;128(3):1385-95 - PubMed
- Am Psychol. 1979 Oct;34(10):932-7 - PubMed
- Endocrinology. 1973 Jun;92(6):1775-9 - PubMed
- Clin Perinatol. 2011 Dec;38(4):643-55 - PubMed
- Neuroendocrinology. 2000 Jun;71(6):333-42 - PubMed
- Psychoneuroendocrinology. 2014 Jan;39:39-57 - PubMed
- Science. 1980 Jun 6;208(4448):1174-6 - PubMed
- Biol Psychiatry. 2010 Jun 15;67(12):1137-45 - PubMed
- Front Behav Neurosci. 2009 Sep 01;3:16 - PubMed
- Neuroscience. 2008 Jun 26;154(3):1132-42 - PubMed
- Dev Med Child Neurol. 2011 Sep;53 Suppl 4:14-8 - PubMed
- Trends Neurosci. 1998 Jul;21(7):306-11 - PubMed
- Ann N Y Acad Sci. 2008 Dec;1148:64-73 - PubMed
- Behav Neurosci. 1993 Apr;107(2):254-63 - PubMed
- Ann N Y Acad Sci. 1999;896:30-47 - PubMed
- J Neurosci. 2003 Jun 15;23(12):5329-36 - PubMed
- Brain Behav Immun. 2005 Jul;19(4):296-308 - PubMed
- Learn Mem. 2004 Jul-Aug;11(4):406-11 - PubMed
- Trauma Violence Abuse. 2009 Oct;10(4):389-410 - PubMed
- Endocrinology. 2008 Oct;149(10):4892-900 - PubMed
- Dev Psychopathol. 2001 Summer;13(3):539-64 - PubMed
- Dev Psychobiol. 1996 Apr;29(3):191-204 - PubMed
- Brain Res Dev Brain Res. 2001 Mar 29;127(1):23-30 - PubMed
- Dev Psychopathol. 1994 Winter;6(1):57-75 - PubMed
- Nature. 1977 Apr 21;266(5604):730-2 - PubMed
- J Comp Physiol Psychol. 1980 Aug;94(4):588-95 - PubMed
- Endocrinology. 1996 Apr;137(4):1212-8 - PubMed
- J Neurosci. 1998 Dec 1;18(23):10171-9 - PubMed
- Learn Mem. 2008 Aug 26;15(9):649-56 - PubMed
- Dev Psychobiol. 2010 Nov;52(7):661-70 - PubMed
- Am J Psychiatry. 2002 Dec;159(12):2072-80 - PubMed
- Dev Psychobiol. 1988 Jan;21(1):25-42 - PubMed
- Psychoneuroendocrinology. 1998 Oct;23(7):663-700 - PubMed
- Endocrinology. 2000 May;141(5):1590-2 - PubMed
- Adv Exp Med Biol. 1990;265:269-76 - PubMed
- Biol Psychiatry. 2003 Dec 15;54(12):1389-98 - PubMed
- J Neurosci. 2004 Feb 4;24(5):1182-9 - PubMed
- Nat Rev Neurosci. 2008 Dec;9(12):947-57 - PubMed
- Dev Psychobiol. 2010 Jul;52(5):402-10 - PubMed
- Nat Rev Neurosci. 2009 Jun;10(6):434-45 - PubMed
- J Neurophysiol. 1988 Jun;59(6):1770-82 - PubMed
- Nat Neurosci. 2009 Nov;12(11):1367-9 - PubMed
- Ann N Y Acad Sci. 1995 Dec 29;771:339-51 - PubMed
- Brain Res. 2002 Sep 20;950(1-2):52-63 - PubMed
- Behav Neurosci. 1997 Dec;111(6):1257-64 - PubMed
- Science. 1979 Jul 27;205(4404):419-21 - PubMed
- Prog Neurobiol. 1997 Nov;53(4):399-430 - PubMed
- Brain Res Bull. 1994;35(5-6):467-72 - PubMed
