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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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“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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Role of BDNF in the development of an OFC-amygdala circuit regulating sociability in mouse and human
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The autism diagnosis in translation: shared affect in children and mouse models of ASD
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Age‐specific autistic‐like behaviors in heterozygous Fmr1‐KO female mice
Gauducheau, M., Lemaire, V., D'Amato, F. R., Oddi, D., Crusio, W. E., & Pietropaolo, S. (2017) · Autism Research · doi:10.1002/aur.1743 · Cited by 40
“The specific behavioral abnormality of HET females could therefore be interpreted as sign of repetitive behavior or insistence on sameness, that can resemble a typical autistic core symptom [Crawley, 2007; McDougle, Kresch, & Posey, 2000].”
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“4) and the total protein content was estimated by Lowry et al [49].”
BackgroundMethodInfluentialPobbe, R. L. H., Pearson, B. L., Blanchard, D. C., & Blanchard, R. J. (2012) · Physiology & Behavior · doi:10.1016/j.physbeh.2012.02.024 · Cited by 40
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“…of ASDs from each other with respect to their profiles of deficits in various discrete dimensions of sociability [Brodkin, 2007; Brodkin, Hagemann, Nemetski, & Silver, 2004; Crawley, 2004, 2007; Moy et al., 2007; Silverman, Tolu, Barkan, & Crawley, 2010; Yang, Perry, Weber, Katz, & Crawley, 2010].”
BackgroundMethodInfluentialSex-Dependent Changes in Social Behaviors in Motor Pre-Symptomatic R6/1 Mice
Pietropaolo, S., Delage, P., Cayzac, S., Crusio, W. E., & Cho, Y. H. (2011) · PLoS ONE · doi:10.1371/journal.pone.0019965 · Cited by 43
“Time spent in selfgrooming (the animal licks and mouths its own fur) was analyzed separately, since this is sometimes considered representing a sign of repetitive behavior and emotional distress [48,50,51,52,53].”
BackgroundThe effects of aging on the BTBR mouse model of autism spectrum disorder
Jasien, J., Daimon, C. M., Wang, R., Shapiro, B. K., Martin, B., & Maudsley, S. R. (2014) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2014.00225 · Cited by 42
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“…scope of the current review to discuss in detail the breadth of rodent behavioural tests available (for comprehensive reviews of these assays see Crawley, 2007, Silverman et al., 2011), for readers unfamiliar with these behavioural assays, in the following section we will provide a brief…”
Morais, L. H., Felice, D., Golubeva, A. V., Moloney, G. M., Dinan, T. G., & Cryan, J. F. (2018) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000374 · Cited by 40
“These deficits have long been reported in C57BL6/J (Moy et al., 2006; Crawley, 2007) but, to our knowledge, this is the first study to show these MIA-induced deficits in NIH Swiss mice.”
BackgroundWhy Schizophrenia Epidemiology Needs Neurobiology--and Vice Versa
McGrath, J. J., & Richards, L. J. (2009) · Schizophrenia Bulletin · doi:10.1093/schbul/sbp004 · Cited by 40
Sociosexual and Communication Deficits after Traumatic Injury to the Developing Murine Brain
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“While we cannot exclude the possibility that general memory impairment may underlie this observation [62], the finding is suggestive of a deficit in social recognition and/ or social memory in this context [49,63,90].”
BackgroundResultDioxins as potential risk factors for autism spectrum disorder
Guo, Z., Xie, H. Q., Zhang, P., Luo, Y., Xu, T., Liu, Y., Fu, H., Xu, S. L., Valsami‐Jones, E., Boksa, P., et al. (2018) · Environment International · doi:10.1016/j.envint.2018.10.028 · Cited by 39
Weber‐Stadlbauer, U., Langhans, W., & Meyer, U. (2013) · Neuropsychopharmacology · doi:10.1038/npp.2013.146 · Cited by 42
“Finally, social interaction deficits are prominent in schizophrenic patients with marked negative symptoms (Foussias and Remington, 2010) and are also a cardinal feature of related neurodevelopmental disorders, especially autism (Crawley, 2007).”
