Cited by 541Autism Spectrum Disorder ResearchGenetics and Neurodevelopmental DisordersNeuroendocrine regulation and behavior

The DOI matches its Crossref record; 214 of the 216 references it cites were found in a registry or an index.

Mouse Behavioral Assays Relevant to the Symptoms of Autism*

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Crawley, Jacqueline N.·2007·Brain Pathology

DOI 10.1111/j.1750-3639.2007.00096.xPMC PMC8095652

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Abstract

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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Background
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BackgroundMethodResultInfluentialSelf-citation
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10.1002/1096-8628(20010108)105:1<53::AID-AJMG1059>3.0.CO;2-U · DOI

Sorted by citations

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“The effects of subchronic PCP treatment on social behavior were assessed based on methods previously described to test for autism- and schizophrenia-related phenotypes in mice (Crawley, 2007; McFarlane et al., 2008).”
Method
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“In this paradigm, test mice are placed in a three-chambered arena, in one chamber, a “stranger” mouse is placed under a wire cup, and in the opposite chamber there is an empty wire container (Crawley 2007; Moy et al. 2004).”
Method
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Homberg, J. R., Kyzar, E. J., Nguyen, M., Norton, W., Pittman, J. T., Poudel, M. K., Gaikwad, S., Nakamura, S., Koshiba, M., Yamanouchi, H., et al. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.03.013 · Cited by 86
“…deficits are a common symptom of ASD and many other NDDs. Popular rodent behavioral assays designed to target social behaviors characterize social interaction and communication deficits (Bishop and Lahvis, 2011; Crawley, 2004, 2007; Hunsaker, 2012; Lahvis and Black, 2011; Silverman et al., 2010b).”
Background
Early Postnatal Exposure to Airborne Fine Particulate Matter Induces Autism-like Phenotypes in Male Rats
Li, K., Li, L., Cui, B., Gai, Z., Li, Q., Wang, S., Yan, J., Lin, B., Tian, L., Liu, H., et al. (2017) · Toxicological Sciences · doi:10.1093/toxsci/kfx240 · Cited by 82
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“The chamber was cleaned using ethanol between each trial [41].”
Method
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Boxer, A. L., Gold, M., Huey, E. D., Gao, F., Burton, E. A., Chow, T. W., Kao, A. W., Leavitt, B. R., Lamb, B. T., Grether, M. E., et al. (2012) · Alzheimer s & Dementia · doi:10.1016/j.jalz.2012.03.002 · Cited by 84
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C57BL/6J mice fail to exhibit preference for social novelty in the three-chamber apparatus
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“These tests are therefore recognized as ASD phenotype tasks (Crawley 2007; Moy et al. 2007).”
Background
How Many Ways Can Mouse Behavioral Experiments Go Wrong? Confounding Variables in Mouse Models of Neurodegenerative Diseases and How to Control Them
Schellinck, H. M., Cyr, D. P., & Brown, R. E. (2010) · Advances in the study of behavior · doi:10.1016/s0065-3454(10)41007-4 · Cited by 80
The promise and the pitfalls of autism research: An introductory note for new autism researchers
Amaral, D. G. (2010) · Brain Research · doi:10.1016/j.brainres.2010.11.077 · Cited by 77
“And, Crawley has written extensively on this topic [14,15,37].”
Background
Interaction between environmental and genetic factors modulates schizophrenic endophenotypes in the Snap-25 mouse mutant blind-drunk
Oliver, P. L., & Davies, K. E. (2009) · Human Molecular Genetics · doi:10.1093/hmg/ddp425 · Cited by 78
“The sociability paradigm used here was originally developed to model autistic-like behaviour, although social communication problems are common in many neuropsychiatric disorders including schizophrenia (68,69).”
Method
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“In the Crawley’s social approach test (Moy et al, 2004; Crawley, 2007), all mice showed similar sociability, but YAC128 mice spent more time with a familiar mouse rather than a new mouse (Fig 7A, preference for social novelty), a behaviour that is also observed in AD mouse models (Faizi et al,…”
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“…derived from a bioinformatics research suggested four critical brain regions related to ASD pathogenesis: the olfactory bulb (involved in both olfactory signal transmission and social behavior, at least in mouse models; Crawley, 2007), the occipital lobe, the prefrontal cortex and the pituitary.”
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Synaptic P-Rex1 signaling regulates hippocampal long-term depression and autism-like social behavior
Li, J., Chai, A., Wang, L., Ma, Y., Wu, Z., Yu, H., Mei, L., Lu, L., Zhang, C., Yue, W., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1512913112 · Cited by 75
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Background
Dysfunctional dopaminergic neurotransmission in asocial BTBR mice
Squillace, M., Dodero, L., Federici, M., Migliarini, S., Errico, F., Napolitano, F., Krashia, P., Maio, A. D., Galbusera, A., Bifone, A., et al. (2014) · Translational Psychiatry · doi:10.1038/tp.2014.69 · Cited by 73
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“The changes in social behavior observed in the present study are similar to changes observed in some of the animal models of autism (Crawley, 2007; Presti-Torres et al., 2007;Harmonet al., 2008, 2009).”
