Neuropeptides and the social brain: Potential rodent models of autism

International Journal of Developmental Neuroscience

Volumn 23, Issue 2-3 SPEC. ISS., 2005, Pages 235-243

  Lim, Miranda M ^a,b   Bielsky, Isadora F ^a   Young, Larry J ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b EMORY UNIVERSITY   (United States)

Author keywords

Knockout mice; Neuropeptides; Oxytocin; Oxytocin receptor; Pair bond; Social memory; Vasopressin; Vasopressin V1a receptor; Vole

Indexed keywords

NEUROPEPTIDE; OXYTOCIN; VASOPRESSIN; VASOPRESSIN V1 RECEPTOR;

AUTISM; BRAIN REGION; NONHUMAN; PRIORITY JOURNAL; RECOGNITION; REVIEW; SEXUAL BEHAVIOR; SIGNAL PROCESSING; SOCIAL BEHAVIOR;

EID: 14644392908     PISSN: 07365748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijdevneu.2004.05.006     Document Type: Article

References (91)

1. Abell F., Krams M., Ashburner J., Passingham R., Friston K., Frackowiak R., Happe F., Frith C., Frith U. The neuroanatomy of autism: a voxel-based whole brain analysis of structural scans. Neuroreport. 10:1999;1647-1651
2. Aharon I., Etcoff N., Ariely D., Chabris C.F., O'Connor E., Breiter H.C. Beautiful faces have variable reward value: fMRI and behavioral evidence. Neuron. 32:2001;537-551
3. Aragona B.J., Liu Y., Curtis J.T., Stephan F.K., Wang Z. A critical role for nucleus accumbens dopamine in partner-preference formation in male prairie voles. J. Neurosci. 23:2003;3483-3490
4. Aylward E.H., Minshew N.J., Goldstein G., Honeycutt N.A., Augustine A.M., Yates K.O., Barta P.E., Pearlson G.D. MRI volumes of amygdala and hippocampus in non-mentally retarded autistic adolescents and adults. Neurology. 53:1999;2145-2150
5. Baird G., Cass H., Slonims V. Diagnosis of autism. BMJ. 327:2003;488-493
6. Bales K.L., Carter C.S. Sex differences and developmental effects of oxytocin on aggression and social behavior in prairie voles (Microtus ochrogaster). Horm. Behav. 44:2003a;178-184
7. Bales K.L., Carter C.S. Developmental exposure to oxytocin facilitates partner preferences in male prairie voles (Microtus ochrogaster). Behav. Neurosci. 117:2003b;854-859
8. Bales K.L., Pfeifer L.A., Carter C.S. Sex differences and developmental effects of manipulations of oxytocin on alloparenting and anxiety in prairie voles. Dev. Psychobiol. 44:2004;123-131
9. Bartels A., Zeki S. The neural basis of romantic love. Neuroreport. 11:2000;3829-3834
10. Barton J.J. Disorders of face perception and recognition. Neurol. Clin. 21:2003;521-548
11. Benelli A., Bertolini A., Poggioli R., Menozzi B., Basaglia R., Arletti R. Polymodal dose-response curve for oxytocin in the social recognition test. Neuropeptides. 28:1995;251-255
12. Bielsky I.F., Hu S.B., Szegda K.L., Westphal H., Young L.J. Profound impairment in social recognition and reduction in anxiety-like behavior in vasopressin V1a receptor knockout mice. Neuropsychopharmacology. 29:2004;483-493
13. Blaicher W., Gruber D., Bieglmayer C., Blaicher A.M., Knogler W., Huber J.C. The role of oxytocin in relation to female sexual arousal. Gynecol. Obstet. Invest. 47:1999;125-126
14. Boucher J., Lewis V. Unfamiliar face recognition in relatively able autistic children. J. Child Psychol. Psychiatry. 33:1992;843-859
15. Boucher J., Lewis V., Collis G. Familiar face and voice matching and recognition in children with autism. J. Child Psychol. Psychiatry. 39:1998;171-181
16. Breiter H.C., Gollub R.L., Weisskoff R.M., Kennedy D.N., Makris N., Berke J.D., Goodman J.M., Kantor H.L., Gastfriend D.R., Riorden J.P., Mathew R.T., Rosen B.R., Hyman S.E. Acute effects of cocaine on human brain activity and emotion. Neuron. 19:1997;591-611
