Animal Models of Autism Spectrum Disorders and Behavioral Techniques of their Examination

Autism Spectrum Disorder Fact Sheet. American Psychiatric Publishing, рр. 1-2 (2013).

S. J. Blumberg, M. D. Bramlett, M. D. Kogan, et al., “Changes in prevalence of parent-reported Autism Spectrum Disorder in school-aged U.S. children: 2007 to 2011–2012,” Nat. Health Stat. Rep., 65 , 1-11 (2013).

C. J. Newschaffer, L. A. Croen, J. Daniels, et al., “The epidemiology of autism spectrum disorders”, Annu. Rev. Public Health, 28, 235–258 (2007).

J. Piven and P. Palmer, “Psychiatric disorder and the broad autism phenotype: evidence from a family study of multiple-incidence autism families,” Am. J. Psych., 156, No. 4, 557-563 (1999).

N. Micali, S. Chakrabarti, and E. Fombonne, “The broad autism phenotype findings from an epidemiological survey,” Autism, 8, No. 1, 21-37 (2004).

American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders, 4th ed, American Psychiatric Association, Washington, DC (1994).

B. S. Abrahams and D. H. Geschwind, “Advances in autism genetics: on the threshold of a new neurobiology,” Nat. Rev. Genet., 9, No. 5, 341–355 (2008).

T. L. Arndt, C. J. Stodgell, and P. M. Rodier, “The teratology of autism,” Int. J. Dev. Neurosci., 23, No. 2–3, 189–99 (2005).

J. F. Shelton, I. Hertz-Picciotto, and I. N. Pessah, “Tipping the balance of autism risk: Potential mechanisms linking pesticides and autism,” Environ. Health Perspect., 120, No. 7, 944-951 (2012).

T. Bourgeron, S. Jamain, and S. Granon, “Animal models of autism. Transgenic and knockout models of neuropsychiatric disorders,” Contemp. Clin. Neurosci., 151-174 (2006).

S. E. Folstein and B. Rosen-Sheidley, “Genetics of autism: complex aetiology for a heterogeneous disorder,” Nat. Rev. Genet., 2, 943–955 (2001).

M. Rutter, “Incidence of autism spectrum disorders: changes over time and their meaning,” Acta Paediatr., 94, No. 1, 2–15 (2005).

C. Belzung, S. Leman, P. Vourc’h, and C. Andres, “Rodent models for autism: A critical review,” Drug Discov. Today: Dis. Models, 2, No. 2, 93-101 (2005).

T. B. Van Wimersma Greidanus, “Disturbed behavior and memory of the Brattleboro rat,” Ann. N.Y. Acad. Sci., 394, 655-662 (1982).

R. L. Pobbe, B. L. Pearson, and E. B. Defensor, “Oxytocin receptor knockout mice display deficits in the expression of autism-related behaviors,” Horm. Behav., 61, No. 3, 436-444 (2012).

M. Wцhr, A. Moles, R. K. Schwarting, and F. R. D’Amato, “Lack of social exploratory activation in male μ-opioid receptor KO mice in response to playback of female ultrasonic vocalizations,” Soc. Neurosci., 6, No. 1, 76-87 (2011).

M. Narita, A. Oyabu, Y. Imura, et al., “Nonexploratory movement and behavioral alterations in a thalidomide or valproic acid-induced autism model rat,” Neurosci. Res., 66, No. 1, 2–6 (2010).

D. Kahne, A. Tudorica, A. Borella, et al., “Behavioral and magnetic resonance spectroscopic studies in the rat hyperserotonemic model of autism,” Physiol. Behav., 75, No. 3, 403-410 (2002).

I. Lucki, “The spectrum of behaviors influenced by serotonin,” Biol. Psychiatry, 44, No. 3, 151-62 (1998).

P. T. Tsai, C. Hull, Y. X. Chu, et al., “Autistic-like behaviour and cerebellar dysfunction in Purkinje cell Tsc1 mutant mice,” Nature, 488, 647–651 (2012).

M. A. Mines, C. J. Yuskaitis, M. K. King, et al., “GSK3 influences social preference and anxiety-related behaviors during social interaction in a mouse model of fragile X syndrome and autism,” PLoS ONE, 5, No. 3, e9706 (2010).

