Density and function of central serotonin (5-HT) transporters, 5-HT 1A and 5-HT2A receptors, and effects of their targeting on BTBR T+tf/J mouse social behavior

Journal of Neurochemistry

Volumn 116, Issue 2, 2011, Pages 291-303

  Gould, Georgianna G ^a   Hensler, Julie G ^a   Burke, Teresa F ^a   Benno, Robert H ^b   Onaivi, Emmanuel S ^b   Daws, Lynette C ^a  

^a Mays Cancer Center at UT Health San Antonio   (United States)

^b WILLIAM PATERSON UNIVERSITY   (United States)

Author keywords

5 HT1A receptor; buspirone; CA1 of hippocampus; fluoxetine; SERT; sociability

Indexed keywords

2 DIPROPYLAMINO 8 HYDROXYTETRALIN; BUSPIRONE; CIANOPRAMINE; CITALOPRAM; FLUOXETINE; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN GAMMA SUBUNIT; RISPERIDONE; SEROTONIN 1A RECEPTOR; SEROTONIN 2A RECEPTOR; SEROTONIN TRANSPORTER; TRITIUM;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN HOMOGENATE; BTBR MOUSE; C57BL 10 MOUSE; C57BL 6 MOUSE; COMPULSION; CONTROLLED STUDY; HIPPOCAMPUS; MALE; MOUSE; MOUSE STRAIN; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; RECEPTOR BINDING; SOCIAL INTERACTION; SOCIOPATHY; STRAIN DIFFERENCE;

ANIMALS; BRAIN; BUSPIRONE; FLUOXETINE; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED STRAINS; PROTEIN BINDING; PROTEIN TRANSPORT; RECEPTOR, SEROTONIN, 5-HT1A; RECEPTOR, SEROTONIN, 5-HT2A; SEROTONIN PLASMA MEMBRANE TRANSPORT PROTEINS; SOCIAL BEHAVIOR;

MUS;

EID: 78650706553     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2010.07104.x     Document Type: Article

References (100)

