Mouse Behavioral Assays Relevant to the Symptoms of Autism*
Open accessAbstract
While the cause of autism remains unknown, the high concordance between monozygotic twins supports a strong genetic component. The importance of genetic factors in autism encourages the development of mutant mouse models, to advance our understanding of biological mechanisms underlying autistic behaviors. Mouse models of human neuropsychiatric diseases are designed to optimize (i) face validity (resemblance to the human symptoms) (ii) construct validity (similarity to the underlying causes of the disease) and (iii) predictive validity (expected responses to treatments that are effective in the human disease). There is a growing need for mouse behavioral tasks with all three types of validity, to define robust phenotypes in mouse models of autism. Ideal mouse models will incorporate analogies to the three diagnostic symptoms of autism: abnormal social interactions, deficits in communication and high levels of repetitive behaviors. Social approach is tested in an automated three chambered apparatus that offers the subject a choice between spending time with another mouse, with a novel object, or remaining in an empty familiar environment. Reciprocal social interaction is scored from videotapes of interactions between pairs of unfamiliar mice. Communication is evaluated by measuring emission and responses to vocalizations and olfactory cues. Repetitive behaviors are scored for measures of grooming, jumping, or stereotyped sniffing of one location or object. Insistence on sameness is modeled by scoring a change in habit, for example, reversal of the spatial location of a reinforcer in the Morris water maze or T‐maze. Associated features of autism, for example, mouse phenotypes relevant to anxiety, seizures, sleep disturbances and sensory hypersensitivity, may be useful to include in a mouse model that meets some of the core diagnostic criteria. Applications of these assays include (i) behavioral phenotyping of transgenic and knockout mice with mutations in genes relevant to autism; (ii) characterization of inbred strains of mice; (iii) evaluation of environmental toxins; (iv) comparison of behavioral phenotypes with genetic factors, such as unusual expression patterns of genes or unusual single nucleotide polymorphisms; and (v) evaluation of proposed therapeutics for the treatment of autism.
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Impairments in social behavior is one of hallmarks of ASD.
“Because impairments in social behavior is one of hallmarks of ASD1415”
From Transient blockade of ERK phosphorylation in the critical period causes autistic phenotypes as an adult in mice (2015) · cites this paper as [15]
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Psychosis and autism as diametrical disorders of the social brain
Crespi, B. J., & Badcock, C. R. (2008) · Behavioral and Brain Sciences · doi:10.1017/s0140525x08004214 · Cited by 618 · see citing works
“Various animal models of autism are being similarly explored (Crawley 2007; Moy et al. 2007).”
BackgroundAutomated Three‐Chambered Social Approach Task for Mice
Yang, M., Silverman, J. L., & Crawley, J. N. (2011) · Current Protocols in Neuroscience · doi:10.1002/0471142301.ns0826s56 · Cited by 598 · see citing works
Self-citationUnusual repertoire of vocalizations in the BTBR T+tf/J mouse model of autism
Scattoni, M. L., Gandhy, S. U., Ricceri, L., & Crawley, J. N. (2008) · PLoS ONE · doi:10.1371/journal.pone.0003067 · Cited by 550 · see citing works
“We hypothesize that USVs may be a measure of social communication in mice [15,26–28].”
BackgroundSelf-citationEtherton, M. R., Blaiss, C. A., Powell, C. M., & Südhof, T. C. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0910297106 · Cited by 447 · see citing works
Neuroligin-1 Deletion Results in Impaired Spatial Memory and Increased Repetitive Behavior
Blundell, J., Blaiss, C. A., Etherton, M. R., Espinosa, F., Tabuchi, K., Walz, C., Bolliger, M. F., Südhof, T. C., & Powell, C. M. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.4517-09.2010 · Cited by 450 · see citing works
“…2003; Chih et al., 2004; Comoletti et al., 2004; Laumonnier et al., 2004; Feng et al., 2006; Szatmari et al., 2007), we characterized grooming behavior in NL1 KO mice, a behavior that might reflect the repetitive, stereotyped behavior core symptom domain of autism (Moy et al., 2006; Crawley, 2007).”
BackgroundSilverman, J. L., Tolu, S. S., Barkan, C. L., & Crawley, J. N. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2009.201 · Cited by 438 · see citing works
“Time spent in each chamber and number of entries into each chamber was calculated by the automated software, based on the movements of the subject mouse in sequentially breaking and unbreaking a series of photocell beams embedded in the openings between chambers (Crawley, 2007).”
InfluentialSelf-citationMacFabe, D. F. (2012) · Microbial Ecology in Health and Disease · doi:10.3402/mehd.v23i0.19260 · Cited by 432 · see citing works
“There have been a number of valid animal models of ASDs, concentrating on genetic knockouts of key neurodevelopmental processes (112, 113) and also on exposures to environmental factors such as metals, drugs (valproic acid, terbutaline) (114, 115), viruses (116) and inflammatory agents (i.”