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“Social interaction behaviour of rats was tested according to Crawley's methods (Crawley, 2007).”
RFID-supported video tracking for automated analysis of social behaviour in groups of mice
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Benno, R. H., Smirnova, Y., Vera, S., Liggett, A., & Schanz, N. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.09.041 · Cited by 69
Zinc as a therapy in a rat model of autism prenatally induced by valproic acid
Cezar, L. C., Kirsten, T. B., da Fonseca, C. C. N., Lima, A. P., Bernardi, M. M., & Felício, L. F. (2018) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2018.02.008 · Cited by 69
“Animals that insist on visiting the same spatial location in one of the arms of the T-maze are considered an “autistic type” (Crawley, 2007; MacFabe et al., 2011).”
Background
Rapamycin improves sociability in the BTBR T+Itpr3/J mouse model of autism spectrum disorders
Burket, J. A., Benson, A. D., Tang, A., & Deutsch, S. I. (2013) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2013.11.005 · Cited by 66
“Sociability procedure The laboratory adopted an established mouse behavioral procedure for the quantitative assessment of sociability (Brodkin, 2007; Burket et al., 2013, 2010; Crawley, 2007, 2004; Deutsch et al., 2012, 2011; Jacome et al., 2011a; Sankoorikal et al., 2006).”
Method
Outbred CD1 mice are as suitable as inbred C57BL/6J mice in performing social tasks
Hsieh, L. S., Wen, J. H., Miyares, L. C., Lombroso, P. J., & Bordey, A. (2016) · Neuroscience Letters · doi:10.1016/j.neulet.2016.11.035 · Cited by 64
“To assess sociability without the confound from aggressive behaviors in CD1 mice, we used the three-chamber sociability task, which is now broadly used for testing mouse sociability [9;10].”
BackgroundMethod
Improvement in motor and exploratory behavior in Rett syndrome mice with restricted ketogenic and standard diets
Mantis, J. G., Fritz, C. L., Marsh, J., Heinrichs, S. C., & Seyfried, T. N. (2009) · Epilepsy & Behavior · doi:10.1016/j.yebeh.2009.02.038 · Cited by 66
“The rotarod test examined defects in mouse motor neurodevelopment related to coordination and balance [60].”
Method
Increased oxidative stress in the cerebellum and peripheral immune cells leads to exaggerated autism-like repetitive behavior due to deficiency of antioxidant response in BTBR T + tf/J mice
Nadeem, A., Ahmad, S. F., Al-Harbi, N. O., Attia, S. M., Alshammari, M. A., Alzahrani, K. S., & Bakheet, S. A. (2018) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2018.09.012 · Cited by 65
“These mice have communication or social interaction deficits similar to human subjects with autism (Meyza et al., 2013; McFarlane et al., 2008; Crawley, 2007).”
Complex effects of mGluR5 antagonism on sociability and stereotypic behaviors in mice: Possible implications for the pharmacotherapy of autism spectrum disorders
Burket, J. A., Herndon, A. L., Winebarger, E. E., Jacome, L. F., & Deutsch, S. I. (2011) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2011.08.001 · Cited by 65
Mouse Models of Autism: Testing Hypotheses About Molecular Mechanisms
Roullet, F., & Crawley, J. N. (2011) · Current topics in behavioral neurosciences · doi:10.1007/7854_2010_113 · Cited by 67
“The fundamental challenge is to design mouse behavioral tasks with sufficient face validity to the core symptoms within each of the three diagnostic behavioral categories of autism (Crawley 2004, 2007a, b).”
BackgroundSelf-citation
Sexually dimorphic vasopressin cells modulate social investigation and communication in sex-specific ways
Rigney, N., Whylings, J., Mieda, M., de Vries, G. J., & Petrulis, A. (2019) · eNeuro · doi:10.1523/eneuro.0415-18.2019 · Cited by 63
“USV, UM, and social investigation were recorded in an acrylic three-chamber apparatus (Crawley, 2007; Arakawa et al., 2008a; Moy et al., 2009; Harvard Apparatus; dimensions: 20.3 42 22 cm).”