Schwartzer, J. J., Koenig, C. M., & Berman, R. F. (2012) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2012.08.007 · Cited by 41
“For detailed descriptions and methods of each task see for example Crawley 2007; Moy, Nadler et al. 2007; Amodeo, Jones et al. 2012 ASD Signs Mouse Task Behavioral Measures Abnormal social approach, lack of initiation of social interaction1 Three-chambered social approach • Number of entries • Time…”
BackgroundMethodSingh, S., Mishra, A., Srivastava, N., & Shukla, S. (2016) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.6b00354 · Cited by 40
Novel behavioral assays of spontaneous and precipitated THC withdrawal in mice
Trexler, K. R., Nass, S. R., Crowe, M. S., Gross, J., Jones, M. S., McKitrick, A. W., Siderovski, D. P., & Kinsey, S. G. (2018) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2018.05.029 · Cited by 38
Murakami, Y., Imamura, Y., Saito, K., Sakai, D., & Motoyama, J. (2019) · Scientific Reports · doi:10.1038/s41598-019-49781-y · Cited by 40
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“Many behavioral phenotypes have been reported in transgenic and knockout mice, such as learning and memory impairments, feeding disorders, aberrant social, reproductive, parental behaviors, behaviors relevant to human anxiety, depression, schizophrenia, autism, drug addiction, and many others [19–21].”
BackgroundBehavioral Animal Models of Antipsychotic Drug Actions
Peleg‐Raibstein, D., Feldon, J., & Meyer, U. (2012) · Handbook of experimental pharmacology · doi:10.1007/978-3-642-25761-2_14 · Cited by 39
Onaivi, E. S., Benno, R. H., Halpern, T., Mehanovic, M., Schanz, N., Sanders, C., Yan, X., Ishiguro, H., Liu, Q.-R., Llorente‐Berzal, A., et al. (2011) · Current Neuropharmacology · doi:10.2174/157015911795017047 · Cited by 37
“Specifically mouse behavioral tests modeling some of the core symptoms of autism have now been established [11].”
BackgroundEarly development of social deficits in APP and APP-PS1 mice
Pietropaolo, S., Delage, P., Lebreton, F., Crusio, W. E., & Cho, Y. H. (2011) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2011.09.012 · Cited by 36
“Time spent in self-grooming (the animal licks and mouths its own fur) was analyzed separately, because this is sometimes considered representing a sign of repetitive behavior and emotional distress (Blundell et al., 2010; Crawley, 2007; Etherton et al., 2009; McFarlane et al., 2008; Mines et al., 2010).”
BackgroundExposure to Environmental Toxins in Mothers of Children with Autism Spectrum Disorder
Kim, S. M., Han, D. H., Lyoo, H. S., Min, K. J., Kim, K. H., & Renshaw, P. F. (2010) · Psychiatry Investigation · doi:10.4306/pi.2010.7.2.122 · Cited by 37
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Voltage-gated Calcium Channels and Autism Spectrum Disorders
Breitenkamp, A. F., Matthes, J., & Herzig, S. (2015) · Current Molecular Pharmacology · doi:10.2174/1874467208666150507105235 · Cited by 36
Grković, I., Drakulić, D., Martinović, J., & Mitrović, N. (2017) · Current Neuropharmacology · doi:10.2174/1570159x15666170518151541 · Cited by 37
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“Various tasks for assessing different aspects of social behavior of mice and rats have been developed (Crawley, 2007a, 2007b; Defensor et al., 2011; File, 1980; Sams-Dodd, 1995; Silverman et al., 2010; Terranova and Laviola, 2005) and they are summarized in Table 2.”
BackgroundVerma, M., Beaulieu‐Abdelahad, D., Ait‐Ghezala, G., Li, R., Crawford, F., MULLAN, M. J., & Paris, D. (2015) · PLoS ONE · doi:10.1371/journal.pone.0128224 · Cited by 36
“The three-chamber test known as the “Crawley's sociability and preference for social novelty protocol” was used to assess sociability and social memory [25].”