1. Ayhan Y., Abazyan B., Nomura J., Kim R., Ladenheim B., Krasnova I. N., Sawa A., Margolis R. L., Cadet J. L., Mori S., Vogel M. W., Ross C. A., and, Pletnikov M. V., (2010) Differential effects of prenatal and postnatal expressions of mutant human DISC1 on neurobehavioral phenotypes in transgenic mice: evidence for neurodevelopmental origin of major psychiatric disorders. Mol. Psychiatry in press, doi:.
2. Anderson G. M., Horne W. C., Chatterjee D., and, Cohen D. J., (1990) The hyperserotonemia of autism. Ann. N Y Acad. Sci. 600, 331-340.
3. Bartlett C. W., Gharani N., Millonig J. H., and, Brzustowicz L. M., (2005) Three autism candidate genes: a synthesis of human genetic analysis with other disciplines. Int. J. Dev. Neurosci. 23, 221-234.
4. Bartolomucci A., Carola V., Pascucci T., Puglisi-Allegra S., Cabib S., Lesch K. P., Parmigiani S., Palanza P., and, Gross C., (2010) Increased vulnerability to psychosocial stress in heterozygous serotonin transporter knockout mice. Dis. Model. Mech. 3, 459-470.
5. Benno R. H., Liggett A., Sagato F., and, Schanz N., (2008) The potential role of stress as a mechanism in the production of autism spectrum disorders in the BTBR T+tf/J mouse. Soc. Neurosci. Abstr. 446, 5.
6. Benno R., Smirnova Y., Vera S., Liggett A., and, Schanz N., (2009) Exaggerated responses to stress in the BTBR T+tf/J mouse: an unusual behavioral phenotype. Behav. Brain Res. 197, 462-465.
7. Blatt G. J., Fitzgerald C. M., Guptill J. T., Booker A. B., Kemper T. L., and, Bauman M. L., (2001) Density and distribution of hippocampal neurotransmitter receptors in autism: an autoradiographic study. J. Autism Dev. Disord. 31, 537-543.
8. Bolivar V. J., Walters S. R., and, Phoenix J. L.,. (2007) Assessing autism-like behavior in mice: variations in social interactions among inbred strains. Behav. Brain Res. 176, 21-26.
9. Borue X., Chen J., and, Condron B. G., (2007) Developmental effects of SSRIs: lessons learned from animal studies. Int. J. Dev. Neurosci. 25, 341-347.
10. Boylan C. B., Blue M. E., and, Hohmann C. F., (2007) Modeling early cortical serotonergic deficits in autism. Behav. Brain Res. 176, 94-108.
11. Brahm N. C., Fast G. A., and, Brown R. C., (2008) Buspirone for autistic disorder in a woman with an intellectual disability. Ann. Pharmacother. 42, 131-137.
12. Bruins-Slot L. A., Bardin L., Auclair A. L., Depoortere R., and, Newman-Tancredi A., (2008) Effects of antipsychotics and reference monoaminergic ligands on marble burying behavior in mice. Behav. Pharmacol. 19, 145-152.
13. Brune C. W., Kim S. J., Salt J., Leventhal B. L., Lord C., and, Cook E. H., (2006) 5-HTTLPR Genotype-specific phenotype in children and adolescents with autism. Am. J. Psychiatry. 163, 2148-2156.
14. Caspi A., Sugden K., Moffitt T. E., Taylor A., Craig I. W., Harrington H., McClay J., Mill J., Martin J., Braithwaite A., and, Poulton R., (2003) Influence of life stress on depression: moderation by a polymorphism in the 5-HTT gene. Science 301, 386-389.
15. Carneiro A. M., Airey D. C., Thompson B., Zhu C. B., Lu L., Chesler E. J., Erikson K. M., and, Blakely R. D., (2009) Functional coding variation in recombinant inbred mouse lines reveals multiple serotonin transporter-associated phenotypes. Proc. Natl Acad. Sci. USA 106, 2047-2052.
16. Chadman K., (2010) Fluoxetine but not risperidone increases sociability in the BTBR mouse model of autism. Pharmacol. Biochem. Behav. in press, doi:.