MethodInfluential
Behavioral abnormalities in the Fmr1‐KO2 mouse model of fragile X syndrome: The relevance of early life phases
Gaudissard, J., Ginger, M. R., Premoli, M., Memo, M., Frick, A., & Pietropaolo, S. (2017) · Autism Research · doi:10.1002/aur.1814 · Cited by 64
“Behavior of mice at this age can be investigated through the analysis of ultrasonic vocalizations emitted upon short isolation periods and of social recognition in the homing test [Ricceri, Moles, & Crawley, 2007; Scattoni, Crawley, & Ricceri, 2009].”
Background
Cognitive and social functions and growth factors in a mouse model of Rett syndrome
Schaevitz, L. R., Moriuchi, J. M., Nag, N., Mellott, T. J., & Berger-Sweeney, J. E. (2010) · Physiology & Behavior · doi:10.1016/j.physbeh.2009.12.025 · Cited by 65
Monogenic mouse models of social dysfunction: Implications for autism
Oddi, D., Crusio, W. E., D'Amato, F. R., & Pietropaolo, S. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.01.002 · Cited by 66
Essential role of GluD1 in dendritic spine development and GluN2B to GluN2A NMDAR subunit switch in the cortex and hippocampus reveals ability of GluN2B inhibition in correcting hyperconnectivity
Gupta, S. C., Yadav, R., Pavuluri, R., Morley, B. J., Stairs, D. J., & Dravid, S. M. (2015) · Neuropharmacology · doi:10.1016/j.neuropharm.2015.02.013 · Cited by 70
“We used the hole-board test which measures repetitive or stereotyped behavior which is one of the core features of the neurodevelopmental disorders such as autism (Crawley, 2007).”
The Roles of Oxytocin and CD38 in Social or Parental Behaviors
Lopatina, O. L., Ивановна, И. А., Salmina, A. B., & Higashida, H. (2013) · Frontiers in Neuroscience · doi:10.3389/fnins.2012.00182 · Cited by 66
“…a number of relevant www.frontiersin.org January 2013 | Volume 6 | Article 182 | 5 behavioral and social changes have been documented in transgenic mouse models of neurodevelopmental disorders (Branchi et al., 2001; Brooks et al., 2005; Crawley, 2007; Moy et al., 2007, 2008; Wöhr et al., 2011).”
Background
Early and adult hippocampal TGF-β1 overexpression have opposite effects on behavior
Depino, A. M., Lucchina, L., & Pitossi, F. J. (2011) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2011.05.007 · Cited by 63
“Therefore, we specifically focused on two murine behaviors linked to the major symptoms of ASD (American Psychiatric Association, 2000): social interaction and self-grooming (Crawley, 2007).”
Background
PKBγ/AKT3 loss-of-function causes learning and memory deficits and deregulation of AKT/mTORC2 signaling: Relevance for schizophrenia
Howell, K. R., Floyd, K., & Law, A. J. (2017) · PLoS ONE · doi:10.1371/journal.pone.0175993 · Cited by 67
Prenatal immune challenge in rats: altered responses to dopaminergic and glutamatergic agents, prepulse inhibition of acoustic startle, and reduced route-based learning as a function of maternal body weight gain after prenatal exposure to poly IC
Vorhees, C. V., Graham, D. L., Braun, A. A., Schaefer, T. L., Skelton, M. R., Richtand, N. M., & Williams, M. T. (2012) · Synapse · doi:10.1002/syn.21561 · Cited by 62
Oxytocin Receptors Regulate Social Preference in Zebrafish
Landin, J., Hovey, D., Xu, B., Lagman, D., Zettergren, A., Larhammar, D., Kettunen, P., & Westberg, L. (2020) · Scientific Reports · doi:10.1038/s41598-020-61073-4 · Cited by 65
Mouse Model of Chromosome 15q13.3 Microdeletion Syndrome Demonstrates Features Related to Autism Spectrum Disorder
Kogan, J. H., Gross, A. K., Featherstone, R. E., Shin, R., Chen, Q., Heusner, C. L., Adachi, M., Lin, A., Walton, N. M., Miyoshi, S., et al. (2015) · The Journal of Neuroscience · doi:10.1523/jneurosci.3967-14.2015 · Cited by 59
“The deficits in reciprocal social interaction reported here in D/ mice were assessed by both a free social interaction task in the subject’s home cage with a novel partner mouse and by a three-chamber sociability test (Crawley, 2007).”
MethodInfluential
Lasting adaptations in social behavior produced by social disruption and inhibition of adult neurogenesis
Opendak, M., Offit, L., Monari, P., Schoenfeld, T. J., Sonti, A. N., Cameron, H. A., & Gould, E. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.4435-15.2016 · Cited by 61
“Social recognition and novelty preference were tested using an apparatus based on previous social behavior studies done in mice, with dimensions scaled up to accommodate rats (Engelmann et al., 1995; Moy et al., 2004; Crawley, 2007; Eagle et al., 2013).”