K. M. Huber, S. M. Gallagher, S. T. Warren, and M. F. Bear, “Altered synaptic plasticity in a mouse model of fragile X mental retardation,” Proc. Natl. Acad. Sci. USA, 99, No. 11, 7746–7750 (2002).

N. J. Minshew, B. Luna, and J. A. Sweeney, “Oculomotor evidence for neocortical systems but not cerebellar dysfunction in autism,” Neurology, 52, No. 5, 917–922 (1999).

T. H. Wassink, J. Piven, V. J. Vieland, et al., “Examination of AVPR1a as an autism susceptibility gene,” Mol. Psychiatry, 9, 968–972 (2004).

M. D. Bauman, J. E. Toscano, B. A. Babineau, et al., “Emergence of stereotypies in juvenile monkeys (Macaca mulatta) with neonatal amygdala or hippocampus lesions,” Behav. Neurosci., 122, No. 5, 1005-1015 (2008).

L. Malkova, M. Mishkin, S. J. Suomi, and J. Bachevalier, “Long-term effects of neonatal medial temporal ablations on socioemotional behavior in monkeys (Macaca mulatta),” Behav. Neurosci., 124, No. 6, 742-760 (2010).

S. C. Panaitof, “A songbird animal model for dissecting the genetic bases of autism spectrum disorder,” Dis. Markers, 33, No. 5, 241–249 (2012).

J. F. Cryan and A. Holmes, “The ascent of mouse: advances in modelling human depression and anxiety,” Nat Rev Drug Discov., 4, No. 9, 775-790 (2005).

E. Grant and J. Macintosh, “A comparison of the social postures of some common laboratory rodents,” Behaviour, 21, 246–259 (1963).

C. S. Carter, J. R. Williams, D. M. Witt, and T. R. Insel, “Oxytocin and social bonding,” Ann. N.Y. Acad. Sci., 652, 204–211 (1992).

M. L. Terranova and G. Laviola, “Scoring of Social Interactions and Play in Mice During Adolescence,” Curr. Protoc. Toxicol., 13, No. 10 (2005).

H. G. McFarlane, G. K. Kusek, M. Yang, et al., “Autism-like behavioral phenotypes in BTBR T+tf/J mice,” Genes Brain Behav., 7, No. 2, 152-163 (2008).

M. A. Hofer and H. N. Shair, “Ultrasonic vocalization, laryngeal braking, and thermogenesis in rat pups: a reappraisal,” Behav. Neurosci., 107, 354–362 (1993).

K. A. Miczek, S. C. Maxson, E. W. Fish, S. Faccidomo, “Aggressive behavioral phenotypes in mice,” Behav. Brain Res., 125, 167–181 (2001).

J. T. Winslow, E. F. Hearn, J. Ferguson, et al., “Infant vocalization, adult aggression, and fear behavior of an oxytocin null mutant mouse,” Horm. Behav., 37, 145–155 (2000).

C. C. Wrenn, A. P. Harris, M. C. Saavedra, and J. N. Crawley, “Social transmission of food preference in mice: methodology and application to galanin-overexpressing transgenic mice,” Behav. Neurosci., 117, 21–31 (2003).

D. W. Wesson, M. Keller, Q. Douhard, et al., “Enhanced urinary odor discrimination in female aromatase knockout (ArKO) mice,” Horm. Behav., 49, 580–586 (2006).

J. B. Panksepp, K. A. Jochman, J. U. Kim, et al., “Affiliative behavior, ultrasonic communication and social reward are influenced by genetic variation in adolescent mice,” PLoS One, 2, e351 (2007).

S. R. Wersinger, H. K. Caldwell, L. Martinez, et al., “Vasopressin 1a receptor knockout mice have a subtle olfactory deficit but normal aggression,” Genes Brain Behav., 6, 540–551 (2007).

J. Brielmaier, P. G. Matteson, J. L. Silverman et al., “Autism-Relevant Social Abnormalities and Cognitive Deficits in Engrailed-2 Knockout Mice,” PLoS ONE, 7, No. 7, e40914 (2012).