17. Chandana S. R., Behen M. E., Juhász C., Muzik O., Rothermel R. D., Mangner T. J., Chakraborty P. K., Chugani H. T., and, Chugani D. C., (2005) Significance of abnormalities in developmental trajectory and asymmetry of cortical serotonin synthesis in autism. Int. J. Dev. Neurosci. 23, 171-182.
18. Cho I. H., Yoo H. J., Park M., Lee Y. S., and, Kim S. A., (2007) Family-based association study of 5-HTTLPR and the 5-HT2A receptor gene polymorphisms with autism spectrum disorder in Korean trios. Brain Res. 1139, 34-41.
19. Chubb J. E., Bradshaw N. J., Soares D. C., Porteous D. J., and, Millar J. K., (2008) The DISC locus in psychiatric illness. Mol. Psychiatry 13, 36-64.
20. Chugani D. C., (2002) Role of altered brain serotonin mechanisms in autism. Mol. Psychiatry 7, S16-S17.
21. Clapcote S. J., and, Roder J. C., (2006) Deletion polymorphism of Disc1 is common to all 129 mouse substrains: implications for gene-targeting studies of brain function. Genetics. 173, 2407-2410.
22. Clapcote S. J., and, Roder J. C., (2007) Inbred mouse strains 101/RI, BTBR T tf/J and LP/J have a deletion in Disc1. MGI Direct Data Submission. Ref ID J:118317.
23. Crawley J. N., (2007) Mouse behavioral assays relevant to the symptoms of autism. Brain Pathol. 17, 448-459.
24. Crowley J. J., Blendy J. A., and, Lucki I., (2006) Strain-dependent antidepressant-like effects of citalopram in the mouse tail suspension test. Psychopharmacology 183, 257-264.
25. 3H] imipramine. J. Pharmacol. Exp. Ther. 242, 364-371.
26. Daws L. C., (2009) Unfaithful neurotransmitter transporters: focus on serotonin uptake and implications for antidepressant efficacy. Pharmacol. Ther. 121, 89-99.
27. Deacon R. M., Thomas C. L., Rawlins J. N., and, Morley B. J., (2007) A comparison of the behavior of C57BL/6 and C57BL/10 mice. Behav. Brain Res. 179, 239-247.
28. Devlin B., Cook E., Coon H., Dawson G., Grigorenko E., McMahon W., Minshew N., Pauls D., Smith M., Spence M., Rodier P., Stodgell C., Network C. G., and, Schellenberg G., (2005) Autism and the serotonin transporter: the long and short of it. Mol. Psychiatry 10, 1110-1116.
29. Dolzan V., Serretti A., Mandelli L., Koprivsek J., Kastelic M., and, Plesnicar B. K., (2008) Acute antipyschotic efficacy and side effects in schizophrenia: association with serotonin transporter promoter genotypes. Prog. Neuropsychopharmacol. Biol. Psychiatry 32, 1562-1566.
30. Dulawa S. C., Holick K. A., Gundersen B., and, Hen R., (2004) Effects of chronic fluoxetine in animal models of anxiety and depression. Neuropsychopharmacology 29, 1321-1330.
31. Duan X., Chang J. H., Ge S., Faulkner R. L., Kim J. Y., Kitabatake Y., Liu X. B., Yang C. H., Jordan J. D., Ma D. K., Liu C. Y., Ganesan S., Cheng H. J., Ming G. L., Lu B., and, Song H., (2007) Disrupted-In-Schizophrenia 1 regulates integration of newly generated neurons in the adult brain. Cell 130, 1146-1158. (Pubitemid 47422304)
32. Fairless A. H., Dow H. C., Toledo M. M., Malkus K. A., Edelmann M., Li H., Talbot K., Arnold S. E., Abel T., and, Brodkin E. S., (2008) Low sociability is associated with reduced size of the corpus callosum in the BALB/cJ inbred mouse strain. Brain Res. 1230, 211-217.
33. Fernandez F., Coomans V., Mormede P., and, Chaouloff F., (2001) Effects of corticosterone ingestion on hippocampal [(3)H]serotonin reuptake in inbred rat strains. Endocr. Regul. 35, 119-126.
34. File S. E., and, Seth P., (2003) A review of 25 years of the social interaction test. Eur. J. Pharmacol. 463, 35-53.
35. 1A receptor-based responses in mice genetically deficient in the serotonin 5-HT transporter (SERT). Br. J. Pharmacol. 159, 879-887.