BackgroundMarble Burying and Nestlet Shredding as Tests of Repetitive, Compulsive-like Behaviors in Mice
Angoa‐Pérez, M., Kane, M. J., Briggs, D. I., Francescutti, D. M., & Kuhn, D. M. (2013) · Journal of Visualized Experiments · doi:10.3791/50978 · Cited by 391 · see citing works
Meyer, U., Feldon, J., & Fatemi, S. H. (2009) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2009.05.001 · Cited by 367 · see citing works
“Likewise, abnormalities in one particular brain area or neurotransmitter system are likely to have an impact on a wide range of behavioral, cognitive and pharmacological functions (Arguello and Gogos, 2006; Crawley, 2007, 2008).”
Epidemiology-driven neurodevelopmental animal models of schizophrenia
Meyer, U., & Feldon, J. (2009) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2009.10.018 · Cited by 366 · see citing works
“…used to study schizophrenia-like functional phenotypes summarized in Table 1 may also be relevant for the phenotypic characterization of functional brain abnormalities relevant to other neurodevelopmental brain disorders, especially autism (Moy et al., 2006; Moy and Nadler, 2008; Crawley, 2007).”
BackgroundEtherton, M. R., Földy, C., Sharma, M., Tabuchi, K., Liu, X., Shamloo, M., Malenka, R. C., & Südhof, T. C. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1111093108 · Cited by 340 · see citing works
Validating γ oscillations and delayed auditory responses as translational biomarkers of autism
Gandal, M. J., Edgar, J. C., Ehrlichman, R. S., Mehta, M., Roberts, T. P. L., & Siegel, S. J. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.09.031 · Cited by 314 · see citing works
Bauman, M. D., Iosif, A.-M., Smith, S. E. P., Bregere, C., Amaral, D. G., & Patterson, P. H. (2014) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.06.025 · Cited by 294 · see citing works
Young, J. W., Powell, S. B., Risbrough, V. B., Marston, H. M., & Geyer, M. A. (2009) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2009.02.004 · Cited by 299 · see citing works
Smith, S. E. P., Zhou, Y.-D., Zhang, G., Jin, Z., Stoppel, D. C., & Anderson, M. P. (2011) · Science Translational Medicine · doi:10.1126/scitranslmed.3002627 · Cited by 267 · see citing works
Deczkowska, A., Matcovitch-Natan, O., Tsitsou-Kampeli, A., Ben-Hamo, S., Dvir-Szternfeld, R., Spinrad, A., Singer, O., David, E., Winter, D. R., Smith, L. K., et al. (2017) · Nature Communications · doi:10.1038/s41467-017-00769-0 · Cited by 260 · see citing works
The Emerging Picture of Autism Spectrum Disorder: Genetics and Pathology
Chen, J. A., Peñagarikano, O., Belgard, T. G., Swarup, V., & Geschwind, D. H. (2015) · Annual Review of Pathology: Mechanisms of Disease · doi:10.1146/annurev-pathol-012414-040405 · Cited by 254 · see citing works
Characterization of behavioral and endocrine effects of LSD on zebrafish
Grossman, L., Utterback, E., Stewart, A., Gaikwad, S., Chung, K. M., Suciu, C., Wong, K., Elegante, M. F., Elkhayat, S. I., Tan, J., et al. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.05.039 · Cited by 247 · see citing works
Exploring the Validity of Valproic Acid Animal Model of Autism
Mabunga, D. F. N., Gonzales, E. L., Kim, J., Kim, K. C., & Shin, C. Y. (2015) · Experimental Neurobiology · doi:10.5607/en.2015.24.4.285 · Cited by 247 · see citing works
“[73] reasoned that a quantitative measure of social interaction is an essential factor in establishing an animal model of autism.”
BackgroundComputerized video analysis of social interactions in mice
de Chaumont, F., Coura, R., Serreau, P., Cressant, A., Chabout, J., Granon, S., & Olivo‐Marín, J. (2012) · Nature Methods · doi:10.1038/nmeth.1924 · Cited by 238 · see citing works
“…of the location or duration of the scene); (iii) some events result from the temporal and/or logical concatenation of the previous ones, thus increasing the complexity of the analysis (for example, event 15 is the logical concatenation of events 5 and 8 conditioned on a distance threshold).”
BackgroundBitanihirwe, B. K., Peleg-Raibstein, D., Mouttet, F., Feldon, J., & Meyer, U. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2010.129 · Cited by 237 · see citing works
“As mice (like most other rodents) are highly social animals, social interaction can be efficiently studied under experimental conditions (Crawley, 2007).”