- Neuroendocrinology. 1993 Jun;57(6):1003-10 - PubMed
- Trends Neurosci. 2008 Apr;31(4):183-91 - PubMed
- Birth Defects Res A Clin Mol Teratol. 2011 Aug;91(8):797-805 - PubMed
- J Neurosci. 1987 Oct;7(10):3154-62 - PubMed
- Psychoneuroendocrinology. 2002 Jan-Feb;27(1-2):199-220 - PubMed
- Dev Psychobiol. 1980 Sep;13(5):513-8 - PubMed
- Science. 1997 Sep 12;277(5332):1659-62 - PubMed
- Brain Res. 1986 Jun;392(1-2):278-82 - PubMed
- Nat Rev Neurosci. 2005 Jul;6(7):507-20 - PubMed
- Brain Res Dev Brain Res. 1997 Sep 20;102(2):291-3 - PubMed
- Prog Brain Res. 1988;73:101-20 - PubMed
- Ann N Y Acad Sci. 2003 Apr;985:125-34 - PubMed
- Proc Natl Acad Sci U S A. 2013 Sep 24;110(39):15638-43 - PubMed
- Neuron. 1999 Jun;23(2):229-32 - PubMed
- Prog Brain Res. 1991;88:173-85 - PubMed
- Neurosci Biobehav Rev. 2009 Apr;33(4):573-85 - PubMed
- J Neuroendocrinol. 1998 Sep;10(9):663-9 - PubMed
- Dev Psychobiol. 1980 Mar;13(2):141-50 - PubMed
- J Neurosci. 2006 Mar 1;26(9):2434-42 - PubMed
- J Neuroendocrinol. 2006 Jun;18(6):393-411 - PubMed
- Ann Med. 2010 May 6;42(4):252-64 - PubMed
- Dev Psychobiol. 1982 Sep;15(5):479-90 - PubMed
- Endocrinology. 1995 Oct;136(10):4517-25 - PubMed
- Psychoneuroendocrinology. 2002 Jan-Feb;27(1-2):99-114 - PubMed
- Neurosci Biobehav Rev. 1992 Winter;16(4):553-68 - PubMed
- Prog Neurobiol. 1990;34(6):505-26 - PubMed
- Dev Psychopathol. 1998 Fall;10(4):793-809 - PubMed
- Dev Psychobiol. 1984 Mar;17(2):161-81 - PubMed
- Arch Gen Psychiatry. 1991 Aug;48(8):693-9 - PubMed
- J Neurophysiol. 2002 Jun;87(6):3156-9 - PubMed
- Nat Neurosci. 2009 Nov;12(11):1355-6 - PubMed
- Dev Psychopathol. 2001 Summer;13(3):419-49 - PubMed
- J Neurosci. 1993 Sep;13(9):3839-47 - PubMed
- Biol Psychiatry. 2010 Aug 15;68(4):314-9 - PubMed
- Learn Mem. 2012 Oct 15;19(11):499-502 - PubMed
- Cell. 2011 Oct 28;147(3):509-24 - PubMed
- Cell Mol Neurobiol. 1993 Aug;13(4):295-319 - PubMed
- J Neurosci. 1991 May;11(5):1478-84 - PubMed
- Behav Neural Biol. 1981 Aug;32(4):391-405 - PubMed
- Dev Sci. 2010 Jan 1;13(1):46-61 - PubMed
- Neurosci Biobehav Rev. 2003 Jan-Mar;27(1-2):33-44 - PubMed
- Psychopharmacology (Berl). 2011 Mar;214(1):107-20 - PubMed
- Behav Neurosci. 1991 Apr;105(2):307-12 - PubMed
- Nature. 1976 Sep 16;263(5574):242-4 - PubMed
- J Comp Neurol. 1991 Feb 15;304(3):467-77 - PubMed
- Biol Psychiatry. 2002 Dec 1;52(11):1037-46 - PubMed
- Dev Psychopathol. 1998 Fall;10(4):589-605 - PubMed