Effects of maternal or paternal bisphenol A exposure on offspring behavior
Harris, E. P., Allardice, H. A., Schenk, A. K., & Rissman, E. F. (2018) · Hormones and Behavior · doi:10.1016/j.yhbeh.2017.09.017 · Cited by 33
“The behavioral tests in this study were chosen to address the three core symptoms in ASD: communication difficulties, impaired social interactions, and perseverative behaviors (Crawley, 2007).”
Familiarity and Mate Preference Assessment with the Partner Preference Test
Beery, A. K. (2021) · Current Protocols · doi:10.1002/cpz1.173 · Cited by 39
“Background Information Contemporary neuroscience uses a variety of tests to assess social behaviors from recognition to social approach (Crawley, 2007; also see Current Protocols article: Winslow, 2003).”
BackgroundKumar, M., Kim, S., Pickup, S., Chen, R., Fairless, A. H., Ittyerah, R., Abel, T. G., Brodkin, E. S., & Poptani, H. (2012) · Brain Research · doi:10.1016/j.brainres.2012.03.041 · Cited by 35
“…confirm or disprove the correlation of DTI with social behavioral abnormalities, future studies involving additional mouse models relevant to ASD (Crawley, 2007; McFarlane et al., 2008; Moy et al., 2009; Tabuchi et al., 2007) and assays that test additional behavioral phenotypes relevant to ASD…”
BackgroundWitchey, S. K., Samara, L. A., Horman, B. M., Stapleton, H. M., & Patisaul, H. B. (2020) · Hormones and Behavior · doi:10.1016/j.yhbeh.2020.104853 · Cited by 33
“, 2019) using published testing methodologies (Crawley, 2007; Insel, 1999).”
MethodBernard, P. B., Castano, A. M., Beitzel, C. S., Carlson, V. B., & Benke, T. A. (2015) · Epilepsy & Behavior · doi:10.1016/j.yebeh.2015.01.006 · Cited by 35
“These abnormalities in the three-chambered SA task are consistent with ASD features after KA-ELS and other rodent models of ASD [31,36].”
BackgroundResultBlossom, S. J., Doss, J. C., Hennings, L. J., Jernigan, S., Melnyk, S., & James, S. J. (2008) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2008.05.009 · Cited by 33
“These behaviors have been validated as indicators of social behaviors in mice by others (Crawley, 2007; McFarlane et al., 2008).”
BackgroundComprehensive behavioral study and proteomic analyses of CRMP 2‐deficient mice
Nakamura, H., Yamashita, N., Kimura, A., Kimura, Y., Hirano, H., Makihara, H., Kawamoto, Y., Jitsuki‐Takahashi, A., Yonezaki, K., Takase, K., et al. (2016) · Genes to Cells · doi:10.1111/gtc.12403 · Cited by 32
“Auditory function was examined using the Preyer reflex test (Henry & Willott 1972; Huang et al. 1995; Crawley 2007; Takase et al. 2012) (Table S1 in Supporting Information).”
BackgroundMethodInfluentialNeurobiological Mechanisms of Autism Spectrum Disorder and Epilepsy, Insights from Animal Models
Sierra-Arregui, T., Llorente, J., Mínguez, P., Tønnesen, J., & Peñagarikano, O. (2020) · Neuroscience · doi:10.1016/j.neuroscience.2020.02.043 · Cited by 34
Amini, F., Amini-Khoei, H., Haratizadeh, S., Setayesh, M., Basiri, M., Raeiszadeh, M., & Nozari, M. (2023) · Journal of Traditional and Complementary Medicine · doi:10.1016/j.jtcme.2023.02.005 · Cited by 34
Eltokhi, A., Gonzalez-Lozano, M. A., Oettl, L.-L., Rozov, A., Pitzer, C., Röth, R., Berkel, S., Hüser, M., Harten, A., Kelsch, W., et al. (2021) · Molecular Psychiatry · doi:10.1038/s41380-021-01140-y · Cited by 38
“The test was performed as described previously [88], with some modifications.”
MethodOrnoy, A., Echefu, B. E., & Becker, M. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms251910469 · Cited by 36
“Several strategies are utilized for designing mouse models of ASD [12,13].”