BackgroundTranslational animal models of autism and neurodevelopmental disorders
Crawley, J. N. (2012) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2012.14.3/jcrawley · Cited by 227 · see citing works
“This 3-chambered assay, which was developed by our team to provide a simple measure of general sociability,(30) is widely used as an initial, highthroughput test for social deficits in mouse models of autism.(27,32,34,38,41,64-70)”
MethodSelf-citationSociability and motor functions in Shank1 mutant mice
Silverman, J. L., Turner, S. M., Barkan, C. L., Tolu, S. S., Saxena, R., Hung, A. Y., Sheng, M., & Crawley, J. N. (2011) · Brain Research · doi:10.1016/j.brainres.2010.09.026 · Cited by 218 · see citing works
Self-citationSpencer, C. M., Alekseyenko, O. V., Hamilton, S. M., Thomas, A. M., Serysheva, E., Yuva‐Paylor, L. A., & Paylor, R. E. (2011) · Autism Research · doi:10.1002/aur.168 · Cited by 215 · see citing works
Animal Models of Neuropsychiatric Disorders
Fernando, A. B. P., & Robbins, T. W. (2011) · Annual Review of Clinical Psychology · doi:10.1146/annurev-clinpsy-032210-104454 · Cited by 216 · see citing works
“The recent keen interest in animal models of autism (Crawley 2007) is thus also relevant to negative symptoms in schizophrenia.”
BackgroundSomatostatin interneurons in the prefrontal cortex control affective state discrimination in mice
Scheggia, D., Managò, F., Maltese, F., Bruni, S., Nigro, M., Dautan, D., Latuske, P., Contarini, G., Gomez-Gonzalo, M., Requie, L. M., et al. (2020) · Nature Neuroscience · doi:10.1038/s41593-019-0551-8 · Cited by 192 · see citing works
Prenatal Programming of Mental Illness: Current Understanding of Relationship and Mechanisms
Kim, D. R., Bale, T. L., & Epperson, C. N. (2015) · Current Psychiatry Reports · doi:10.1007/s11920-014-0546-9 · Cited by 203 · see citing works
Sinclair, D., Oranje, B., Razak, K. A., Siegel, S. J., & Schmid, S. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.05.029 · Cited by 198 · see citing works
Reith, R. M., McKenna, J., Wu, H. C., Hashmi, S. S., Cho, S., Dash, P. K., & Gambello, M. J. (2012) · Neurobiology of Disease · doi:10.1016/j.nbd.2012.10.014 · Cited by 191 · see citing works
“A number of behavioral paradigms have been developed to asses social interactions inmice (Crawley, 2007).”
Peripheral and central inflammation in autism spectrum disorders
Depino, A. M. (2013) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2012.10.003 · Cited by 189 · see citing works
Human Models Are Needed for Studying Human Neurodevelopmental Disorders
Zhao, X., & Bhattacharyya, A. (2018) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2018.10.009 · Cited by 192 · see citing works
Mehta, M. V., Gandal, M. J., & Siegel, S. J. (2011) · PLoS ONE · doi:10.1371/journal.pone.0026077 · Cited by 182 · see citing works
“Several mouse behavioral paradigms have been proposed to assess the repetitive, restricted behaviors and insistence on sameness, which comprise the third core symptomatic domain of autism [24,38,39,40,41,42].”
BackgroundWöhr, M., & Scattoni, M. L. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.05.047 · Cited by 178 · see citing works
Klin, A., Shultz, S., & JONES, W. R. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.10.006 · Cited by 184 · see citing works
“Clearly, tractable model systems are crucial to the study of autism, but creation of appropriate systems has, to date, been modest (Crawley, 2007).”
BackgroundArbogast, T., Ouagazzal, A.-M., Chevalier, C., Kopanitsa, M., Afinowi, N., Migliavacca, E., Cowling, B. S., Birling, M.-C., Champy, M.-F., Reymond, A., et al. (2016) · PLOS Genetics · doi:10.1371/journal.pgen.1005709 · Cited by 151 · see citing works
“Interestingly, Del/+mice also showed stereotypic behaviors (jumping and excessive climbing) commonly found in mouse models for autism [46].”
Bauman, M. D., Iosif, A.-M., Ashwood, P., Braunschweig, D., Lee, A., Schumann, C. M., Van de Water, J., & Amaral, D. G. (2013) · Translational Psychiatry · doi:10.1038/tp.2013.47 · Cited by 174 · see citing works
Genetic-background modulation of core and variable autistic-like symptoms in Fmr1 knock-out mice
Pietropaolo, S., Guilleminot, A., Martin, B., D'Amato, F. R., & Crusio, W. E. (2011) · PLoS ONE · doi:10.1371/journal.pone.0017073 · Cited by 178 · see citing works
“to the view that the ideal ASD model should reproduce all core symptoms and some secondary ones [23], the Fmr1-KO should”
BackgroundResultA Systematic Review of the Valproic-Acid-Induced Rodent Model of Autism
Chaliha, D. R., Albrecht, M. A., Vaccarezza, M., Takechi, R., Lam, V., Al‐Salami, H., & Mamo, J. C. L. (2020) · Developmental Neuroscience · doi:10.1159/000509109 · Cited by 173 · see citing works
SHANK3 controls maturation of social reward circuits in the VTA
Bariselli, S., Tzanoulinou, S., Glangetas, C., Prévost-Solié, C., Pucci, L., Viguié, J., Bezzi, P., O'Connor, E. C., Georges, F., Lüscher, C., et al. (2016) · Nature Neuroscience · doi:10.1038/nn.4319 · Cited by 168 · see citing works
Karlsson, R.-M., Tanaka, K., Saksida, L. M., Bussey, T. J., Heilig, M., & Holmes, A. (2009) · Neuropsychopharmacology · doi:10.1038/npp.2008.215 · Cited by 165 · see citing works
“A food burying test was conducted as a control test for potential deficits in general olfactory function that could potentially confound measurement of social behavior (Crawley, 2007).”