17. Carmichael M.S., Humbert R., Dixen J., Palmisano G., Greenleaf W., Davidson J.M. Plasma oxytocin increases in the human sexual response. J. Clin. Endocrinol. Metab. 64:1987;27-31
18. Carter C.S. Developmental consequences of oxytocin. Physiol. Behav. 79:2003;383-397
19. Carter C.S., DeVries A.C., Getz L.L. Physiological substrates of mammalian monogamy: the prairie vole model. Neurosci. Biobehav. Rev. 19:1995;303-314
20. Choleris E., Gustafsson J.-A., Korach K.S., Muglia L.J., Pfaff D.W., Ogawa S. An estrogen-dependent four-gene micronet regulating social recognition: a study with oxytocin and estrogen receptor-α and -β knockout mice. Proc. Natl. Acad. Sci. U.S.A. 100:2003;6192-6197
21. Critchley H.D., Daly E.M., Bullmore E.T., Williams S.C., Van Amelsvoort T., Robertson D.M., Rowe A., Phillips M., McAlonan G., Howlin P., Murphy D.G. The functional neuroanatomy of social behaviour: changes in cerebral blood flow when people with autistic disorder process facial expressions. Brain. 123(Pt 11):2000;2203-2212
22. Dantzer R., Bluthe R.M., Koob G.F., Le Moal M. Modulation of social memory in male rats by neurohypophyseal peptides. Psychopharmacology (Berl). 91:1987;363-368
23. Davies S., Bishop D., Manstead A.S., Tantam D. Face perception in children with autism and Asperger's syndrome. J. Child Psychol. Psychiatry. 35:1994;1033-1057
24. De Vries G.J., Buijs R.M. The origin of the vasopressinergic and oxytocinergic innervation of the rat brain with special reference to the lateral septum. Brain Res. 273:1983;307-317
25. Engelmann M., Landgraf R. Microdialysis administration of vasopressin into the septum improves social recognition in Brattleboro rats. Physiol. Behav. 55:1994;145-149
26. Engelmann M., Ebner K., Wotjak C.T., Landgraf R. Endogenous oxytocin is involved in short-term olfactory memory in female rats. Behav. Brain Res. 90:1998;89-94
27. Everts H.G.J., Koolhaas J.M. Differential modulation of lateral septal vasopressin receptor blockade in spatial-learning, social recognition, and anxiety-related behaviors in rats. Behav. Brain Res. 99:1999;7-16
28. Fehm-Wolfsdorf G., Born J. Behavioral effects of neurohypophyseal peptides in healthy volunteers: 10 years of research. Peptides. 12:1991;1399-1406
29. Ferguson J.N., Aldag J.M., Insel T.R., Young L.J. Oxytocin in the medial amygdala is essential for social recognition in the mouse. J. Neurosci. 21:2001;8278-8285
30. Ferguson J.N., Young L.J., Hearn E.F., Matzuk M.M., Insel T.R., Winslow J.T. Social amnesia in mice lacking the oxytocin gene. Nat. Genet. 25:2000;284-288
31. Ferris, C.F., Harder, J.A., Messenger, T.L., Insel, T.R., 2003. Is motherhood more rewarding than cocaine? A fMRI study on conscious lactating rats. In: Society for Neuroscience, New Orleans, LA (Abstract Viewer/Itinerary Planner).
32. Fields R.L., House S.B., Gainer H. Regulatory domains in the intergenic region of the oxytocin and vasopressin genes that control their hypothalamus-specific expression in vitro. J. Neurosci. 23:2003;7801-7809
33. Gabreels B.A., Swaab D.F., de Kleijn D.P., Dean A., Seidah N.G., Van de Loo J.W., Van de Ven W.J., Martens G.J., Van Leeuwen F.W. The vasopressin precursor is not processed in the hypothalamus of Wolfram syndrome patients with diabetes insipidus: evidence for the involvement of PC2 and 7B2. J. Clin. Endocrinol. Metab. 83:1998;4026-4033
34. Gainer, H., Wray, W., 1994. Cellular and molecular biology of oxytocin and vasopressin. In: Knobil E., Neill J.D. (Eds.), The Physiology of Reproduction. Raven Press, New York, USA, pp. 1099-1129.
35. Getz L.L., McGuire B., Pizzuto T., Hofmann J.E., Frase B. Social organization of the prairie vole (Microtus ochragaster). J. Mammol. 74:1993;44-58