Method
KDM5A mutations identified in autism spectrum disorder using forward genetics
Hayek, L. E., Tuncay, İ. O., Nijem, N., Russell, J. L., Ludwig, S. M., Kaur, K. J., Li, X., Anderton, P. D., Tang, M., Gerard, A., et al. (2020) · eLife · doi:10.7554/elife.56883 · Cited by 60
Chronic unpredictable stress negatively regulates hippocampal neurogenesis and promote anxious depression-like behavior via upregulating apoptosis and inflammatory signals in adult rats
Parul, P., Mishra, A., Singh, S., Singh, S., Tiwari, V., Chaturvedi, S., Wahajuddin, M., Palit, G., & Shukla, S. (2021) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2021.04.017 · Cited by 64
A novel system for tracking social preference dynamics in mice reveals sex- and strain-specific characteristics
Netser, S., Haskal, S., Magalnik, H., & Wagner, S. (2017) · Molecular Autism · doi:10.1186/s13229-017-0169-1 · Cited by 65
“A main goal of social neuroscience, one of the most rapidly developing fields in neuroscience, is to reveal and characterize the biological mechanisms underlying deficits in social behavior displayed by humans in pathological conditions such as ASD [1].”
MethodInfluential
Distinct Phenotypes of Shank2 Mouse Models Reflect Neuropsychiatric Spectrum Disorders of Human Patients With SHANK2 Variants
Eltokhi, A., Rappold, G., & Sprengel, R. (2018) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2018.00240 · Cited by 63
“As suggested (Crawley, 2007; Tordjman et al., 2007), a consistent ‘‘multi-trait’’ analysis of cognitive and social behavior is necessary for the dissection of the clinically heterogeneous ASD spectrum in the different mouse models.”
BackgroundInfluential
What we can learn from a genetic rodent model about autism
Möhrle, D., Fernández, M. C., Peñagarikano, O., Frick, A., Allman, B. L., & Schmid, S. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.12.015 · Cited by 60
Loss of Cntnap2 in the Rat Causes Autism‐Related Alterations in Social Interactions, Stereotypic Behavior, and Sensory Processing
Scott, K. E., Kazazian, K., Mann, R. S., Möhrle, D., Schormans, A. L., Schmid, S., & Allman, B. L. (2020) · Autism Research · doi:10.1002/aur.2364 · Cited by 62
“Each rat’s preference for a conspecific over an inanimate object (sociability), as well as its preference for a stranger rat over a familiar rat (social novelty) was assessed using previously established 3-chamber assays [Crawley, 2007; Moy et al., 2004].”
Method
Reversible Behavioral Phenotypes in a Conditional Mouse Model of TDP-43 Proteinopathies
Alfieri, J. A., Pino, N. S., & Igaz, L. M. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.1918-14.2014 · Cited by 60
“For example, social dysfunction is an aspect of FTD that can be examined in mice and social tests have proven to be useful in disorders with prominent social deficits such as autism (Crawley, 2007).”
Background
Mice lacking Asic3 show reduced anxiety‐like behavior on the elevated plus maze and reduced aggression
Wu, W. ‐., Lin, Y., Min, M., & Chen, C. (2010) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2010.00591.x · Cited by 61
“These stereotypic repetitive behaviors were not found in Asic3+/+ mice, which suggests that the Asic3−/− mice show some indications of behavioral alterations commonly associated with neuropsychiatric disorders (Boria et al. 2009; Crawley 2007).”
Background
Enriched rearing improves behavioral responses of an animal model for CNV-based autistic-like traits
Lacaria, M., Spencer, C. M., Gu, W., Paylor, R. E., & Lupski, J. R. (2012) · Human Molecular Genetics · doi:10.1093/hmg/dds124 · Cited by 60
Malformation of the superior olivary complex in an animal model of autism
Lukose, R., Schmidt, E., Wolski, T. P., Murawski, N. J., & Kulesza, R. J. (2011) · Brain Research · doi:10.1016/j.brainres.2011.05.013 · Cited by 59
Perinatal exposure to concentrated ambient particulates results in autism-like behavioral deficits in adult mice
Church, J. S., Tijerina, P. B., Emerson, F. J., Coburn, M. A., Blum, J. L., Zelikoff, J. T., & Schwartzer, J. J. (2018) · NeuroToxicology · doi:10.1016/j.neuro.2017.10.007 · Cited by 59
Transient blockade of ERK phosphorylation in the critical period causes autistic phenotypes as an adult in mice
Yufune, S., Satoh, Y., Takamatsu, I., Ohta, H., Kobayashi, Y., Takaenoki, Y., Pagès, G., Pouysségur, J., Endo, S., & Kazama, T. (2015) · Scientific Reports · doi:10.1038/srep10252 · Cited by 57
Loss of MeCP2 in the rat models regression, impaired sociability and transcriptional deficits of Rett syndrome
Veeraragavan, S., Wan, Y.-W., Connolly, D. R., Hamilton, S. M., Ward, C. S., Soriano, S., Pitcher, M. R., McGraw, C. M., Huang, S. G., Green, J. R., et al. (2016) · Human Molecular Genetics · doi:10.1093/hmg/ddw178 · Cited by 59
“As genetic tools in the mouse evolved, assays used for behaviour in the rat were adapted, developed and improved for comparable studies in the mouse (46,47).”