MethodSinger, H. S., Morris, C., Gause, C., Pollard, M., Zimmerman, A. W., & Pletnikov, M. (2009) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2009.03.011 · Cited by 164 · see citing works
“Left upper insert, Iba1 stained groups spent significantly more time on the side with stranger 1, as is normal (Crawley, 2007; Moy et al., 2007).”
BackgroundInfluentialBehavioral profiles of mouse models for autism spectrum disorders
Ey, E., Leblond, C. S., & Bourgeron, T. (2011) · Autism Research · doi:10.1002/aur.175 · Cited by 158 · see citing works
Autism-Relevant Social Abnormalities and Cognitive Deficits in Engrailed-2 Knockout Mice
Brielmaier, J. M., Matteson, P. G., Silverman, J. L., Senerth, J. M., Kelly, S., Genestine, M., Millonig, J. H., DiCicco-Bloom, E. M., & Crawley, J. N. (2012) · PLoS ONE · doi:10.1371/journal.pone.0040914 · Cited by 156 · see citing works
“Behavioral Tests Behavioral experiments were conducted between 10:00 and 16:00 in dedicated testing rooms, using methods previously described [52–55].”
MethodSelf-citationBehavioural Assays to Model Cognitive and Affective Dimensions of Depression and Anxiety in Rats
Lapiz‐Bluhm, M. D. S., Bondi, C. O., Doyen, J., Rodriguez, G. A., Bédard‐Arana, T., & Morilak, D. A. (2008) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2008.01772.x · Cited by 174 · see citing works
Animal Models of Serotonergic Psychedelics
Hanks, J. B., & González-Maeso, J. (2013) · ACS Chemical Neuroscience · doi:10.1021/cn300138m · Cited by 156 · see citing works
“(70) Crawley, J. N. (2007) Mouse behavioral assays relevant to the symptoms of autism.”
BackgroundOptogenetic insights on the relationship between anxiety-related behaviors and social deficits
Allsop, S. A., Vander Weele, C. M., Wichmann, R., & Tye, K. M. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00241 · Cited by 150 · see citing works
“Just as in anxiety, animal models have also been a useful tool for scientific inquiry into the brain regions, connections, and signaling involved in social function (Cacioppo, 2002; Insel and Fernald, 2004; Crawley, 2007; Adolphs, 2009; Silverman et al., 2010).”
MethodYaddanapudi, K., Hornig, M., Serge, R., Miranda, J. D., Baghban, A. A., Villar, G., & Lipkin, W. I. (2009) · Molecular Psychiatry · doi:10.1038/mp.2009.77 · Cited by 149 · see citing works
The Human Language–Associated Gene SRPX2 Regulates Synapse Formation and Vocalization in Mice
Sia, G.-M., Clem, R. L., & Huganir, R. L. (2013) · Science · doi:10.1126/science.1245079 · Cited by 147 · see citing works
Rodent tests of depression and anxiety: Construct validity and translational relevance
Gencturk, S., & Unal, G. (2024) · Cognitive, Affective, & Behavioral Neuroscience · doi:10.3758/s13415-024-01171-2 · Cited by 138 · see citing works
“Assessing social interaction levels in animals is widely used to study different psychological disorders, including autism spectrum disorders (Crawley, 2007), schizophrenia (Wilson & Koenig, 2014), and social anxiety disorder (social phobia) (Toth & Neumann, 2013).”
BackgroundKane, M. J., Angoa‐Pérez, M., Briggs, D. I., Sykes, C. E., Francescutti, D. M., Rosenberg, D. R., & Kuhn, D. M. (2012) · PLoS ONE · doi:10.1371/journal.pone.0048975 · Cited by 140 · see citing works
“Mouse genetic models of ASDs are contributing valuable mechanistic information on those factors that can alter susceptibility to this disorder [88,89,90].”