36. Gingrich B., Liu Y., Cascio C., Wang Z., Insel T.R. Dopamine D2 receptors in the nucleus accumbens are important for social attachment in female prairie voles (Microtus ochrogaster). Behav. Neurosci. 114:2000;173-183
37. Goodson J.L., Bass A.H. Social behavior functions and related anatomical characteristics of vasotocin/vasopressin systems in vertebrates. Brain Res. Brain Res. Rev. 35:2001;246-265
38. Green L., Fein D., Modahl C., Feinstein C., Waterhouse L., Morris M. Oxytocin and autistic disorder: alterations in peptide forms. Biol. Psychiatry. 50:2001;609-613
39. Hammock E.A.D., Young L.J. Variation in the vasopressin V1a receptor promoter and expression: implications for inter- and intraspecific variation in social behaviour. Eur. J. Neurosci. 16:2002;399-402
40. Hammock E.A.D., Young L.J. Functional microsatellite polymorphism associated with divergent social structure in vole species. Mol. Biol. E. 2(6):2004;1057-1063
41. Haxby J.V., Hoffman E.A., Gobbini M.I. The distributed human neural system for face perception. Trends Cogn. Sci. 4:2000;223-233
42. Haznedar M.M., Buchsbaum M.S., Wei T.C., Hof P.R., Cartwright C., Bienstock C.A., Hollander E. Limbic circuitry in patients with autism spectrum disorders studied with positron emission tomography and magnetic resonance imaging. Am. J. Psychiatry. 157:2000;1994-2001
43. Hernando F., Schoots O., Lolait S.J., Burbach J.P. Immunohistochemical localization of the vasopressin V1b receptor in the rat brain and pituitary gland: anatomical support for its involvement in the central effects of vasopressin. Endocrinology. 142:2001;1659-1668
44. Hobson R.P. The autistic child's recognition of age- and sex-related characteristics of people. J. Autism. Dev. Disord. 17:1987;63-79
45. Hobson R.P., Ouston J., Lee A. What's in a face? The case of autism. Br. J. Psychol. 79(Pt 4):1988;441-453
46. Hollander E., Novotny S., Hanratty M., Yaffe R., DeCaria C.M., Aronowitz B.R., Mosovich S. Oxytocin infusion reduces repetitive behaviors in adults with autistic and Asperger's disorders. Neuropsychopharmacology. 28:2003;193-198
47. Howard M.A., Cowell P.E., Boucher J., Broks P., Mayes A., Farrant A., Roberts N. Convergent neuroanatomical and behavioural evidence of an amygdala hypothesis of autism. Neuroreport. 11:2000;2931-2935
48. Insel T.R., Young L.J. Neuropeptides and the evolution of social behavior. Curr. Opin. Neurobiol. 10:2000;784-789
49. Insel T.R., Young L.J. The neurobiology of attachment. Nat. Rev. Neurosci. 2:2001;129-136
50. Kendrick K.M., Keverne E.B., Baldwin B.A. Intracerebroventricular oxytocin stimulates maternal behaviour in the sheep. Neuroendocrinology. 46:1987;56-61
51. Kendrick K.M., Da Costa A.P., Broad K.D., Ohkura S., Guevara R., Levy F., Keverne E.B. Neural control of maternal behaviour and olfactory recognition of offspring. Brain Res. Bull. 44:1997;383-395
52. Kim S.J., Young L.J., Gonen D., Veenstra-VanderWeele J., Courchesne R., Courchesne E., Lord C., Leventhal B.L., Cook E.H. Jr., Insel T.R. Transmission disequilibrium testing of arginine vasopressin receptor 1A (AVPR1A) polymorphisms in autism. Mol. Psychiatry. 7:2002;503-507
53. Kovacs G.L., Sarnyai Z., Szabo G. Oxytocin and addiction: a review. Psychoneuroendocrinology. 23:1998;945-962
54. Landgraf R., Gerstberger R., Montkowski A., Probst J.C., Wotjak C.T., Holsboer F., Engelmann M. V1 vasopressin receptor antisense oligodeoxynucleotide into the septum reduced vasopressin binding, social discrimination abilities, and anxiety-related behavior in rats. J. Neurosci. 15:1995;4250-4258