- Biol Psychiatry. 2005 Apr 15;57(8):823-31 - PubMed
- Brain Res Mol Brain Res. 1993 May;18(3):195-200 - PubMed
- Ciba Found Symp. 1991;156:171-83; discussion 183-8 - PubMed
- Physiol Behav. 2003 Aug;79(3):399-407 - PubMed
- Behav Brain Res. 2000 Jun 1;110(1-2):25-37 - PubMed
- Neuropsychopharmacology. 2004 Apr;29(4):641-8 - PubMed
- Ann N Y Acad Sci. 2003 Dec;1008:238-47 - PubMed
- J Child Psychol Psychiatry. 1998 May;39(4):465-76 - PubMed
- Brain Res. 1994 Apr 18;643(1-2):306-9 - PubMed
- Dev Psychobiol. 1990 Jul;23(5):395-410 - PubMed
- Prog Brain Res. 1970;32:79-85 - PubMed
- Biol Psychiatry. 2001 Jun 15;49(12):1023-39 - PubMed
- Biol Psychiatry. 1999 Dec 1;46(11):1509-22 - PubMed
- J Exp Psychol Anim Behav Process. 1982 Oct;8(4):329-41 - PubMed
- Science. 1981 Jan 30;211(4481):506-8 - PubMed
- Behav Neurosci. 1988 Oct;102(5):692-700 - PubMed
- Prog Neuropsychopharmacol Biol Psychiatry. 2005 Dec;29(8):1201-13 - PubMed
- Psychoneuroendocrinology. 2010 Jun;35(5):743-51 - PubMed
- J Neurosci. 2003 Jun 1;23(11):4760-5 - PubMed
- Neurosci Biobehav Rev. 2010 May;34(6):867-76 - PubMed
- Metabolism. 2008 Oct;57 Suppl 2:S11-5 - PubMed
- Prog Neuropsychopharmacol Biol Psychiatry. 1986;10(1):57-65 - PubMed
- Behav Neurosci. 1993 Oct;107(5):860-6 - PubMed
- Annu Rev Psychol. 2007;58:145-73 - PubMed
- Curr Protoc Neurosci. 2001 May;Chapter 8:Unit 8.10A - PubMed
- Ann N Y Acad Sci. 1995 Dec 29;771:730-42 - PubMed
- Neurosci Biobehav Rev. 2005;29(4-5):649-74 - PubMed
- J Endocrinol. 1999 Jan;160(1):1-12 - PubMed
- Pharmacol Biochem Behav. 1994 Dec;49(4):911-20 - PubMed
- Child Abuse Negl. 1987;11(3):319-30 - PubMed
- Endocrinology. 1986 Oct;119(4):1816-21 - PubMed
- J Neurosci. 1989 Nov;9(11):3998-4006 - PubMed
- J Neurobiol. 1992 Dec;23(10):1557-73 - PubMed
- Monogr Soc Res Child Dev. 1994;59(2-3):192-207 - PubMed
- Ann N Y Acad Sci. 2003 Apr;985:106-13 - PubMed
- Dev Psychobiol. 2010 Nov;52(7):671-90 - PubMed
- J Neurosci. 2010 Sep 29;30(39):13005-15 - PubMed
- Nat Rev Endocrinol. 2009 Jul;5(7):374-81 - PubMed
- Child Dev. 1996 Jun;67(3):877-89 - PubMed
- Psychiatr Clin North Am. 2002 Jun;25(2):397-426, vii-viii - PubMed
- Acta Endocrinol (Copenh). 1977 Jan;84(1):167-76 - PubMed
- N Engl J Med. 1998 Jan 15;338(3):171-9 - PubMed
- J Neuroendocrinol. 2000 Jan;12(1):5-12 - PubMed
- Psychoneuroendocrinology. 2008 Jul;33(6):693-710 - PubMed
- Dev Psychobiol. 2012 Sep;54(6):598-611 - PubMed