Method
Altered anxiety-related and abnormal social behaviors in rats exposed to early life seizures
Castelhano, A. S. S., Cassane, G. D. S. T., Scorza, F. A., & Cysneiros, R. M. (2013) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2013.00036 · Cited by 58
“The social behavior apparatus was adapted by Novaes et al. (2012) from Crawley (2007).”
Current perspectives in autism spectrum disorder: from genes to therapy
Chahrour, M., O'Roak, B. J., Santini, E., Samaco, R. C., Kleiman, R. J., & Manzini, M. C. (2016) · The Journal of Neuroscience · doi:10.1523/jneurosci.2335-16.2016 · Cited by 54
“…rodent Well-controlled in vivo studies in a tractable model organism with a high degree of genetic conservation relative to humans have been instrumental to our current understanding of ASD pathogenesis, with the most useful mouse models having high construct and face validities (Crawley, 2007).”
BackgroundMethod
Absence of social conditioned place preference in BTBR T+tf/J mice: Relevance for social motivation testing in rodent models of autism
Pearson, B. L., Bettis, J. K., Meyza, K. Z., Yamamoto, L. Y., Blanchard, D. C., & Blanchard, R. J. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.04.040 · Cited by 57
d-Cycloserine improves sociability in the BTBR T+ Itpr3tf/J mouse model of autism spectrum disorders with altered Ras/Raf/ERK1/2 signaling
Burket, J. A., Benson, A. D., Tang, A., & Deutsch, S. I. (2013) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2013.05.003 · Cited by 57
Perseverative responding and neuroanatomical alterations in adult heterozygous reeler mice are mitigated by neonatal estrogen administration
Macrı̀, S., Biamonte, F., Romano, E., Marino, R., Keller, F., & Laviola, G. (2010) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2010.03.012 · Cited by 55
“Compared to other sociability tasks, the sequential procedure adopted in this study — based on previous work done in the Crawley’s group (see e.g. Crawley, 2007) — specifically allows addressing social approach during task 2 (comparison between the empty side and the novel stimulus) and social…”
Influential
Sustained lentiviral-mediated overexpression of microRNA124a in the dentate gyrus exacerbates anxiety- and autism-like behaviors associated with neonatal isolation in rats
Bahí, A. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2016.05.033 · Cited by 57
CD73 Is a Major Regulator of Adenosinergic Signalling in Mouse Brain
Kulesskaya, N., Võikar, V., Peltola, M. A., Yegutkin, G. G., Salmi, M., Jalkanen, S., & Rauvala, H. (2013) · PLoS ONE · doi:10.1371/journal.pone.0066896 · Cited by 54
“It is worth noting that changes in these behavioural patterns belong to endophenotypes (for the endophenotype concept, see [50]) of common behavioural disorders, such as schizophrenia [51] and autism [52].”
Background
NEXMIF/KIDLIA Knock-out Mouse Demonstrates Autism-Like Behaviors, Memory Deficits, and Impairments in Synapse Formation and Function
Gilbert, J. P., O’Connor, M. G., Templet, S., Moghaddam, M., Ioschpe, A. D. V., Sinclair, A., Zhu, L., Xu, W., & Man, H. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.0222-19.2019 · Cited by 55
“We therefore first sought to characterize the social behavior of the NEXMIF KO mouse in the three-chamber social task, a test broadly used for assessing mouse sociability and interest in social novelty (Crawley, 2007; Moy et al., 2009).”
Background
Communication, interventions, and scientific advances in autism: A commentary
Llaneza, D. C., DeLuke, S. V., Batista, M., Crawley, J. N., Christodulu, K. V., & Frye, C. A. (2010) · Physiology & Behavior · doi:10.1016/j.physbeh.2010.01.003 · Cited by 62
“‘Predictive validity’ is the anticipated response of animal models to treatments used to manage ASD in humans [142].”
BackgroundSelf-citation
Spatial navigation in autism spectrum disorders: a critical review
Smith, A. D. (2015) · Frontiers in Psychology · doi:10.3389/fpsyg.2015.00031 · Cited by 54
Activation of the G protein-coupled estrogen receptor, but not estrogen receptor α or β, rapidly enhances social learning.