55. Landgraf R., Frank E., Aldag J.M., Neumann I.D., Sharer C.A., Ren X., Terwilliger E.F., Niwa M., Wigger A., Young L.J. Viral vector-mediated gene transfer of the vole V1a vasopressin receptor in the rat septum: improved social discrimination and active social behaviour. Eur. J. Neurosci. 18:2003;403-411
56. Langdell T. Recognition of faces: an approach to the study of autism. J. Child Psychol. Psychiatry. 19:1978;255-268
57. Le Moal M., Dantzer R., Michaud B., Koob G.F. Centrally injected arginine vasopressin (AVP) facilitates social memory in rats. Neurosci. Lett. 77:1987;353-359
58. Lim M.M., Young L.J. Vasopressin-dependent neural circuits underlying pair bond formation in the monogamous prairie vole. Neuroscience. 125:2004;35-45
59. Lim M.M., Murphy A.Z., Young L.J. Ventral striatopallidal oxytocin and vasopressin V1a receptors in the monogamous prairie vole (Microtus ochrogaster). J. Comp. Neurol. 468:2004a;555-570
60. Lim M.M., Hammock E.A., Young L.J. The role of vasopressin in the genetic and neural regulation of monogamy. J. Neuroendocrinol. 16:2004b;325-332
61. Lim M.M., Wang Z., Olazabal D.E., Ren X., Terwilliger E.F., Young L.J. Enhanced partner preference in a promiscuous species by manipulating the expression of a single gene. Nature. 429(6993):2004;754-757
62. Lorberbaum, J.P., Kose, S., Dubno, J.R., Horwitz, A.R., Newman, J.D., Kose, R., Hamner, M.B., Bohning, D.E., Arana, G.W., George, M.S., 2003. A third fMRI study of healthy mothers hearing infant cries. In: American College of Neuropsychopharmacology, San Juan, Puerto Rico (Abstract Viewer/Itinerary Planner).
63. Lorberbaum J.P., Newman J.D., Dubno J.R., Horwitz A.R., Nahas Z., Teneback C.C., Bloomer C.W., Bohning D.E., Vincent D., Johnson M.R., Emmanuel N., Brawman-Mintzer O., Book S.W., Lydiard R.B., Ballenger J.C., George M.S. Feasibility of using fMRI to study mothers responding to infant cries. Depress. Anxiety. 10:1999;99-104
64. Loup F., Tribollet E., Dubois-Dauphin M., Dreifuss J.J. Localization of high-affinity binding sites for oxytocin and vasopressin in the human brain. An autoradiographic study. Brain Res. 555:1991;220-232
65. McCarthy M.M., Altemus M. Central nervous system actions of oxytocin and modulation of behavior in humans. Mol. Med. Today. 3:1997;269-275
66. Modahl C., Green L., Fein D., Morris M., Waterhouse L., Feinstein C., Levin H. Plasma oxytocin levels in autistic children. Biol. Psychiatry. 43:1998;270-277
67. Murphy M.R., Seckl J.R., Burton S., Checkley S.A., Lightman S.L. Changes in oxytocin and vasopressin secretion during sexual activity in men. J. Clin. Endocrinol. Metab. 65:1987;738-741
68. Nissen E., Gustavsson P., Widstrom A.M., Uvnas-Moberg K. Oxytocin, prolactin, milk production and their relationship with personality traits in women after vaginal delivery or cesarean section. J. Psychosom. Obstet. Gynaecol. 19:1998;49-58
69. Pedersen C.A., Ascher J.A., Monroe Y.L., Prange A.J. Jr. Oxytocin induces maternal behavior in virgin female rats. Science. 216:1982;648-650
70. Phelps S.M., Young L.J. Extraordinary diversity in vasopressin (V1a) receptor distributions among wild prairie voles (Microtus ochrogaster): patterns of variation and covariation. J. Comp. Neurol. 466:2003;564-576
71. Pierce K., Muller R.A., Ambrose J., Allen G., Courchesne E. Face processing occurs outside the fusiform 'face area' in autism: evidence from functional MRI. Brain. 124:2001;2059-2073
72. Pitkow L.J., Sharer C.A., Ren X., Insel T.R., Terwilliger E.F., Young L.J. Facilitation of affiliation and pair-bond formation by vasopressin receptor gene transfer into the ventral forebrain of a monogamous vole. J. Neurosci. 21:2001;7392-7396
73. Popik P., Vetulani J., van Ree J.M. Low doses of oxytocin facilitate social recognition in rats. Psychopharmacology. 106(1):1992;71-74