S. S. Moy, J. J. Nadler, and N. B. Young, “Mouse Behavioral Tasks Relevant to Autism: Phenotypes of Ten Inbred Strains,” Behav. Brain Res., 176, No. 1, 4–20 (2007).

J. L. Silverman, S. M. Turner, C. L. Barkan, et al., “Sociability and motor functions in Shank1 mutant mice,” Brain Res., 1380, 120-137 (2011).

M. Alarcуn, B. S. Abrahams, J. L. Stone, et al., “Linkage, association, and gene-expression analyses identify CNTNAP2 as an autism-susceptibility gene,” Am. J. Hum. Genet., 82, No. 1, 150-159 (2008).

H. C. Whalley, G. O’Connell, J. E. Sussmann, et al., “Genetic variation in CNTNAP2 alters brain function during linguistic processing in healthy individuals,” Am. J. Med. Genet. B. Neuropsychiatr. Genet., 156, No. 8, 941-948 (2011).

T. M. DeLorey, P. Sahbaie, E. Hashemi, et al., “Gabrb3 gene deficient mice exhibit impaired social and exploratory behaviors, deficits in non-selective attention and hypoplasia of cerebellar vermal lobules: a potential model of autism spectrum disorder,” Behav. Brain. Res., 187, 207–220 (2008).

B. C. Ryan, N. B. Young, S. S. Moy, and J. N. Crawley, “Olfactory cues are sufficient to elicit social approach behaviors but not social transmission of food preference in C57BL/6J mice,” Behav. Brain Res., 193, 235–242 (2008).

K. Radyushkin, K. Hammerschmidt, S. Boretius, et al., “Neuroligin-3-deficient mice: model of a monogenic heritable form of autism with an olfactory deficit,” Genes Brain Behav., 8, 416–425 (2009).

E. Callaway, “Rat models on the rise in autism research,” Nature News, 23 November (2011).

E. C. Azmitia, A. V. Shemer, and P. M. Whitaker-Azmitia, “Dose-related effects of prenatal 5-methoxytryptamine (5-MT) on development of serotonin terminal density and behavior,” Dev. Brain Res., 59, No. 1, 59-63 (1991).

A. G. Foley, S. Gannon, N. Rombach-Mullan, et al., “Class I histone deacetylase inhibition ameliorates social cognition and cell adhesion molecule plasticity deficits in a rodent model of autism spectrum disorder,” Neuropharmacology, 63, 750-760 (2012).

J. Caston, E. Yon, D. Mellier, et al., “An animal model of autism: behavioural studies in the GS guinea-pig,” Eur. J. Neurosci., 10, No. 8, 2677-2684 (1998).

M. V. Pletnikov, T. H. Moran, and K. M. Carbone, “Borna disease virus infection of the neonatal rat: developmental brain injury model of autism spectrum disorders,” Front Biosci., 7, 593-607 (2002).

J. N. Crawley, What’s Wrong with My Mouse? Behavioral Phenotyping of Transgenic and Knockout Mice, John Wiley and Sons, 329 pp. (2000).

M. Yang, J. L. Silverman, and J. N. Crawley, “Automated three-chambered social approach task for mice,” in: Curr. Protoc. Neurosci., Chapter 8: Unit 8. 26 (2011).

J. J. Nadler, S. S. Moy, G. Dold, et al., “Automated apparatus for quantitation of social approach behaviors in mice,” Genes Brain Behav., 3, No. 5, 303-14 (2004).

J. Veenstra-Van der Weele, C. L. Muller, H. Iwamoto, et al., “Autism gene variant causes hyperserotonemia, serotonin receptor hypersensitivity, social impairment and repetitive behavior,” Proc. Natl. Acad. Sci. USA, 109, 5469–5474 (2012).

J. Bakker, S. Honda, N. Harada, and J. Balthazart,“Sexual partner preference requires a functional aromatase (cyp19) gene in male mice,” Horm. Behav., 42, 158–171 (2002).

T. H. Ahern, M. E. Modi, J. P. Burkett, and L. J. Young, “Evaluation of two automated metrics for analyzing partner preference tests,” J. Neurosci. Methods, 182, 180–188 (2009).