MethodIs exposure to aluminium adjuvants associated with social impairments in mice? A pilot study
Sheth, S. K. S., Li, Y., & Shaw, C. A. (2017) · Journal of Inorganic Biochemistry · doi:10.1016/j.jinorgbio.2017.11.012 · Cited by 33
Computerized assessment of social approach behavior in mouse
Page, D. T. (2009) · Frontiers in Behavioral Neuroscience · doi:10.3389/neuro.08.048.2009 · Cited by 32
“…results are compared to those of other studies examining social approach in C57BL/6 mice using three-chambered apparatuses of varying dimensions (Crawley et al., 2007; Labrie et al., 2008; McFarlane et al., 2008), there was no substantial difference in chamber preference, even in cases where…”
BackgroundResultYee, B. K., & Singer, P. (2013) · Cell and Tissue Research · doi:10.1007/s00441-013-1611-0 · Cited by 31
“Sucrose preference test: measures the rewarding (hedonic) effect of sucrose consumption Reduced sucrose preference is a model of anhedonia, a negative symptom of SZ No human analogue Simple and cheap apparatus Preferentially performed in rats Concentration of sucrose solution Nutritional value of sucrose Pothion et al…”
BackgroundMethodInfluentialHenbid, M. T., Marks, W. N., Collins, M. J., Cain, S. M., Snutch, T. P., & Howland, J. G. (2017) · Experimental Neurology · doi:10.1016/j.expneurol.2017.06.022 · Cited by 32
Jia, Y., Wininger, K. M., Ho, A. M., Peyton, L., Baker, M., & Choi, D. (2020) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2020.00057 · Cited by 32
“The early stage of spontaneous seizures behavior in mice including grooming, jumping, and nodding etc. can be recognized as a type of repetitive behavior, which is highly correlated with anxiety (Crawley, 2007).”
BackgroundPrenatal Zinc Deficient Mice as a Model for Autism Spectrum Disorders
Sauer, A. K., Hagmeyer, S., & Grabrucker, A. M. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23116082 · Cited by 35
Impaired Social Behavior in 5-HT3A Receptor Knockout Mice
Smit‐Rigter, L. A., Wadman, W. J., & van Hooft, J. A. (2010) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2010.00169 · Cited by 31
A Model of Alcohol Drinking under an Intermittent Access Schedule Using Group-Housed Mice
Smutek, M., Turbasa, M., Sikora, M., Piechota, M., Zajdel, J., Przewłocki, R., & Parkitna, J. M. R. (2014) · PLoS ONE · doi:10.1371/journal.pone.0096787 · Cited by 30
“These types of models typically involve animals that are selected arbitrarily and are tested outside their home cages ([35–37], but see [23,38] for notable exceptions).”
BackgroundLow home cage social behaviors in BTBR T+tf/J mice during juvenile development
Babineau, B. A., Yang, M., Berman, R. F., & Crawley, J. N. (2013) · Physiology & Behavior · doi:10.1016/j.physbeh.2013.03.006 · Cited by 31
Self-citationHui, K. K., Katayama, Y., Nakayama, K. I., Nomura, J., & Sakurai, T. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.08.001 · Cited by 31
Stahmer, A. C., Aranbarri, A., Drahota, A., & Rieth, S. R. (2017) · Autism · doi:10.1177/1362361317692950 · Cited by 32
“Some first steps are being made in animal model research, where basic researchers have started to collaborate with clinical experts in autism to develop mouse behavioral assays relevant to human behavior (Crawley, 2007).”
BackgroundThe PAIR-R24M Dataset for Multi-animal 3D Pose EstimationPreprint
Marshall, J. D., Klibaite, U., Gellis, A., Aldarondo, D. E., Ölveczky, B. P., & Dunn, T. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.11.23.469743 · Cited by 30
“Currently, studies largely rely on scoring performance in highly structured assays, for instance the tube test, 3 chamber test, or resident-intruder test [6].”