- Neurosci Biobehav Rev. 2010 May;34(6):835-44 - PubMed
- Aust N Z J Psychiatry. 2002 Feb;36(1):9-30 - PubMed
- Ann N Y Acad Sci. 2003 Dec;1008:304-7 - PubMed
- Dev Psychopathol. 2011 Nov;23(4):1001-16 - PubMed
- Brain Res Dev Brain Res. 1993 Oct 15;75(2):185-92 - PubMed
- Stress. 2004 Mar;7(1):15-27 - PubMed
- Behav Neurosci. 2002 Feb;116(1):4-12 - PubMed
- Am J Physiol. 1990 Nov;259(5 Pt 1):E601-13 - PubMed
- Behav Neurosci. 2000 Oct;114(5):957-62 - PubMed
- Endocrinology. 1984 Oct;115(4):1364-70 - PubMed
- Synapse. 1996 May;23(1):39-51 - PubMed
- Endocrinology. 1994 Dec;135(6):2364-8 - PubMed
- Biol Psychiatry. 2002 Sep 15;52(6):529-42 - PubMed
- Dev Psychopathol. 2000 Autumn;12(4):695-712 - PubMed
- Child Abuse Negl. 2002 Jun;26(6-7):715-29 - PubMed
- Bull N Y Acad Med. 1985 Nov;61(9):771-91 - PubMed
- Biol Psychiatry. 1994 Feb 15;35(4):221-7 - PubMed
- Brain Res. 1985 Feb;350(1-2):165-8 - PubMed
- Nature. 2000 Sep 7;407(6800):38-9 - PubMed
- Biol Psychol. 2006 Jul;73(1):72-89 - PubMed
- Endocrinology. 2001 Jan;142(1):89-97 - PubMed
- Child Dev. 1969 Dec;40(4):969-1025 - PubMed
- Neuroendocrinology. 1980 Aug;31(2):101-5 - PubMed
- Learn Mem. 1999 Nov-Dec;6(6):608-18 - PubMed
- Behav Neurosci. 2004 Apr;118(2):274-81 - PubMed
- Psychol Bull. 1998 May;123(3):234-7 - PubMed
- Proc Natl Acad Sci U S A. 2012 Oct 16;109 Suppl 2:17208-12 - PubMed
- Dev Psychobiol. 2005 Nov;47(3):230-42 - PubMed
- Acta Paediatr Suppl. 1994 Jun;397:57-63 - PubMed
- Synapse. 1996 May;23(1):28-38 - PubMed
- Trends Neurosci. 1997 Feb;20(2):78-84 - PubMed
- Brain Res. 1995 Nov 20;699(2):192-200 - PubMed
- Semin Clin Neuropsychiatry. 2002 Apr;7(2):147-59 - PubMed
- Annu Rev Clin Psychol. 2005;1:409-38 - PubMed
- Arch Gen Psychiatry. 1998 May;55(5):473-7 - PubMed
- J Am Acad Child Adolesc Psychiatry. 1995 May;34(5):541-65 - PubMed
- Curr Opin Neurobiol. 1999 Feb;9(1):128-34 - PubMed
- Brain Res. 1986 Mar;396(1):64-76 - PubMed
- Philos Trans R Soc Lond B Biol Sci. 2006 Dec 29;361(1476):2215-28 - PubMed
- Neurosci Lett. 1995 Jun 2;192(1):49-52 - PubMed
- Chem Senses. 2005 Jan;30 Suppl 1:i152-3 - PubMed
- Neuroscience. 1990;35(1):133-8 - PubMed
- Endocrinology. 1975 Apr;96(4):1044-7 - PubMed
- Science. 1962 Mar 9;135(3506):795-6 - PubMed
- Trends Endocrinol Metab. 2002 Nov;13(9):373-80 - PubMed
- Integr Physiol Behav Sci. 2001 Oct;36(4):293-307 - PubMed
- Learn Mem. 2009 Oct 26;16(11):676-81 - PubMed
Publication Types
Grant support