36. Frye C. A., and, Llaneza D. C., (2010) Corticosteroid and neurosteroid dysregulation in an animal model of autism, BTBR mice. Physiol. Behav. 100, 264-267.
37. Geary W. A., Toga A. W., and, Wooten G. F., (1985) Quantitative film autoradiography for tritium: methodological considerations. Brain Res. 337, 99-108.
38. Gelernter J., Kranzler H., and, Cubells J. F., (1997) Serotonin transporter protein (SLC6A4) alleleand haplotype frequencies and linkage disequilibria in African- and European-American and Japanese populations and in alcohol-dependent subjects. Hum. Genet. 101, 243-246.
39. Henry C. A., Shervin D., Neumeyer A., Steingard R., Spybrook J., Choueiri R., and, Bauman M., (2009) Retrial of selective serotonin reuptake inhibitors in children with pervasive developmental disorders: a retrospective chart review. J. Child Adolesc. Psychopharmacol. 19, 111-117.
40. Hensler J. G., Advani T., and, Monteggia L. M., (2007) Regulation of serotonin-1A receptor function in inducible brain-derived neurotrophic factor knockout mice after administration of corticosterone. Biol. Psychiatry 62, 521-529.
41. Holmes A., Yang R. J., Murphy D. L., and, Crawley J. N., (2002) Evaluation of antidepressant-related behavioral responses in mice lacking the serotonin transporter. Neuropsychopharmacology 27, 914-923.
42. Jackson Laboratory (2008) JAX Mice Database Data Sheet 002282 BTBR T+ tf/J. Available at: http://jaxmice.jax.org/strain/002282.html.
43. Jansen F., Heiming R. S., Lewejohann L., Touma C., Palme R., Schmitt A., Lesch K. P., and, Sachser N., (2010) Modulation of behavioural profile and stress response by 5-HTT genotype and social experience in adulthood. Behav. Brain Res. 207, 21-29.
44. Jones K. L., Smith R. M., Edwards K. S., Givens B., Tilley M. R., and, Beversdorf D. Q., (2010) Combined effect of maternal serotonin transporter genotype and prenatal stress in modulating offspring social interaction in mice. Int. J. Dev. Neurosci. 28, 529-536.
45. Kovachich G. B., Aronson C. E., Brunswick D. J., and, Frazer A., (1988) Quantitative autoradiography of serotonin uptake sites in rat brain using [3H] cyanoimipramine. Brain Res. 454, 78-88.
46. Kirsch I., Deacon B. J., Huedo-Medina T. B., Scoboria A., Moore T. J., and, Johnson B. T., (2008) Initial severity and antidepressant benefits: a meta-analysis of data submitted to the Food and Drug Administration. PLoS Med. 5, e45.
47. Kusek G. K., Wahlsten D., Herron B. J., Bolivar V. J., and, Flaherty L., (2007) Localization of two new X-linked quantitative trait loci controlling corpus callosum size in the mouse. Genes Brain Behav. 6, 359-363.
48. Lam K. S., Aman M. G., and, Arnold L. E., (2006) Neurochemical correlates of autistic disorder: a review of the literature. Res. Dev. Disabil. 27, 254-289.
49. Lesch K. P., Bengel D., Heils A., Sabol S. Z., Greenberg B. D., Petri S., Benjamin J., Muller C. R., Hamer D. H., and, Murphy D. L., (1996) Association of anxiety-related traits with a polymorphism in the serotonin transporter gene regulatory region. Science 274, 1527-1531.
50. Li Q., Wichems C., Heils A., Lesch K. P., and, Murphy D. L., (2000) Reduction in the density and expression, but not G-protein coupling, of serotonin receptors (5-HT1A) in 5-HT transporter knock-out mice: gender and brain region differences. J. Neurosci. 20, 7888-7895.
51. 2C receptors in serotonin transporter knockout mice. J. Neurochem. 84, 1256-1265.
52. Maines L. W., Keck B. J., Smith J. E., and, Lakoski J. M., (1999) Corticosterone regulation of serotonin transporter and 5-HT1A receptor expression in the aging brain. Synapse 32, 58-66.