BackgroundRigney, N., Zbib, A., de Vries, G. J., & Petrulis, A. (2022) · Journal of Neuroendocrinology · doi:10.1111/jne.13083 · Cited by 29
Chabout, J., Cressant, A., Hu, M. X., Edeline, J., & Granon, S. (2013) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2013.00468 · Cited by 34
Supplementation of Korean Red Ginseng improves behavior deviations in animal models of autism
Gonzales, E. L., Jang, J., Mabunga, D. F. N., Kim, J., Ko, M. J., Cho, K. S., Bahn, G. H., Hong, M., Ryu, J. H., Kim, H. J., et al. (2016) · Food & Nutrition Research · doi:10.3402/fnr.v60.29245 · Cited by 29
“In accordance with the duration in the compartments, sniffing duration may further show a more sensitive and ethological measure of social preference in mice (50) (Fig.”
BackgroundNeurodevelopmental Consequences of Dietary Zinc Deficiency: A Status Report
Ross, M. M., Hernández-Espinosa, D. R., & Aizenman, E. (2023) · Biological Trace Element Research · doi:10.1007/s12011-023-03630-2 · Cited by 31
“These observations from rodent behavioral assays have been used to explore the pathogenesis of neuropsychiatric conditions linked to zinc deficiency, including ASD [130].”
BackgroundThe EL mouse: A natural model of autism and epilepsy
Meidenbauer, J. J., Mantis, J. G., & Seyfried, T. N. (2011) · Epilepsia · doi:10.1111/j.1528-1167.2010.02898.x · Cited by 27
Memantine rescues prenatal citalopram exposure-induced striatal and social abnormalities in mice
Zahra, A., Jiang, J., Chen, Y., Long, C., & Yang, L. (2018) · Experimental Neurology · doi:10.1016/j.expneurol.2018.06.003 · Cited by 28
“The three-chambered social interaction test was conducted as described previously (Crawley, 2007; Moy et al., 2009).”
Early genistein exposure of California mice and effects on the gut microbiota–brain axis
Marshall, B. L., Liu, Y., Farrington, M. J., Mao, J., Helferich, W. G., Schenk, A. K., Bivens, N. J., Sarma, S. J., Lei, Z., Sumner, L. W., et al. (2019) · Journal of Endocrinology · doi:10.1530/joe-19-0214 · Cited by 29
“We chose this time period to elucidate the potential immediate effects perinatal exposure to GEN might exert on socio-communicative behaviors with deficits in these traits considered one type of autistic-like behaviors in rodent models of autism (Crawley 2007; Silverman, et al. 2010).”
Mabunga, D. F. N., Park, D., Ryu, O., Valencia, S. T., Adil, K. J., Kim, S., Kwon, K. J., Shin, C. Y., & Jeon, S. J. (2019) · Experimental Neurobiology · doi:10.5607/en.2019.28.6.697 · Cited by 29
“Adapted from Crawley [23] and modified by Kim et al.”
MethodComprehensive Behavioral Phenotyping of a 16p11.2 Del Mouse Model for Neurodevelopmental Disorders
Lynch, J. F., Ferri, S. L., Angelakos, C. C., Schoch, H., Nickl‐Jockschat, T., Gonzalez, A., O'Brien, W. T., & Abel, T. G. (2020) · Autism Research · doi:10.1002/aur.2357 · Cited by 28
“Mice are vocal throughout their lifespan with the earliest vocalizations occurring shortly after birth and peaking by postnatal day 8 [Crawley, 2007].”
BackgroundGottfried, C., Bambini-Júnior, V., Baronio, D., Zanatta, G., Bristot, R., Vaccaro, T. D. S., & Riesgo, R. D. S. (2013) · InTech eBooks · doi:10.5772/54824 · Cited by 33
“The main aspects to take into account in developing animal models, is (i) to reproduce a circumstance that would lead to a certain condition, for example, inducing a genetic disease by manipulating a specific gene; (ii) to induce similar patterns found in the studied condition, for example, observing the same behavior…”
BackgroundGunn, R. K., Huentelman, M. J., & Brown, R. E. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.07.008 · Cited by 31
“A mouse model of autism should replicate at least one core symptom of the human disorder, if not all three, and some of the secondary symptoms [16].”