BackgroundChoi, J., Lee, S., Won, J., Jin, Y., Hong, Y., Hur, T.-Y., Kim, J.-H., Lee, S.-R., & Hong, Y. (2018) · PLOS ONE · doi:10.1371/journal.pone.0192925 · Cited by 139 · see citing works
Gould, G. G., Hensler, J. G., Burke, T. F., Benno, R. H., Onaivi, E. S., & Daws, L. C. (2010) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2010.07104.x · Cited by 138 · see citing works
Oxytocin receptor knockout mice display deficits in the expression of autism-related behaviors
Pobbe, R. L. H., Pearson, B. L., Defensor, E. B., Bolivar, V. J., Young, W. S., Lee, H., Blanchard, D. C., & Blanchard, R. J. (2011) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.10.010 · Cited by 139 · see citing works
“Recently, much effort has gone into modeling the behavioral symptoms of ASD in mice aiming to further understand the underlying genetic mechanisms (Crawley, 2007; Silverman et al., 2010).”
BackgroundAltered auditory processing in a mouse model of fragile X syndrome
Rotschafer, S. E., & Razak, K. A. (2013) · Brain Research · doi:10.1016/j.brainres.2013.02.038 · Cited by 138 · see citing works
“There is also evidence that Fmr1 KO mice show social deficits when interacting with other mice, and engage in repetitive behaviors (Mineur et al., 2002; Spencer et al., 2005; Crawley, 2007) and show abnormal social vocalizations (Rotschafer et al., 2012).”
BackgroundEcological validity of social interaction tests in rats and mice
Kondrakiewicz, K., Kostecki, M., Szadzińska, W., & Knapska, E. (2019) · Genes, Brain and Behavior · doi:10.1111/gbb.12525 · Cited by 136 · see citing works
“simple behavioral measures, for example, time spent on exploring a social stimulus.(3) The attractiveness of this approach lies in a high level”
BackgroundMethodDefensor, E. B., Pearson, B. L., Pobbe, R. L. H., Bolivar, V. J., Blanchard, D. C., & Blanchard, R. J. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.10.033 · Cited by 136 · see citing works
“A combination of social interaction tests have been used to identify low social responsiveness in inbred candidate strains [4],[11],[12],[18],[19], [20],[41],[45],[46],[48],[54],[70].”
MethodEllegood, J., Babineau, B. A., Henkelman, R. M., Lerch, J. P., & Crawley, J. N. (2013) · NeuroImage · doi:10.1016/j.neuroimage.2012.12.029 · Cited by 135 · see citing works
“1A) using methods previously described (Chadman et al., 2008; Crawley, 2007; McFarlane et al., 2008; Moy et al., 2008; Silverman et al., 2010a, 2010b, 2011; Yang et al., 2009, 2011a, 2011b).”
MethodSelf-citationKlocke, C. R., & Lein, P. J. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21031013 · Cited by 135 · see citing works
Development and function of the midbrain dopamine system: what we know and what we need to
Bissonette, G. B., & Roesch, M. R. (2015) · Genes Brain & Behavior · doi:10.1111/gbb.12257 · Cited by 135 · see citing works
“Association work has linked Engrailed 2 (located at chromosome 7q36) with ASD (Gharani et al. 2004) in humans.”
ResultInfluentialKas, M. J., Glennon, J. C., Buitelaar, J., Ey, E., Biemans, B., Crawley, J., Ring, R. H., Lajonchere, C., Esclassan, F., Talpos, J., et al. (2014) · Psychopharmacology · doi:10.1007/s00213-013-3268-5 · Cited by 132 · see citing works
“Olfactory signals are also very ethologically relevant proxies for communicative abilities in rodent models of ASD (Crawley 2007).”
BackgroundSelf-citationSilverman, J. L., Thurm, A. E., Ethridge, S. B., Soller, M. M., Petkova, S. P., Abel, T. G., Bauman, M. D., Brodkin, E. S., Harony‐Nicolas, H., Wöhr, M., et al. (2022) · Genes Brain & Behavior · doi:10.1111/gbb.12803 · Cited by 127 · see citing works
Emotional contagion and prosocial behavior in rodents
Keysers, C., Knapska, E., Moita, M. A. P., & Gazzola, V. (2022) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2022.05.005 · Cited by 123 · see citing works
“[165,172] that lead to considerable strain differences in fear contagion [146].”
Autistic-Like Syndrome in Mu Opioid Receptor Null Mice is Relieved by Facilitated mGluR4 Activity
Becker, J. A. J., Clesse, D., Spiegelhalter, C., Schwab, Y., Merrer, J. L., & Kieffer, B. L. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2014.59 · Cited by 123 · see citing works
“…high homology between mouse and human genomes and feasibility of genetic modifications in mice, interest in developing genetic mouse models of ASDs has raised recently, together with the development of dedicated behavioral assessment (Buxbaum et al, 2012; Crawley, 2007; Robertson and Feng, 2011).”
BackgroundHiramoto, T., Kang, G., Suzuki, G., Satoh, Y., Kucherlapati, R., Watanabe, Y., & Hiroi, N. (2011) · Human Molecular Genetics · doi:10.1093/hmg/ddr404 · Cited by 126 · see citing works
“Although any attempt to model ASD in animals is at best a proxy for the real events, a number of behavioral paradigms to model symptomatic elements have validity (27).”