Ervin, K., Mulvale, E., Gallagher, N., Roussel, V., & Choleris, E. (2015) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2015.04.002 · Cited by 48
Behavioral impact of maternal allergic-asthma in two genetically distinct mouse strains
Schwartzer, J. J., Careaga, M., Coburn, M., Rose, D. R., Hughes, H. K., & Ashwood, P. (2016) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2016.09.007 · Cited by 53
Early accumulation of intracellular fibrillar oligomers and late congophilic amyloid angiopathy in mice expressing the Osaka intra-Aβ APP mutation
Kulic, L., McAfoose, J., Welt, T., Tackenberg, C., Späni, C. B., Wirth, F., Finder, V. H., Konietzko, U., Giese, M., Eckert, A., et al. (2012) · Translational Psychiatry · doi:10.1038/tp.2012.109 · Cited by 51
“and carefully controlled tests was used to behaviorally assess mice for motoric and cognitive performance.(29) At the time of testing, mice were weighed and examined for”
BackgroundMethod
Studying Autism in Rodent Models: Reconciling Endophenotypes with Comorbidities
Argyropoulos, A., Gilby, K. L., & Hill‐Yardin, E. L. (2013) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2013.00417 · Cited by 51
“…the presence of potential comorbidities including anxiety-like and aggressive behaviors, seizures, disrupted motor activity, sleep dysfunction, and sensory processing deﬁcits (Crawley, 2007) as well as assays for gastrointestinal motility dysfunction (Roberts et al., 2007) in these models.”
Background
Relationship between Rgs2 gene expression level and anxiety and depression-like behaviour in a mutant mouse model: serotonergic involvement
Lifschytz, T., Broner, E. C., Zozulinsky, P., Slonimsky, A., Eitan, R., Greenbaum, L., & Lerer, B. (2011) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145711001453 · Cited by 51
“2008), we deemed it worthwhile to study the relationship of the different Rgs2 genotype groups in mice to preference for social novelty using the three-chamber sociability test (Crawley, 2007 ; Nadler et al. 2004).”
BackgroundMethod
Sex differences in vasopressin 1a receptor regulation of social communication within the lateral habenula and dorsal raphe of mice
Rigney, N., Beaumont, R., & Petrulis, A. (2020) · Hormones and Behavior · doi:10.1016/j.yhbeh.2020.104715 · Cited by 49
“Social communication and behavior Ultrasonic vocalizations (USV), urine marking, and social investigation by subjects was recorded in an acrylic three-chamber apparatus (Crawley 2007; Arakawa et al. 2008; Moy et al. 2009; Harvard Apparatus; dimensions: 20.3 × 42 × 22 cm).”
MethodInfluential
d-cycloserine improves sociability and spontaneous stereotypic behaviors in 4-week old mice
Deutsch, S. I., Pepe, G. J., Burket, J. A., Winebarger, E. E., Herndon, A. L., & Benson, A. D. (2011) · Brain Research · doi:10.1016/j.brainres.2011.12.040 · Cited by 49
Reduced Cortical BDNF Expression and Aberrant Memory inCarfKnock-Out Mice
McDowell, K. A., Hutchinson, A. N., Wong‐Goodrich, S. J. E., Presby, M. M., Su, D., Rodriguiz, R. M., Law, K., Williams, C. L., Wetsel, W. C., & West, A. E. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.3997-09.2010 · Cited by 52
“Reversal learning in the Morris water maze can suggest procedural and cognitive flexibility (Crawley, 2007).”
Background
The Protein Arginine Methyltransferase PRMT8 and Substrate G3BP1 Control Rac1-PAK1 Signaling and Actin Cytoskeleton for Dendritic Spine Maturation
Lo, L. H.-Y., Dong, R., Lyu, Q., & Lai, K. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.107744 · Cited by 51
“We performed the marbleburying test, which indicates repetitive behavior, and the threechamber social interaction test (Crawley, 2007; Moy et al., 2008; Silverman et al., 2010) on Prmt8 homozygous mice and wild-type littermates ( P45).”
Method
Impaired hippocampus-dependent spatial flexibility and sociability represent autism-like phenotypes in GluK2 mice
Micheau, J., Vimeney, A., Normand, E., Mulle, C., & Riedel, G. (2014) · Hippocampus · doi:10.1002/hipo.22290 · Cited by 43
What microglia depletion approaches tell us about the role of microglia on synaptic function and behavior
Basilico, B., Ferrucci, L., Khan, A., Angelantonio, S. D., Ragozzino, D., & Reverte, I. (2022) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2022.1022431 · Cited by 52
“C57BL/6 or 6J mice (typical experimental strains) also display sociability toward mice of other strains (e.g., CD-1 mice) (Crawley, 2007; van der Kooij and Sandi, 2012; Ayash et al., 2020).”