BackgroundChlorination byproducts induce gender specific autistic-like behaviors in CD-1 mice
Guariglia, S. R., Jenkins, E. C., Chadman, K. K., & Wen, G. Y. (2011) · NeuroToxicology · doi:10.1016/j.neuro.2011.06.008 · Cited by 27
Tests for learning and memory in rodent regulatory studies
Vorhees, C. V., & Williams, M. T. (2024) · Current Research in Toxicology · doi:10.1016/j.crtox.2024.100151 · Cited by 34
“Social learning: The Crawley social preference test (Crawley, 2007b) and social interaction test (Crawley, 2007a) have not been used in regulatory studies to our knowledge, although FDA has indicated that social tests may be appropriate in juvenile toxicity studies.”
MethodThe dynamic state of a prefrontal–hypothalamic–midbrain circuit commands behavioral transitions
Chen, C., Altafi, M., Corbu, M.-A., Trenk, A., van den Munkhof, H. E., Weineck, K., Bender, F., Carús-Cadavieco, M., Bakhareva, A., Korotkova, T. M., et al. (2024) · Nature Neuroscience · doi:10.1038/s41593-024-01598-3 · Cited by 28
“…to feeding and to social interactions: exposure to a new environment suppresses feeding Article https://doi.org/10.1038/s41593-024-01598-3 behavior in mice 59 ; animals spend more time with a new conspecific than with a familiar one 60 , suggesting overlapping circuits encoding those behaviors.”
InfluentialmTOR plays an important role in cow's milk allergy-associated behavioral and immunological deficits
Wu, J., de Theije, C. G. M., da Silva, S. L., van der Horst, H. J., Reinders, M. T. M., Broersen, L. M., Willemsen, L. E. M., Kas, M. J., Garssen, J., & Kraneveld, A. D. (2015) · Neuropharmacology · doi:10.1016/j.neuropharm.2015.04.035 · Cited by 28
Alexander, J., Pirone, A., & Jacob, M. H. (2020) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2020.00014 · Cited by 25
“β-cat cOEs Exhibit Phenotypes Relevant to ASD, But APC/β-cat cKOs Do Not Using the classic three-chamber assay (Crawley, 2007), we tested for altered social interactions in the β-cat cOEs (elevated β-cat, normal APC levels) and APC/β-cat cKOs (reduced β-cat, reduced APC), compared to their control littermates and to A…”
ResultShahrbabaki, S. S. V., Jonaidi, H., Sheibani, V., & Bashiri, H. (2022) · Physiology & Behavior · doi:10.1016/j.physbeh.2022.113739 · Cited by 27
Guerra, M., Medici, V., Weatheritt, R. J., Corvino, V., Palacios, D., Geloso, M. C., Farini, D., & Sette, C. (2023) · Translational Psychiatry · doi:10.1038/s41398-023-02391-9 · Cited by 27
“During the entire duration of the three-chamber social behaviour test, also self-grooming duration and frequency were evaluated to assess the presence of repetitive or stereotypical actions [41].”
BackgroundMethodSchwabenland, M., Mossad, O., Sievert, A., Peres, A. G., Ringel, E., Baasch, S., Kolter, J., Cascone, G., Dokalis, N., Vlachos, A., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-38373-0 · Cited by 26
Blossom, S. J., Cooney, C. A., Melnyk, S. B., Rau, J. L., Swearingen, C. J., & Wessinger, W. D. (2013) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2013.03.025 · Cited by 26
“These behavioral tests were loosely based on free exploration tests and reaction to novel object tests as described (Belzung and Griebel, 2001; Crawley, 2007).”
MethodLee, J. Y., Kwak, M., & Lee, P. C.-W. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.12.019 · Cited by 26
Ornaghi, S., Hsieh, L. S., Bordey, A., Vergani, P., Paidas, M. J., & van den Pol, A. N. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.0970-17.2017 · Cited by 25
“Sociability and preference for social novelty were investigated at 5 weeks of age in a threecompartment apparatus (Crawley, 2007; Yang et al., 2011).”