BackgroundCreatine Transporter (CrT; Slc6a8) Knockout Mice as a Model of Human CrT Deficiency
Skelton, M. R., Schaefer, T. L., Graham, D. L., deGrauw, T. J., Clark, J. F., Williams, M. T., & Vorhees, C. V. (2011) · PLoS ONE · doi:10.1371/journal.pone.0016187 · Cited by 120 · see citing works
“[30].”
Deletion of Glutamate Delta-1 Receptor in Mouse Leads to Aberrant Emotional and Social Behaviors
Yadav, R., Gupta, S. C., Hillman, B. G., Bhatt, J. M., Stairs, D. J., & Dravid, S. M. (2012) · PLoS ONE · doi:10.1371/journal.pone.0032969 · Cited by 123 · see citing works
Criteria for validating mouse models of psychiatric diseases
Chadman, K. K., Yang, M., & Crawley, J. N. (2008) · American Journal of Medical Genetics Part B Neuropsychiatric Genetics · doi:10.1002/ajmg.b.30777 · Cited by 123 · see citing works
“Behavioral Phenotyping of Transgenic and Knockout Mice’’ [Crawley, 2007b], Current Protocols in Neuroscience, and in the many excellent review articles cited above.”
BackgroundSelf-citationPobbe, R. L. H., Pearson, B. L., Defensor, E. B., Bolivar, V. J., Blanchard, D. C., & Blanchard, R. J. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.06.025 · Cited by 121 · see citing works
“Therefore, suitable animal models for ASD require a relationship to the types of social deficits that are considered the core symptoms of such disorder, including impairments in social interaction and deficiencies in other functional domains [12,31,33].”
BackgroundMice with reduced NMDA receptor expression: more consistent with autism than schizophrenia?
Gandal, M. J., Anderson, R. L., Billingslea, E. N., Carlson, G. C., Roberts, T. P. L., & Siegel, S. J. (2012) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2012.00816.x · Cited by 120 · see citing works
“744 Genes, Brain and Behavior (2012) 11: 740–750 As such, adult NR1neo−/− mice show strong face validity for autism-like phenotypes (Crawley, 2007).”
BackgroundAutomated test of behavioral flexibility in mice using a behavioral sequencing task in IntelliCage
Endo, T., Maekawa, F., Võikar, V., Haijima, A., Uemura, Y., Zhang, Y., Miyazaki, W., Suyama, S., Shimazaki, K., Wolfer, D. P., et al. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.02.037 · Cited by 117 · see citing works
Monoamine oxidase A and A/B knockout mice display autistic-like features
Bortolato, M., Godar, S. C., Alzghoul, L., Zhang, J., Darling, R. D., Simpson, K. L., Bini, V., Chen, K., Wellman, C. L., Lin, R. C. S., et al. (2012) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145712000715 · Cited by 118 · see citing works
“In the beam-walking assay (Crawley, 2007), both genotypes exhibited a typical crawling posture (Salichon et al.”
General and social anxiety in the BTBR T+ tf/J mouse strain
Pobbe, R. L. H., Defensor, E. B., Pearson, B. L., Bolivar, V. J., Blanchard, D. C., & Blanchard, R. J. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.08.039 · Cited by 115 · see citing works
“Therefore, suitable animal models for ASD require a relationship to the types of behavioral deficits that are considered the core symptoms of such disorder, including impairments in social interaction and deficiencies in other functional domains [14,40,55].”
BackgroundRETRACTED: Enhanced Polyubiquitination of Shank3 and NMDA Receptor in a Mouse Model of Autism
Bangash, M. A., Park, J. M., Melnikova, T., Wang, D., Jeon, S. K., Lee, D., Syeda, S. K., Kim, J., Kouser, M., Schwartz, J. L., et al. (2011) · Cell · doi:10.1016/j.cell.2011.03.052 · Cited by 115 · see citing works
RetractedArakawa, H., Arakawa, K., & Terrence Deak, B. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.10.013 · Cited by 114 · see citing works
Hou, Q.-L., Wang, Y., Li, Y., Chen, D., Yang, F., & Wang, S. (2018) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2018.00182 · Cited by 113 · see citing works
“Autistic individuals often maintain rigid habits and frequently show a strong insistence on sameness and become distraught by a change in routine (Crawley, 2007).”
BackgroundGenetic manipulation of STEP reverses behavioral abnormalities in a fragile X syndrome mouse model
Goebel‐Goody, S. M., Wilson‐Wallis, E. D., Royston, S., Tagliatela, S. M., Naegele, J. R., & Lombroso, P. J. (2012) · Genes, Brain and Behavior · doi:10.1111/j.1601-183x.2012.00781.x · Cited by 108 · see citing works
“We evaluated sociability using a three-chambered social choice task (Crawley 2007; Moy et al. 2009).”