Background
Prenatal Stress Alters the Development of Socioemotional Behavior and Amygdala Neuron Excitability in Rats
Ehrlich, D., & Rainnie, D. G. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.55 · Cited by 48
Stereotypical Alterations in Cortical Patterning Are Associated with Maternal Illness-Induced Placental Dysfunction
Carpentier, P. A., Haditsch, U., Braun, A. E., Cantu, A., Moon, H. M., Price, R. O., Anderson, M. P., Saravanapandian, V., Ismail, K., Rivera, M., et al. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.4654-12.2013 · Cited by 51
“Finally, the behavioral anomalies, although mild, highlight changes in social interaction and associative processing that are thought to be relevant in mouse models of ASD (Crawley, 2007).”
BackgroundMethodInfluential
A Glo1-Methylglyoxal Pathway that Is Perturbed in Maternal Diabetes Regulates Embryonic and Adult Neural Stem Cell Pools in Murine Offspring
Yang, G., Cancino, G. I., Zahr, S. K., Guskjolen, A. J., Voronova, A., Gallagher, D., Frankland, P. W., Kaplan, D. R., & Miller, F. D. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.09.067 · Cited by 50
Phosphorylation of FMRP and alterations of FMRP complex underlie enhanced mLTD in adult rats triggered by early life seizures
Bernard, P. B., Castano, A. M., O’Leary, H., Simpson, K., Browning, M. D., & Benke, T. A. (2013) · Neurobiology of Disease · doi:10.1016/j.nbd.2013.06.013 · Cited by 48
Rett syndrome treatment in mouse models: Searching for effective targets and strategies
Ricceri, L., Filippis, B. D., & Laviola, G. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2012.08.010 · Cited by 46
Systematic autistic-like behavioral phenotyping of 4 mouse strains using a novel wheel-running assay
Karvat, G., & Kimchi, T. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.05.028 · Cited by 46
PRICKLE1 Interaction with SYNAPSIN I Reveals a Role in Autism Spectrum Disorders
Paemka, L., Mahajan, V. B., Skeie, J. M., Sowers, L. P., Ehaideb, S. N., Gonzalez‐Alegre, P., Sasaoka, T., Tao, H., Miyagi, A., Ueno, N., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0080737 · Cited by 47
The Receptor Guanylyl Cyclase Type D (GC-D) Ligand Uroguanylin Promotes the Acquisition of Food Preferences in Mice
Arakawa, H., Kelliher, K. R., Zufall, F., & Munger, S. D. (2013) · Chemical Senses · doi:10.1093/chemse/bjt015 · Cited by 46
“1983; Posadas-Andrews and Roper 1983; Valsecchi and Galef 1989; Crawley 2007; Ryan et al.”
Background
Dietary docosahexaenoic acid alleviates autistic-like behaviors resulting from maternal immune activation in mice
Weiser, M. J., Mucha, B., Denheyer, H., Atkinson, D., Schanz, N., Vassiliou, E. K., & Benno, R. H. (2015) · Prostaglandins Leukotrienes and Essential Fatty Acids · doi:10.1016/j.plefa.2015.10.005 · Cited by 49
“Alterations in ultrasonic vocalizations during early development have been observed in animal models of neurodevelopmental disorders, including autism [45,46].”
Method
Developmental exposures to ultrafine particle air pollution reduces early testosterone levels and adult male social novelty preference: Risk for children’s sex-biased neurobehavioral disorders
Sobolewski, M., Anderson, T., Conrad, K., Marvin, E., Klocke, C., Morris-Schaffer, K., Allen, J. L., & Cory-Slechta, D. A. (2018) · NeuroToxicology · doi:10.1016/j.neuro.2018.08.009 · Cited by 47
“To understand what underlying components of social behavior were disrupted by postnatal UFP exposure, we utilized a battery of social assays, including social place conditioning, social approach communication, and social recognition (Silverman et al., 2010; Crawley, 2007).”
Abnormal behaviours relevant to neurodevelopmental disorders in Kirrel3-knockout mice
Hisaoka, T., Komori, T., Kitamura, T., & Morikawa, Y. (2018) · Scientific Reports · doi:10.1038/s41598-018-19844-7 · Cited by 45
Setd5 haploinsufficiency alters neuronal network connectivity and leads to autistic-like behaviors in mice
Moore, S. M., Seidman, J. S., Ellegood, J., Gao, R., Savchenko, A., Troutman, T. D., Abe, Y., Stender, J. D., Lee, D., Wang, S., et al. (2019) · Translational Psychiatry · doi:10.1038/s41398-018-0344-y · Cited by 45
Intellectual disability: dendritic anomalies and emerging genetic perspectives
Quach, T., Stratton, H. J., Khanna, R., Kolattukudy, P. E., Honnorat, J., Meyer, K., & Duchemin, A. (2020) · Acta Neuropathologica · doi:10.1007/s00401-020-02244-5 · Cited by 47
Prenatal and Early‐Life Exposure to High‐Level Diesel Exhaust Particles Leads to Increased Locomotor Activity and Repetitive Behaviors in Mice
Thirtamara Rajamani, K., Doherty‐Lyons, S., Bolden, C., Willis, D., Hoffman, C., Zelikoff, J., Chen, L., & Gu, H. (2013) · Autism Research · doi:10.1002/aur.1287 · Cited by 42
“Social approach was measured in a three-chambered apparatus using a previously validated procedure [Crawley, 2007].”