BackgroundMerali, Z., Presti-Torres, J., MacKay, J. C., Johnstone, J., Du, L., St-Jean, A., Levesque, D., Kent, P., Schwartsmann, G., Roesler, R., et al. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.01.008 · Cited by 25
Altered social interaction in adult rats following neonatal treatment with domoic acid
Ryan, C. L., Robbins, M. A., Smith, M. T., Gallant, I. C., Marriott, A. L., & Doucette, T. A. (2010) · Physiology & Behavior · doi:10.1016/j.physbeh.2010.11.020 · Cited by 25
Tanaka, K., Osako, Y., Takahashi, K., Hidaka, C., Tomita, K., & Yuri, K. (2019) · Heliyon · doi:10.1016/j.heliyon.2019.e01646 · Cited by 25
“The preferential processing of social over non-social stimuli is commonly observed in healthy adult humans, while it is disrupted in schizophrenia, autism, and the rodent models of these disorders [22, 23, 24].”
BackgroundStrain differences in behaviour and immunity in aged mice: Relevance to Autism
O’Connor, R., van de Wouw, M., Moloney, G. M., Ventura‐Silva, A. P., O’Riordan, K. J., Golubeva, A. V., Dinan, T. G., Schellekens, H., & Cryan, J. F. (2020) · Behavioural Brain Research · doi:10.1016/j.bbr.2020.113020 · Cited by 25
“9 social deficits, with putative face validity to autism based on mouse behavioural measures that do not represent the human ASD behavioural spectrum [79].”
BackgroundLong-term obesity is associated with depression and neuroinflammation
Lorena, F. B., do Nascimento, B. P. P., Camargo, E. L. R. A., Bernardi, M. M., Fukushima, A. R., Panizza, J. D. N., Nogueira, P. D. B., Brandão, M. E., & Ribeiro, M. O. (2021) · Archives of Endocrinology and Metabolism · doi:10.20945/2359-3997000000400 · Cited by 26
“The test evaluated the time that the animal interacted with the known and unknown animals (52,53).”
BackgroundEnvironmental novelty and illumination modify ethanol-induced open-field behavioral effects in mice
Fukushiro, D. F., Benetti, L. F., Josino, F. S., de Oliveira, G. P., Fernandes, M. D., Saito, L. P., Uehara, R. A., Wuo‐Silva, R., Oliveira, C. S., & Frussa‐Filho, R. (2009) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2009.12.001 · Cited by 25
“In this regard, groomingbehavior of rodents has been shown to be affected by stimulation of dopamine D1 receptors (Beninger et al., 1991) and stress (Moody et al., 1988) and consists in an important feature of a range of neuropsychiatric diseases (Crawley, 2007; Graybiel and Saka, 2002).”
BackgroundComprehensive neurocognitive endophenotyping strategies for mouse models of genetic disorders
Hunsaker, M. R. (2012) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2011.12.001 · Cited by 26
NOMA-GAP/ARHGAP33 regulates synapse development and autistic-like behavior in the mouse
Schuster, S., Rivalan, M., Strauß, U., Stoenica, L., Trimbuch, T., Rademacher, N., Parthasarathy, S., Lajkó, D., Rosenmund, C., Shoichet, S. A., et al. (2015) · Molecular Psychiatry · doi:10.1038/mp.2015.42 · Cited by 26
Early-onset behavioral and neurochemical deficits in the genetic mouse model of phenylketonuria
Fiori, E., Oddi, D., Ventura, R., Colamartino, M., Valzania, A., D'Amato, F. R., Bruinenberg, V. M., van der Zee, E., Puglisi‐Allegra, S., & Pascucci, T. (2017) · PLoS ONE · doi:10.1371/journal.pone.0183430 · Cited by 25
Pietropaolo, S., & Marsicano, G. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.11.031 · Cited by 23
Growth restriction, leptin, and the programming of adult behavior in mice
Meyer, L. R., Zhu, V. L., Miller, A. K., & Roghair, R. D. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.08.054 · Cited by 24
“Social interaction was assessed using a tripartite chamber using previously described methods [14], [15], and [16].”
MethodMouse Models of 22q11.2-Associated Autism Spectrum Disorder
Hiroi, N. (2012) · Autism - Open Access · doi:10.4172/2165-7890.s1-001 · Cited by 25
“Unlike a “sociability” task in which one of the mice is confined in a small wire cage, reciprocal interaction can be evaluated in this naturalistic social interaction task [111].”