53. Makkonen I., Riikonen R., Kokki H., Airaksinen M. M., and, Kuikka J. T., (2008) Serotonin and dopamine transporter binding in children with autism determined by SPECT. Dev. Med. Child Neurol. 50, 593-597.
54. MacPherson P., McGaffigan R., Wahlsten D., and, Nguyen P. V., (2008) Impaired fear memory, altered object memory and modified hippocampal synaptic plasticity in split-brain mice. Brain Res. 1210, 179-188.
55. 2A antagonists and selective serotonin reuptake inhibitors in neuropsychiatric disorders. Neuropsychopharmacology 28, 402-412.
56. 1A receptor in mice: implications for obsessive-compulsive disorder. J. Pharmacol. Sci. 99, 154-159.
57. McFarlane H. G., Kusek G. K., Yang M., Phoenix J. L., Bolivar V. J., and, Crawley J. N., (2008) Autism-like behavioral phenotypes in BTBR T+tf/J mice. Genes Brain Behav. 7, 152-163.
58. McGrath K. E., Seidler F. J., and, Slotkin T. A., (1997) Convergent control of serotonin transporter expression by glucocorticoids and cocaine in fetal and neonatal rat brain. Brain Res. Dev. Brain Res. 104, 209-213.
59. Montañez S., Owens W. A., Gould G. G., Murphy D. L., and, Daws L. C., (2003) Exaggerated effect of fluvoxamine in heterozygote serotonin transporter knockout mice. J. Neurochem. 86, 210-219.
60. Mortensen O. V., Kristensen A. S., and, Wiborg O., (2001) Species-scanning mutagenesis of the serotonin transporter reveals residues essential in selective, high-affinity recognition of antidepressants. J. Neurochem. 79, 237-247.
61. Moy S. S., Nadler J. J., Perez A., Barbaro R. P., Johns J. M., Magnuson T. R., Piven J., and, Crawley J. N., (2004) Sociability and preference for social novelty in five inbred strains: an approach to assess autistic-like behavior in mice. Genes Brain Behav. 3, 287-302.
62. Moy S. S., Nadler J. J., Magnuson T. R., and, Crawley J. N., (2006) Mouse models of autism spectrum disorders: the challenge for behavioral genetics. Am. J. Med. Genet. 142C, 40-51.
63. Moy S. S., Nadler J. J., Young N. B., Perez A., Holloway L. P., Barbaro R. P., Barbaro J. R., Wilson L. M., Threadgill D. W., Lauder J. M., Magnuson T. R., and, Crawley J. N., (2007) Mouse behavioral tasks relevant to autism: phenotypes of 10 inbred strains. Behav. Brain Res. 176, 4-20.
64. Moy S. S., Nadler J. J., Young N. B., Nonneman R. J., Grossman A. W., Murphy D. L., D'Ercole A. J., Crawley J. N., Magnuson T. R., and, Lauder J. M., (2009) Social approach in genetically engineered mouse lines relevant to autism. Genes Brain Behav. 8, 129-142.
65. Murphy D. L., Uhl G. R., Holmes A., Ren-Patterson R., Hall F. S., Sora I., Detera-Wadleigh S., and, Lesch K. P., (2003) Experimental gene interaction studies with SERT mutant mice as models for human polygenic and epistatic traits and disorders. Genes Brain Behav. 2, 350-364.
66. Murrin L. C., Sanders J. D., and, Bylund D. B., (2007) Comparison of the maturation of the adrenergic and serotonergic neurotransmitter systems in the brain: implications for differential drug effects on juveniles and adults. Biochem. Pharmacol. 73, 1225-1236.
67. Nadler J. J., Moy S. S., Dold G., Trang D., Simmons N., Perez A., Young N. B., Barbaro R. P., Piven J., Magnuson T. R., and, Crawley J. N., (2004) Automated apparatus for quantitation of social approach behaviors in mice. Genes Brain Behav. 3, 303-314.
68. Nakamura K., Sekine Y., Ouchi Y., Tsujii M., Yoshikawa E., Futatsubashi M., Tsuchiya K. J., Sugihara G., Iwata Y., Suzuki K., Matsuzaki H., Suda S., Sugiyama T., Takei N., and, Mori N., (2010) Brain serotonin and dopamine transporter bindings in adults with high-functioning autism. Arch. Gen. Psychiatry 67, 59-68.