MethodLe Belle, J. E., Sperry, J., Ngo, A., Ghochani, Y., Laks, D. R., López-Aranda, M., Silva, A. J., & Kornblum, H. I. (2014) · Stem Cell Reports · doi:10.1016/j.stemcr.2014.09.004 · Cited by 105 · see citing works
“Ultrasonic vocalization, three-chamber social interaction, and elevated plus maze tests were performed on adult mice according to the methods of Crawley (2007).”
MethodRicceri, L., Filippis, B. D., & Giovanni Laviola, A. (2008) · Behavioural Pharmacology · doi:10.1097/fbp.0b013e32830c3645 · Cited by 103 · see citing works
“In addition, a robust rodent model can have translational value in offering preclinical surrogate markers to evaluate treatment efficacy (Crawley, 2007).”
BackgroundAuditory Processing in Fragile X Syndrome
Rotschafer, S. E., & Razak, K. A. (2014) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00019 · Cited by 102 · see citing works
“Repetitive behaviors have been demonstrated in Fmr1 KO mice using marble burying tasks (Crawley, 2004, 2007).”
MethodGlutamate receptor dysfunction and drug targets across models of autism spectrum disorders
Carlson, G. C. (2012) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2011.02.003 · Cited by 102 · see citing works
“…of ASD is determined from the presence of core deficits in 1) communication, 2) social, and 3) repetitive behavior; with changes in social behavior and inappropriate repetitive activity being the most easily measured in rodent models {Korff, 2006 #2312; Crawley, 2007 #2314; Lewis, 2007 #2315}.”
BackgroundHumann, J., Mann, B., Gao, G., Moresco, P., Ramahi, J., Loh, L. N., Farr, A., Hu, Y., Durick-Eder, K., Fillon, S. A., et al. (2016) · Cell Host & Microbe · doi:10.1016/j.chom.2016.02.009 · Cited by 100 · see citing works
“Behavioral testing Working memory of WT CW treated mice was tested as previously described using three assays (Bevins and Besheer, 2006; Crawley, 2007): novel object recognition, spatial recognition and delayed non-matched to position tests.”
Abnormal Cerebellar Development in Autism Spectrum Disorders
van der Heijden, M. E., Gill, J. S., & Sillitoe, R. V. (2021) · Developmental Neuroscience · doi:10.1159/000515189 · Cited by 98 · see citing works
Mecp2 organizes juvenile social behavior in a sex-specific manner
Kurian, J. R., Bychowski, M. E., Forbes-Lorman, R. M., Auger, C. J., & Auger, A. P. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.1345-08.2008 · Cited by 100 · see citing works
“Sociability was measured with an adaptation of the social approach task (Crawley, 2004, 2007).”
MethodCastro, K., Baronio, D., Perry, I. D. S., Riesgo, R. D. S., & Gottfried, C. (2016) · Nutritional Neuroscience · doi:10.1080/1028415x.2015.1133029 · Cited by 98 · see citing works
Mouse models of frontotemporal dementia
Roberson, E. D. (2012) · Annals of Neurology · doi:10.1002/ana.23722 · Cited by 97 · see citing works
“Work on autism, which bears some similarities to FTD in its social and behavioral features, has demonstrated the utility of mouse models for studying disorders with these features.(110) Here we highlight a few behavioral domains that have not only a high degree of similarity with the symptoms of FTD, but also a common…”
BackgroundMaternal immune activation promotes hippocampal kindling epileptogenesis in mice
Pineda, E., Shin, D. H., You, S. J., Auvin, S., Sankar, R., & Mazarati, A. M. (2013) · Annals of Neurology · doi:10.1002/ana.23898 · Cited by 98 · see citing works
“At postnatal day 40 (P40), sociability was examined as described.(21,22) The apparatus (Noldus, Leesburg, VA) was a 60 3 40cm Plexiglas box divided into 3 connected chambers.”
MethodSocial dysfunction after pediatric traumatic brain injury: A translational perspective
Ryan, N. P., Catroppa, C., Godfrey, C., Noble‐Haeusslein, L. J., Shultz, S. R., O'Brien, T. J., Anderson, V. A., & Semple, B. D. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.02.020 · Cited by 95 · see citing works
“…social behaviors, and several etiologically-relevant assays with good face validity (i.e. resemblance to the human phenomenology) have been developed to measure different aspects of social behavior in mice (Crawley, 2007; Silverman et al., 2010; Terranova and Laviola, 2005) (see Figure 3).”