BackgroundPujol, C., Pellissier, L. P., Clément, C., Becker, J. A. J., & Merrer, J. L. (2018) · Translational Psychiatry · doi:10.1038/s41398-018-0247-y · Cited by 22
Bond, C. M., Johnson, J. C., Chaudhary, V., McCarthy, E. M., McWhorter, M. L., & Woehrle, N. S. (2019) · Brain Research · doi:10.1016/j.brainres.2019.06.001 · Cited by 27
The role of the endocannabinoid system in autism spectrum disorders: Evidence from mouse studies
Pietropaolo, S., Bellocchio, L., Bouzón‐Arnáiz, I., & Yee, B. K. (2020) · Progress in molecular biology and translational science · doi:10.1016/bs.pmbts.2020.04.016 · Cited by 24
“The definition of the precise criteria that a valid model for ASD should fulfil is still the subject of an intense debate [16]: the most obvious point of view considers an ideal animal model as the one mimicking all core autistic features in association with some of the secondary ones.”
BackgroundWorms on the spectrum - C. elegans models in autism research
Schmeißer, K., & Parker, J. A. (2017) · Experimental Neurology · doi:10.1016/j.expneurol.2017.04.007 · Cited by 26
“Rodent models of repetitive behaviour and motor stereotypies, such as excessive self-grooming and abnormal social interactions, have become the most studied phenotypes in ASD mouse models (Crawley, 2007).”
Fang, K., Liu, D., Pathak, S. S., Yang, B., Li, J., Ramanujam, K., Chao, O. Y.-H., Yang, Y., Jin, V. X., & Cao, R. (2021) · Cells · doi:10.3390/cells10123314 · Cited by 24
“The three-chamber test was performed, as published in [29], using a clear polyvinyl chloride (PVC) apparatus (60 cm × 40 cm × 20 cm) with three compartments (20 cm × 40 cm × 20 cm).”
MethodMolecular and behavioral consequences of Ube3a gene overdosage in mice
Punt, A. M., Judson, M. C., Sidorov, M. S., Williams, B., Johnson, N. S., Belder, S., den Hertog, D., Davis, C. R., Feygin, M. S., Lang, P. F., et al. (2022) · JCI Insight · doi:10.1172/jci.insight.158953 · Cited by 25
“To potentially capture phenotypes relevant to social deficits in ASD, we exposed Ube3a +4 mice to the 3-chamber social interaction test (57–59).”
Are NCAM deficient mice an animal model for schizophrenia?
Albrecht, A., & Stork, O. (2012) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2012.00043 · Cited by 23
On the Digital Psychopharmacology of Valproic Acid in Mice
Bass, J. S., Tuo, A., Ton, L. T., Jankovic, M. J., Kapadia, P., Schirmer, C., & Krishnan, V. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.594612 · Cited by 22
“Rather than manually score specific social behaviors like “sniffing” or “following” (Crawley, 2007), we simultaneously tracked both mice to capture a continuous readout of inter-mouse proximity, termed DBS (distance between subjects).”
BackgroundDeutsch, S. I., Luyo, Z. N. M., & Burket, J. A. (2022) · Biomolecules · doi:10.3390/biom12020181 · Cited by 22
A Brain Region-Specific Predictive Gene Map for Autism Derived by Profiling a Reference Gene Set
Kumar, A., Swanwick, C. C., Johnson, N., Menashe, I., Basu, S. N., Bales, M. E., & Banerjee‐Basu, S. (2011) · PLoS ONE · doi:10.1371/journal.pone.0028431 · Cited by 23
“For example, he olfactory bulb, which transmits information pertaining to smell, has been strongly implicated in mouse models of ASD due to its well-established role in their social behavior [60].”
Henzel, K. S., Ryan, D. P., Schröder, S., Weiergräber, M., & Ehninger, D. (2017) · Scientific Reports · doi:10.1038/s41598-017-03158-1 · Cited by 21
Metadata
- 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
- 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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