BackgroundMethod
Lack of social exploratory activation in male μ-opioid receptor KO mice in response to playback of female ultrasonic vocalizations
Wöhr, M., Moles, A., Schwarting, R. K. W., & D'Amato, F. R. (2010) · Social Neuroscience · doi:10.1080/17470911003765560 · Cited by 49
“Currently, a robust set of sensitive mouse behavioral assays relevant to the first and third symptoms of autism, abnormal reciprocal social interactions and repetitive behaviors, is available (Crawley, 2007).”
Background
Schizophrenia-relevant behaviors in a genetic mouse model of constitutive Nurr1 deficiency
Vuillermot, S., Joodmardi, E., Perlmann, T., Ögren, S. O., Feldon, J., & Meyer, U. (2011) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2011.00698.x · Cited by 46
“As mice (like most other rodents) are highly social animals, social interaction can be efficiently studied under experimental conditions (Crawley 2007).”
Background
Animal models of autism spectrum disorders: Information for neurotoxicologists
Halladay, A. K., Amaral, D. G., Aschner, M., Bolivar, V. J., Bowman, A. B., DiCicco-Bloom, E. M., Hyman, S. L., Keller, F., Lein, P. J., Pessah, I. N., et al. (2009) · NeuroToxicology · doi:10.1016/j.neuro.2009.07.002 · Cited by 45
“They engage in both affiliative (e.g., play, huddling) and aggressive (e.g., biting, tail rattling) social behaviors that can be readily measured with a variety of assays (Crawley, 2007c).”
Influential
Specific Roles of NMDA Receptor Subunits in Mental Disorders
Yamamoto, H., Hagino, Y., Kasai, S., & Ikeda, K. (2015) · Current Molecular Medicine · doi:10.2174/1566524015666150330142807 · Cited by 48
“Failure to switch to the new position may be analogous to the inflexibility of routines that is characteristic of autism [136].”
Background
Modeling rare gene variation to gain insight into the oldest biomarker in autism: construction of the serotonin transporter Gly56Ala knock-in mouse
Veenstra-VanderWeele, J. M., Jessen, T. N., Thompson, B. J., Carter, M. D., Prasad, H. C., Steiner, J. A., Sutcliffe, J. S., & Blakely, R. (2009) · Journal of Neurodevelopmental Disorders · doi:10.1007/s11689-009-9020-0 · Cited by 43
“Some of these questions correspond to establishing face validity for behavioral traits that map onto autism symptoms (reviewed in [88]).”
Background
The deubiquitinase USP6 affects memory and synaptic plasticity through modulating NMDA receptor stability
Zeng, F., Ma, X., Zhu, L., Xu, Q., Zeng, Y., Gao, Y., Li, G., Guo, T., Zhang, H., Tang, X., et al. (2019) · PLoS Biology · doi:10.1371/journal.pbio.3000525 · Cited by 43
“Isolationinduced pup USV behavior is an assay widely used to characterize mouse models of human diseases that involve deficits in language and social behavior [9,27,28].”
Method
Communication and social interaction in the cannabinoid‐type 1 receptor null mouse: Implications for autism spectrum disorder
Fyke, W., Premoli, M., Echeverry‐Alzate, V., López‐Moreno, J. A., Lemaire, V., Crusio, W. E., Marsicano, G., Wöhr, M., & Pietropaolo, S. (2021) · Autism Research · doi:10.1002/aur.2562 · Cited by 43
“The assessment of these behavioral confounders also contributed to the evaluation of the ASDrelevant phenotypes of the CB1 mouse line, since anxiety and enhanced auditory startle are recognized as additional ASD symptoms and are therefore often investigated in genetic mouse models of ASD (Crawley, 2007; Silverman & Cr…”
Background

Authors: Crawley, J. N.
Affiliations: University of North Carolina at Chapel Hill (US)
Corresponding author: Crawley, Jacqueline N.
ORCID: 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
DOI: 10.1111/j.1750-3639.2007.00096.x
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
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor, 3 d)
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
Life Sciences › Neuroscience › Endocrine and Autonomic Systems › 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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Mouse Behavioral Assays Relevant to the Symptoms of Autism*

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