74. Risch N., Spiker D., Lotspeich L., Nouri N., Hinds D., Hallmayer J., Kalaydjieva L., McCague P., Dimiceli S., Pitts T., Nguyen L., Yang J., Harper C., Thorpe D., Vermeer S., Young H., Hebert J., Lin A., Ferguson J., Chiotti C., Wiese-Slater S., Rogers T., Salmon B., Nicholas P., Myers R.M., et al. A genomic screen of autism: evidence for a multilocus etiology. Am. J. Hum. Genet. 65:1999;493-507
75. Rosenblum L.A., Smith E.L., Altemus M., Scharf B.A., Owens M.J., Nemeroff C.B., Gorman J.M., Coplan J.D. Differing concentrations of corticotropin- releasing factor and oxytocin in the cerebrospinal fluid of bonnet and pigtail macaques. Psychoneuroendocrinology. 27:2002;651-660
76. Schultz R.T., Gauthier I., Klin A., Fulbright R.K., Anderson A.W., Volkmar F., Skudlarski P., Lacadie C., Cohen D.J., Gore J.C. Abnormal ventral temporal cortical activity during face discrimination among individuals with autism and Asperger syndrome. Arch. Gen. Psychiatry. 57:2000;331-340
77. Sparks B.F., Friedman S.D., Shaw D.W., Aylward E.H., Echelard D., Artru A.A., Maravilla K.R., Giedd J.N., Munson J., Dawson G., Dager S.R. Brain structural abnormalities in young children with autism spectrum disorder. Neurology. 59:2002;184-192
78. Szatmari P., Tuff L., Finlayson M.A., Bartolucci G. Asperger's syndrome and autism: neurocognitive aspects. J. Am. Acad. Child Adolesc. Psychiatry. 29:1990;130-136
79. Tantam D., Monaghan L., Nicholson H., Stirling J. Autistic children's ability to interpret faces: a research note. J. Child Psychol. Psychiatry. 30:1989;623-630
80. Thompson R., Gupta S., Miller K., Mills S., Orr S. The effects of vasopressin on human facial responses related to social communication. Psychoneuroendocrinology. 29:2004;35-48
81. Uckert S., Becker A.J., Ness B.O., Stief C.G., Scheller F., Knapp W.H., Jonas U. Oxytocin plasma levels in the systemic and cavernous blood of healthy males during different penile conditions. World J. Urol. 20:2003;323-326
82. Uvnas-Moberg K., Widstrom A.M., Nissen E., Bjorvell H. Personality traits in women 4 days postpartum and their correlation with plasma levels of oxytocin and prolactin. J. Psychosom. Obstet. Gynaecol. 11:1990;261-273
83. van Wimersma Greidanus T.B. Disturbed behavior and memory of the Brattelboro rat. Ann. New York Acad. Sci. 394:1982;655-662
84. van Wimersma Greidanus T.B., van Ree J.M., de Wied D. Vasopressin and Memory. Pharmacol. Ther. 20:1983;437-458
85. Wassink, T.H., Piven, J., Vieland, V.J., Pietila, J., Goedken, R.J., Folstein, S.E., Sheffield, V.C., (in press). Examination of AVPR1a as an autism susceptibility gene. Mol. Psychiatry.
86. Wersinger S.R., Ginns E.I., O'Carroll A.M., Lolait S.J., Young W.S. III Vasopressin V1b receptor knockout reduces aggressive behavior in male mice. Mol. Psychiatry. 7:2002;975-984
87. Winslow, J.T., 2003. Mouse social recognition and preference. In: Current Protocols in Neuroscience. Wiley, New York, pp. 8.16.11-18.16.16.
88. Winslow J.T., Noble P.L., Lyons C.K., Sterk S.M., Insel T.R. Rearing effects on cerebrospinal fluid oxytocin concentration and social buffering in rhesus monkeys. Neuropsychopharmacology. 28:2003;910-918
89. Witt D.M., Winslow J.T., Insel T.R. Enhanced social interactions in rats following chronic, centrally infused oxytocin. Pharmacol. Biochem. Behav. 43:1992;855-861
90. Young L.J., Lim M.M., Gingrich B., Insel T.R. Cellular mechanisms of social attachment. Horm. Behav. 40:2001;133-138
91. Young L.J., Nilsen R., Waymire K.G., MacGregor G.R., Insel T.R. Increased affiliative response to vasopressin in mice expressing the V1a receptor from a monogamous vole. Nature. 400:1999;766-768