BackgroundFound in translation: Understanding the biology and behavior of experimental traumatic brain injury
Bondi, C. O., Semple, B. D., Noble‐Haeusslein, L. J., Osier, N. D., Carlson, S. W., Dixon, C. E., Giza, C. C., & Kline, A. E. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.12.004 · Cited by 91 · see citing works
Autism Spectrum Disorders: Translating human deficits into mouse behavior
Pasciuto, E., Borrie, S. C., Kanellopoulos, A. K., Santos, A. R. S., Cappuyns, E., D’Andrea, L., Pacini, L., & Bagni, C. (2015) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2015.07.013 · Cited by 92 · see citing works
Deficits in Social Behavior Emerge during Development after Pediatric Traumatic Brain Injury in Mice
Semple, B. D., Canchola, S. A., & Noble‐Haeusslein, L. J. (2012) · Journal of Neurotrauma · doi:10.1089/neu.2012.2595 · Cited by 92 · see citing works
“quite sensitive to numerous known and unknown factors, including housing and experimental conditions, handling, previous life experiences, and social isolation.(38,41,53) As such, the evaluation of social parameters in experimental TBI studies requires”
Segal‐Gavish, H., Karvat, G., Barak, N., Barzilay, R., Ganz, J., Edry, L., Aharony, I., Offen, D., & Kimchi, T. (2015) · Autism Research · doi:10.1002/aur.1530 · Cited by 93 · see citing works
“, & Crawley, J.N. (2011). Reduced scent marking and ultrasonic vocalizations in the BTBR t1tf/J mouse model of autism. Genes, Brain and Behavior, 10, 35– 43. doi:10.1111/j.1601-183X.2010.00582.x W€ ohr, M., & Scattoni, M. L. (2013). Behavioural methods used in rodent models of autism spectrum disorders: Current standa…”
BackgroundMethodInfluentialAutism spectrum and obsessive–compulsive disorders: OC behaviors, phenotypes and genetics
Jacob, S., Landeros‐Weisenberger, A., & Leckman, J. F. (2009) · Autism Research · doi:10.1002/aur.108 · Cited by 91 · see citing works
“Behavioral genetic approaches related to ASD have examined manipulations on a range of candidate genes [Moy & Nadler, 2008] and have methods to study ‘‘IS’’ or change in habit through reversal learning tasks [Crawley, 2007].”
MethodGut microbiota regulates key modulators of social behavior
Parashar, A., & Udayabanu, M. (2016) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2015.11.002 · Cited by 88 · see citing works
“Now, keeping in view these somewhat contradicting results and the behavioral deficits that are the hallmarks of various neurodevelopmental disorders (Crawley, 2007), emergence of GM has opened new doors for identifying new underlying mechanisms that could potentially lead to novel and more effective therapies to comba…”
ResultRyan, B. C., Young, N. B., Moy, S. S., & Crawley, J. N. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.06.002 · Cited by 95 · see citing works
“The STFP task has also been identified as an assay with potential face validity to the symptoms of autism [16,39].”
BackgroundSelf-citationDoll, C. A., & Broadie, K. S. (2014) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00030 · Cited by 81 · see citing works
“Nevertheless, ASD modeling is made difficult by the underlying genetic diversity, and this difficulty is compounded by the array of symptoms described in human conditions and debates about appropriate genetic models (Crawley, 2007).”
BackgroundBraun, A. E., Carpentier, P. A., Babineau, B. A., Narayan, A. R., Kielhold, M. L., Moon, H. M., Shankar, A., Su, J., Saravanapandian, V., Haditsch, U., et al. (2019) · eNeuro · doi:10.1523/eneuro.0358-19.2019 · Cited by 85 · see citing works
“Sociability and social memory were tested in an adaptation of the three-chamber test (Crawley, 2007).”
Method
- Authors
- Crawley, J. N.
- Affiliations
- University of North Carolina at Chapel Hill (US)
- Corresponding author
- Crawley, Jacqueline N.
- Venue
- Brain Pathology
- Publisher
- Wiley
- Published
- 2007-10
- Volume
- 17
- Issue
- 4
- Pages
- 448-459
- ISSN
- 1015-6305 (ISSN-L)
- 1750-3639
- PMC
- PMC8095652
- OpenAlex
- W2076566560
- Cited by
- 541
- References
- 216
- Citations by year
- 2026: 10 · 2025: 18 · 2024: 18 · 2023: 24 · 2022: 25 · 2021: 31 · 2020: 33 · 2019: 34 · 2018: 21 · 2017: 28 · 2016: 30 · 2015: 38 · 2014: 30 · 2013: 41 · 2012: 42
- FWCI
- 1.68
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Brain Pathology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5u54mh066418-05)
- U.S. Public Health Service (NICHD P30)
- National Institute of Mental Health (U54-MH066418, MH66418)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Autism Spectrum Disorder Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Keywords
- autism spectrum disorder, mouse models of autism, behavioral assays, social interaction, communication difficulties, repetitive behavior, insistence on sameness, reciprocal social interaction, vocalizations, olfactory cues, grooming, anxiety, seizures, sleep disorders, sensory hypersensitivity, phenotyping, inbred mouse strains, environmental toxins
- MeSH terms
- Animals, Autistic Disorder, Behavior, Animal, Biological Assay, Disease Models, Animal, Humans, Mice, Transgenic, Phenotype, Social Behavior Disorders, Genetic Predisposition to Disease, Mice
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