S. Jamain, K. Radyushkin, K. Hammerschmidt, et al., “Reduced social interaction and ultrasonic communication in a mouse model of monogenic heritable autism,” Proc. Natl. Acad. Sci. USA, 105, 1710–1715 (2008).

M. L. Scattoni, L. Ricceri, and J. N. Crawley, “Unusual repertoire of vocalizations in adult BTBR T + tf/J mice during three types of social encounters,” Genes Brain Behav., 10, 44–56 (2011).

O. Peсagarikano, B. S. Abrahams, E. I. Herman, et al., “Absence of CNTNAP2 leads to epilepsy, neuronal migration abnormalities, and core autism-related deficits,” Cell, 147, No. 1, 235-246 (2011).

J. L. Silverman, S. S. Tolu, C. L. Barkan, and J. N. Crawley, “Repetitive self-grooming behavior in the BTBR mouse model of autism is blocked by the mGluR5 antagonist MPEP,” Neuropsychopharmacology, 35, No. 4, 976-989 (2010).

A. Thomas, A. Burant, N. Bui, et al., “Marble burying reflects a repetitive and perseverative behavior more than novelty-induced anxiety,” Psychopharmacology (Berlin), 204, No. 2, 361-373 (2009).

J. P. J. Pinel and D. Treit, “Burying as a defensive response in rats,” J. Comp. Physiol. Psychol., 92, No. 4, 708–712 (1978).

C. L. Broekkamp, H. W. Rijk, D. Joly-Gelouin, and K. L. Lloyd, “Major tranquillizers can be distinguished from minor tranquillizers on the basis of effects on marble burying and swim-induced grooming in mice,” Eur. J. Pharmacol., 126, No. 3, 223-229 (1986).

K. Njung’e and S. L. Handley, “Evaluation of marbleburying behavior as a model of anxiety,” Pharmacol. Biochem. Behav., 38, No. 1, 63-67 (1991).

M. Wöhr and M. L. Scattoni, “Behavioural methods used in rodent models of autism spectrum disorders: Current standards and new developments,” Behav. Brain Res., 251, 5– 17 (2013).

C. Belzung, “Measuring rodent exploratory behavior,” in: Handbook of Molecular Genetic Techniques for Brain and Behavior Research, W. E. Crusio, and R. Gerlai (eds. ), Elsevier, Amsterdam (2001), pp. 739–749.

H. M. Zippelius and W. M. Schleidt, “Ultraschall-Laute bei jungen Mäusen,” Naturwissenschaften, 43, 502 (1956).

G. D. Sewell, “Ultrasonic communication in rodents,” Nature, 227, 410 (1970).

M. Wöhr, F. I. Roullet, A. Y. Hung, et al., “Communication impairments in mice lacking Shank1: Reduced levels of ultrasonic vocalizations and scent marking behavior,” PLoS ONE, 6, No. 6, e20631 (2011).

M. Wöhr, F. I. Roullet, and J. N. Crawley, “Reduced scent marking and ultrasonic vocalizations in the BTBR T+tf/J mouse model of autism,” Genes Brain Behav., 10, No. 1, 35-43 (2011).

C. S. Lai, D. Gerrelli, A. P. Monaco, and S. E. Fisher, “Copp AJ. FOXP2 expression during brain development coincides with adult sites of pathology in a severe speech and language disorder,” Brain, 126, No. 11, 2455-2462 (2003).

T. E. Holy and Z. Guo, “Ultrasonic songs of male mice,” PLoS Biol., 3, No. 12, e386 (2005).

G. Arriaga, E. P. Zhou, E. D. Jarvis, “Of Mice, Birds, and Men: The Mouse Ultrasonic Song System Has Some Features Similar to Humans and Song-Learning Birds,” PLoS ONE , 7, No. 10, e46610 (2012).

M. C. Condro, S. A. White, “Distribution of language-related Cntnap2 protein in neural circuits critical for vocal learning,” J. Compar. Neurol., 522, 169 (2014).

S. Haesler, C. Rochefort, B. Georgi, et al., “Incomplete and inaccurate vocal imitation after knockdown of FoxP2 in songbird basal ganglia nucleus Area X,” PLoS Biol, 5, e321 (2007).