69. Noskova T., Pivac N., Nedic G., Kazantseva A., Gaysina D., Faskhutdinova G., Gareeva A., Khalilova Z., Khusnutdinova E., Kovacic D. K., Kovacic Z., Jokic M., and, Seler D. M., (2008) Ethnic differences in the serotonin transporter polymorphism (5-HTTLPR) in several European populations. Prog. Neuropsychopharmacol. Biol. Psychiatry 32, 1735-1739.
70. Onaivi E. S., Benno R., Halpern T., Mehanovic M., Schanz N., Sanders C., Yan X., Ishiguro H., Liu Q. R., Berzal A. L., Viveros M. P., and, Ali S. F., (2010) Consequences of cannabinoid and monoaminergic system disruption in a mouse model of autism spectrum disorders. Curr. Neuropharmacol., in press.
71. 2C in autism spectrum disorders in Brazilian families. Brain Res. 1250, 14-19.
72. Pardo C. A., and, Eberhart C. G., (2007) The neurobiology of autism. Brain Pathol. 17, 434-447.
73. Pascucci T., Andolina D., Ventura R., Puglisi-Allegra S., and, Cabib S., (2008) Reduced availability of brain amines during critical phases of postnatal development in a genetic mouse model of cognitive delay. Brain Res. 1217, 232-238.
74. Paul L. K., Schieffer B., and, Brown W. S., (2004) Social processing deficits in primary agenesis of the corpus callosum: narratives from the Thematic Apperception Test. Arch. Clin. Neuropsychol. 19, 215-225.
75. Pearson B. L., Defensor E. B., Blanchard D. C., and, Blanchard R. J., (2010) C57BL/6J mice fail to exhibit preference for social novelty in the three-chamber apparatus. Behav. Brain Res. 213, 189-194.
76. Petkov P. M., Ding Y., Cassell M. A., Zhang W., Wagner G., Sargent E. E., Asquith S., Crew V., Johnson K. A., Robinson P., Scott V. E., and, Wiles M. V., (2004) An efficient SNP system for mouse genome scanning and elucidating strain relationships. Genome Res. 14, 1806-1811.
77. Raznahan A., Pugliese L., Barker G. J., Daly E., Powell J., Bolton P. F., and, Murphy D. G., (2009) Serotonin transporter genotype and neuroanatomy in autism spectrum disorders. Psychiatr. Genet. 19, 147-150.
78. Realmuto G., August G., and, Garfinkel B., (1989) Clinical effect of buspirone in autistic children. J. Clin. Psychopharmacol. 9, 122-125.
79. 1A autoreceptor levels determine vulnerability to stress and response to antidepressants. Neuron 65, 40-52.
80. Rossi D. V., Burke T. F., McCasland M., and, Hensler J. G., (2008) Serotonin-1A receptor function in the dorsal raphe nucleus following chronic administration of the selective serotonin reuptake inhibitor sertraline. J. Neurochem. 105, 1091-1099.
81. Ryan B. C., Young N. B., Crawley J. N., Bodfish J. W., and, Moy S. S., (2010) Social deficits, stereotypy and early emergence of repetitive behavior in the C58/J inbred mouse strain. Behav. Brain Res. 208, 178-188.
82. Santangelo S. L., and, Tsatsanis K., (2005) What is known about autism: genes, brain, and behavior. Am. J. Pharmacogenomics 5, 71-92.
83. Silverman J. L., Tolu S. S., Barkan C. L., and, Crawley J. N., (2010) Repetitive self-grooming behavior in the BTBR mouse model of autism is blocked by the mGluR5 antagonist MPEP. Neuropsychopharmacology 35, 976-989.
84. Slotkin T. A., McCook E. C., Ritchie J. C., Carroll B. J., and, Seidler F. J., (1997) Serotonin transporter expression in rat brain regions and blood platelets: aging and glucocorticoid effects. Biol. Psychiatry 41, 172-183.
85. Symington S. H., Paul L. K., Symington M. F., Ono M., and, Brown W. S., (2010) Social cognition in individuals with agenesis of the corpus callosum. Soc. Neurosci. 5, 296-308.
