Autism‐like behavioral phenotypes in BTBR T+tf/J mice

McFarlane, H. G.; Kusek, G. K.; Yang, M.; Phoenix, J. L.; Bolivar, V. J.; Crawley, J. N.

doi:10.1111/j.1601-183x.2007.00330.x

Cited by 817Autism Spectrum Disorder ResearchGenetics and Neurodevelopmental DisordersNeuroendocrine regulation and behavior

Autism‐like behavioral phenotypes in BTBR T+tf/J mice

McFarlane, H. G., Kusek, G. K., Yang, M., Phoenix, J. L., Bolivar, V. J., Crawley, J. N.·2008·Genes, Brain and Behavior

DOI 10.1111/j.1601-183x.2007.00330.x

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Abstract

Autism is a behaviorally defined neurodevelopmental disorder of unknown etiology. Mouse models with face validity to the core symptoms offer an experimental approach to test hypotheses about the causes of autism and translational tools to evaluate potential treatments. We discovered that the inbred mouse strain BTBR T+tf/J (BTBR) incorporates multiple behavioral phenotypes relevant to all three diagnostic symptoms of autism. BTBR displayed selectively reduced social approach, low reciprocal social interactions and impaired juvenile play, as compared with C57BL/6J (B6) controls. Impaired social transmission of food preference in BTBR suggests communication deficits. Repetitive behaviors appeared as high levels of self‐grooming by juvenile and adult BTBR mice. Comprehensive analyses of procedural abilities confirmed that social recognition and olfactory abilities were normal in BTBR, with no evidence for high anxiety‐like traits or motor impairments, supporting an interpretation of highly specific social deficits. Database comparisons between BTBR and B6 on 124 putative autism candidate genes showed several interesting single nucleotide polymorphisms (SNPs) in the BTBR genetic background, including a nonsynonymous coding region polymorphism in Kmo . The Kmo gene encodes kynurenine 3‐hydroxylase, an enzyme‐regulating metabolism of kynurenic acid, a glutamate antagonist with neuroprotective actions. Sequencing confirmed this coding SNP in Kmo , supporting further investigation into the contribution of this polymorphism to autism‐like behavioral phenotypes. Robust and selective social deficits, repetitive self‐grooming, genetic stability and commercial availability of the BTBR inbred strain encourage its use as a research tool to search for background genes relevant to the etiology of autism, and to explore therapeutics to treat the core symptoms.

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Repetitive behaviours are often seen in autistic patients and in some mouse models of ASDs.
“Repetitive behaviours are also often seen in autistic patients and in some mouse models of ASDs34–36.”
From Shank3 mutant mice display autistic-like behaviours and striatal dysfunction (2011) · cites this paper as [34]
BTBR mice show no social preference in the three-chambered social approach test.
“In contrast to C57Bl6J mice, BTBR mice show no social preference in the test (Fig. 1c, d).20,21”
From Enhancement of anandamide-mediated endocannabinoid signaling corrects autism-related social impairment (2016) · cites this paper as [20]
BTBR T+tf/J mice display behavioral phenotypes relevant to all three diagnostic symptoms of autism.
“BTBR T+tf/J (BTBR) is a commercially available inbred strain of mouse that displays behavioral phenotypes relevant to all three diagnostic symptoms of autism (60–62, 64, 66, 68–70, 72, 74–78).”
From Negative allosteric modulation of the mGluR5 receptor reduces repetitive behaviors and rescues social deficits in mouse models of autism (2012) · cites this paper as [64]
Several naturally occurring inbred strains of mice display behavioral features that recapitulate diagnostic symptoms of neurodevelopmental disorders.
“Several naturally occurring inbred strains of mice display behavioral features that recapitulate diagnostic symptoms of neurodevelopmental disorders (59–70).”
From Negative allosteric modulation of the mGluR5 receptor reduces repetitive behaviors and rescues social deficits in mouse models of autism (2012) · cites this paper as [64]
BTBR mice engage in low levels of reciprocal social interactions, minimal social approach, and low ultrasonic vocalizations compared to standard inbred strains such as C57BL/6J and FVB.
“BTBR engages in low levels of reciprocal social interactions as juveniles and adults, minimal social approach by both males and females, and low levels of ultrasonic vocalizations in response to social olfactory cues and during reciprocal social interactions compared to other standard inbred strains such as C57BL/6J (B6) and FVB (60–62, 64, 66, 68–70, 74, 76–78).”
From Negative allosteric modulation of the mGluR5 receptor reduces repetitive behaviors and rescues social deficits in mouse models of autism (2012) · cites this paper as [64]