86. Sutcliffe J. S., Delahanty R. J., Prasad H. C., McCauley J. L., Han Q., Jiang L., Li C., Folstein S. E., and, Blakely R. D., (2005) Allelic heterogeneity at the serotonin transporter locus (SLC6A4) confers susceptibility to autism and rigid-compulsive behaviors. Am. J. Hum. Genet. 77, 265-279.
87. Thomas A., Burant A., Bui N., Graham D., Yuva-Paylor L. A., and, Paylor R., (2009) Marble burying reflects a repetitive and perseverative behavior more than novelty-induced anxiety. Psychopharmacology 204, 361-373.
88. 2 receptor activation. Brain Res. 957, 174-182.
89. Veenstra-Vanderweele J., Jessen T. N., Thompson B. J., Carter M., Prasad H. C., Steiner J. A., Sutcliffe J. S., and, Blakely R. D., (2009) Modeling rare gene variation to gain insight into the oldest biomarker in autism: construction of the serotonin transporter Gly56Ala knock-in mouse. J. Neurodev. Disord. 1, 158-171.
90. Veenstra-VanderWeele J., Kim S. J., Lord C., Courchesne R., Akshoomoff N., Leventhal B. L., Courchesne E., and, Cook E. H., Jr, (2002) Transmission disequilibrium studies of the serotonin 5-HT2A receptor gene (HTR2A) in autism. Am. J. Med. Genet. 114, 277-283.
91. Wahlsten D., Metten P., and, Crabbe J. C., (2003) Survey of 21 inbred mouse strains in two laboratories reveals that BTBR T/+ tf/tf has severely reduced hippocampal commissure and absent corpus callosum. Brain Res. 971, 47-54.
92. Wang D., Noda Y., Zhou Y., Nitta A., Furukawa H., and, Nabeshima T., (2007) Synergistic effect of galantamine with risperidone on impairment of social interaction in phencyclidine-treated mice as a schizophrenic animal model. Neuropharmacology 52, 1179-1187.
93. Wang C. I., and, Lewis R. J., (2009) Emerging structure-function relationships defining monoamine NSS transporter substrate and ligand affinity. Biochem. Pharmacol 79, 1083-1091.
94. West L., Waldrop J., and, Brunssen S., (2009) Pharmacologic treatment for the core deficits and associated symptoms of autism in children. J. Pediatr. Health Care 23, 75-89.
95. Whitaker-Azmitia P. M., (2005) Behavioral and cellular consequences of increasing serotonergic activity during brain development: a role in autism? Int. J. Dev. Neurosci. 23, 75-83.
96. Witmer P. D., Doheny K. F., Adams M. K., Boehm C. D., Dizon J. S., Goldstein J. L., Templeton T. M., Wheaton A. M., Dong P. N., Pugh E. W., Nussbaum R. L., Hunter K., Kelmenson J. A., Rowe L. B., and, Brownstein M. J., (2003) The development of a highly informative mouse Simple Sequence Length Polymorphism (SSLP) marker set and construction of a mouse family tree using parsimony analysis. Genome Res. 13, 485-491.
97. Yang M., Zhodzishsky V., and, Crawley J. N., (2007a) Social deficits in BTBR T+tf/J mice are unchanged by cross-fostering with C57BL/6J mothers. Int. J. Dev. Neurosci. 25, 515-521.
98. Yang M., Scattoni M. L., Zhodzishsky V., Chen T., Caldwell H., Young W. S., McFarlane H. G., and, Crawley J. N., (2007b) Social approach behaviors are similar on conventional versus reverse lighting cycles, and in replications across cohorts, in BTBR T+ tf/J, C57BL/6J, and vasopressin receptor 1B mutant mice. Front. Behav. Neurosci. 1, 1.
99. Yang M., Clarke A. M., and, Crawley J. N., (2009) Postnatal lesion evidence against a primary role for the corpus callosum in mouse sociability. Eur. J. Neurosci. 29, 1663-1677.
100. Yocca F. D., (1990) Neurochemistry and neurophysiology of buspirone and gepirone: interactions at presynaptic and postsynaptic 5-HT1A receptors. J. Clin. Psychopharmacol. 10, 6S-12S.