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Shank3 mutant mice display autistic-like behaviours and striatal dysfunction
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Human Gut Microbiota from Autism Spectrum Disorder Promote Behavioral Symptoms in Mice
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Mouse Behavioral Assays Relevant to the Symptoms of Autism*
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Mouse neurexin-1α deletion causes correlated electrophysiological and behavioral changes consistent with cognitive impairments
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Repetitive Self-Grooming Behavior in the BTBR Mouse Model of Autism is Blocked by the mGluR5 Antagonist MPEP
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Sex differences in animal models of psychiatric disorders
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The neuropeptide oxytocin facilitates pro-social behavior and prevents social avoidance in rats and mice
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Nanoparticle delivery of CRISPR into the brain rescues a mouse model of fragile X syndrome from exaggerated repetitive behaviours
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Recent developments in understanding the role of the gut microbiota in brain health and disease
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Sensory Integration in Mouse Insular Cortex Reflects GABA Circuit Maturation
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Unusual repertoire of vocalizations in adult BTBR T+tf/J mice during three types of social encounters
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The neuroendocrinology of the microbiota-gut-brain axis: a behavioural perspective
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Gestational Exposure to Bisphenol A Produces Transgenerational Changes in Behaviors and Gene Expression
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Clustering autism: using neuroanatomical differences in 26 mouse models to gain insight into the heterogeneity
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Automated measurement of mouse social behaviors using depth sensing, video tracking, and machine learning
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Minimal aberrant behavioral phenotypes of neuroligin‐3 R451C knockin mice
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Autism: A “Critical Period” Disorder?
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Chronic stress followed by social isolation promotes depressive-like behaviour, alters microglial and astrocyte biology and reduces hippocampal neurogenesis in male mice
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Increased Gene Dosage of Ube3a Results in Autism Traits and Decreased Glutamate Synaptic Transmission in Mice
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Ketogenic diet modifies the gut microbiota in a murine model of autism spectrum disorder
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Tests of unconditioned anxiety — Pitfalls and disappointments
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Analyzing grooming microstructure in neurobehavioral experiments
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Negative allosteric modulation of the mGluR5 receptor reduces repetitive behaviors and rescues social deficits in mouse models of autism
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Chd8 Mutation Leads to Autistic-like Behaviors and Impaired Striatal Circuits
Platt, R. J., Zhou, Y., Slaymaker, I. M., Shetty, A. S., Weisbach, N. R., Kim, J.-A., Sharma, J., Desai, M., Sood, S., Kempton, H. R., et al. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.03.052 · Cited by 240 · see citing works
Sodium butyrate attenuates social behavior deficits and modifies the transcription of inhibitory/excitatory genes in the frontal cortex of an autism model
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Association of Mouse Dlg4 (PSD-95) Gene Deletion and Human DLG4 Gene Variation With Phenotypes Relevant to Autism Spectrum Disorders and Williams' Syndrome
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Maternal immune activation and strain specific interactions in the development of autism-like behaviors in mice
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Enhancement of Inhibitory Neurotransmission by GABA A Receptors Having α 2,3 -Subunits Ameliorates Behavioral Deficits in a Mouse Model of Autism
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Translational animal models of autism and neurodevelopmental disorders
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Sociability and motor functions in Shank1 mutant mice
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Prenatal infection leads to ASD-like behavior and altered synaptic pruning in the mouse offspring
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Preclinical research in Rett syndrome: setting the foundation for translational success
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GABAB Receptor Agonist R-Baclofen Reverses Social Deficits and Reduces Repetitive Behavior in Two Mouse Models of Autism
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Gut dysbiosis, defective autophagy and altered immune responses in neurodegenerative diseases: Tales of a vicious cycle
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Genetic-background modulation of core and variable autistic-like symptoms in Fmr1 knock-out mice
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Ketogenic Diet Improves Core Symptoms of Autism in BTBR Mice
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Replicable in vivo physiological and behavioral phenotypes of the Shank3B null mutant mouse model of autism
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Motor and cognitive stereotypies in the BTBR T+tf/J mouse model of autism
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Reduced scent marking and ultrasonic vocalizations in the BTBR T+tf/J mouse model of autism
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Gestational Exposure to Low Dose Bisphenol A Alters Social Behavior in Juvenile Mice
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Behavioral neuroscience of autism
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Autism-Relevant Social Abnormalities and Cognitive Deficits in Engrailed-2 Knockout Mice
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Developing zebrafish models of autism spectrum disorder (ASD)
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Optogenetic insights on the relationship between anxiety-related behaviors and social deficits
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Metabolic Dysfunction Underlying Autism Spectrum Disorder and Potential Treatment Approaches
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The gut microbiota regulates autism-like behavior by mediating vitamin B6 homeostasis in EphB6-deficient mice
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Authors: McFarlane, H. G., Kusek, G. K., Yang, M., Phoenix, J. L., Bolivar, V. J., & Crawley, J. N.
Affiliations: Kenyon College (US)
New York State Department of Health (US)
National Institute of Mental Health (US)
University of North Carolina at Chapel Hill (US)
Corresponding author: Crawley, J. N.
ORCID: Yang, M.
Bolivar, V. J.
Crawley, J. N.
Venue: Genes, Brain and Behavior
Publisher: Wiley
Published: 2007-04-27
Volume: 7
Issue: 2
Pages: 152-163
ISSN: 1601-183X (ISSN-L)
1601-1848
DOI: 10.1111/j.1601-183x.2007.00330.x
OpenAlex: W2071797996
Cited by: 812
References: 82
Citations by year: 2026: 23 · 2025: 36 · 2024: 41 · 2023: 49 · 2022: 52 · 2021: 62 · 2020: 51 · 2019: 44 · 2018: 47 · 2017: 48 · 2016: 63 · 2015: 50 · 2014: 52 · 2013: 42 · 2012: 51
FWCI: 8.99
Type: journal article
Language: en
Open access: closed
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: Genes Brain & Behavior (publishedVersion)
PubMed (publishedVersion)
Funders: National Institute for Health and Care Research
National Institutes of Health
University of North Carolina at Chapel Hill
National Institute of Mental Health
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, BTBR T+tf/J mice, social dysfunction, social approach, reciprocal social interaction, social transmission of food preference, KMO, single nucleotide polymorphisms, autism candidate genes, inbred mouse strains, mouse models of autism
MeSH terms: Aging, Animals, Autistic Disorder, Circadian Rhythm, Disease Models, Animal, Food Preferences, Mice, Inbred C57BL, Mice, Inbred Strains, National Institute of Mental Health (U.S.), Phenotype, Play and Playthings, Social Behavior, United States, Videotape Recording, Mice

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Autism‐like behavioral phenotypes in BTBR T+tf/J mice

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