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Reduced scent marking and ultrasonic vocalizations in the BTBR T+tf/J mouse model of autism
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Qualitative impairments in communication, such as delayed language and poor interactive communication skills, are fundamental to the diagnosis of autism. Investigations into social communication in adult BTBR T+tf/J (BTBR) mice are needed to determine whether this inbred strain incorporates phenotypes relevant to the second diagnostic symptom of autism, communication deficits, along with its strong behavioral phenotypes relevant to the first and third diagnostic symptoms, impairments in social interactions and high levels of repetitive behavior. The aim of the present study was to simultaneously measure female urine-elicited scent marking and ultrasonic vocalizations in adult male BTBR mice, in comparison with a standard control strain with high sociability, C57BL/6J (B6), for the assessment of a potential communication deficit in BTBR. Adult male BTBR mice displayed lower scent marking and minimal ultrasonic vocalization responses to female urine obtained from both B6 and BTBR females. Lower scent marking and ultrasonic vocalizations in a social setting by BTBR, as compared with B6, are consistent with the well-replicated social deficits in this inbred mouse strain. Our findings support the interpretation that BTBR incorporate communication deficits, and suggest that scent marking and ultrasonic vocalizations offer promising measures of interest in social cues that may be widely applicable to investigations of mouse models of autism.
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“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 [70]
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Blanchard, D. C., Defensor, E. B., Meyza, K. Z., Pobbe, R. L. H., Pearson, B. L., Bolivar, V. J., & Blanchard, R. J. (2011) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2011.06.008 · Cited by 56
The role of the dopamine D1 receptor in social cognition: studies using a novel genetic rat model
Homberg, J. R., Olivier, J. D. A., Broeke, M. V., Youn, J., Ellenbroek, A. K., Karel, P., Shan, L., van Boxtel, R., Ooms, S. J., Balemans, M., et al. (2016) · Disease Models & Mechanisms · doi:10.1242/dmm.024752 · Cited by 52
“Scent marking was measured using a protocol very similar to that developed for mice (Wohr et al., 2011).”
NMDA receptor activation regulates sociability by its effect on mTOR signaling activity
Burket, J. A., Benson, A. D., Tang, A., & Deutsch, S. I. (2015) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2015.02.009 · Cited by 53
“In addition to the Balb/c mouse, the BTBR mouse is another inbred mouse strain that models impaired sociability and stereotypic behavior displayed by persons with ASDs (McFarlane et al., 2008; Silverman et al., 2010; Wöhr et al., 2011; Yang et al., 2007).”
Chao, O. Y.-H., Yunger, R., & Yang, Y. (2018) · Behavioural Brain Research · doi:10.1016/j.bbr.2018.03.014 · Cited by 52
Therapeutic Effect of a Synthetic RORα/γ Agonist in an Animal Model of Autism
Wang, Y., Billon, C., Walker, J. K., & Burris, T. P. (2015) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.5b00159 · Cited by 48
Characterization of ultrasonic vocalizations of Fragile X mice
Belagodu, A. P., Johnson, A. M., & Galvez, R. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2016.04.016 · Cited by 46
Perinatal Influences of Valproate on Brain and Behaviour: An Animal Model for Autism
Ranger, P., & Ellenbroek, B. A. (2015) · Current topics in behavioral neurosciences · doi:10.1007/7854_2015_404 · Cited by 43
Modeling dopamine dysfunction in autism spectrum disorder: from invertebrates to vertebrates
DiCarlo, G. E., & Wallace, M. T. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.12.017 · Cited by 39
Wöhr, M. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00073 · Cited by 43
Self-citationAffective communication in rodents
Wöhr, M., van Gaalen, M. M., & Schwarting, R. K. W. (2015) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000172 · Cited by 43
“Moreover, male BTBR mice do not emit USV to attract females and show reduced scent marking behavior in response to female urine cues, in stark contrast to male C57BL/6J mice (Wöhr et al., 2011).”
BackgroundSelf-citationNeuronal correlates of asocial behavior in a BTBR T+Itpr3tf/J mouse model of autism
Meyza, K. Z., Nikolaev, T., Kondrakiewicz, K., Blanchard, D. C., Blanchard, R. J., & Knapska, E. (2015) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2015.00199 · Cited by 45
Influence of stimulant-induced hyperactivity on social approach in the BTBR mouse model of autism
Silverman, J. L., Babineau, B. A., Oliver, C. F., Karras, M. N., & Crawley, J. N. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2012.07.042 · Cited by 46
“BTBR emit significantly fewer ultrasonic vocalizations in response to social olfactory cues and during reciprocal social interactions, as compared to other standard inbred strains such as C57BL/6J (B6) (Scattoni et al., 2008, 2011; Wohr et al., 2011).”
Self-citationPobbe, 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
“emit fewer ultrasonic vocalizations in several social settings [39,40], and display higher levels of repetitive self-grooming throughout developmental stages [37,38,41].”
The 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
“…(Bolivar et al., 2007; Moy et al., 2007), resistance to change (Moy et al., 2007; Moy and Nadler, 2008), increased display of self-grooming behavior (Pobbe et al., 2010), display of repetitive behaviors (Pearson et al., 2011), and reduced display of territorial scent marking (Wohr et al., 2011).”
BackgroundSociosexual and Communication Deficits after Traumatic Injury to the Developing Murine Brain
Semple, B. D., Noble‐Haeusslein, L. J., Kwon, Y. J., Sam, P. N., Gibson, A. M., Grissom, S., Brown, S., Adahman, Z., Hollingsworth, C. A., Kwakye, A., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0103386 · Cited by 40
“Quantification of scent marking was adapted from that previously described [22,26].”
BackgroundMethodInfluentialClinical and Neurobiological Relevance of Current Animal Models of Autism Spectrum Disorders
Kim, K. C., Gonzales, E. L., Lázaro, M. T., Choi, C. S., Bahn, G. H., Yoo, H. J., & Shin, C. Y. (2016) · Biomolecules & Therapeutics · doi:10.4062/biomolther.2016.061 · Cited by 44
“BTBR mice show decreased social behaviors (Bolivar et al., 2007), defects in ultrasonic vocalizations, (Wohr et al., 2011a), increased stereotyped repetitive behaviors (Amodeo et al., 2012) and repetitive self-grooming (McFarlane et al., 2008).”
BackgroundToddes, C., Lefevre, E. M., Brandner, D. D., Zugschwert, L., & Rothwell, P. E. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.2440-20.2021 · Cited by 36
Schwartzer, J. J., Koenig, C. M., & Berman, R. F. (2012) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2012.08.007 · Cited by 41
Physiological and Behavioral Responses to Vocalization Playback in Mice
Niemczura, A. C., Grimsley, J. M. S., Kim, C., Alkhawaga, A., Poth, A., Carvalho, A., & Wenstrup, J. J. (2020) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2020.00155 · Cited by 37
“…et al., 2008; Grimsley et al., 2011, 2016; Hanson and Hurley, 2012; Sangiamo et al., 2020) and how vocal behavior is altered by internal state (Gaub et al., 2016; Grimsley et al., 2016; Demir et al., 2020) and in disease models (Scattoni et al., 2008; Wöhr et al., 2011; Belagodu et al., 2016).”
BackgroundAhadullah, Yau, S., Lu, H., Lee, T. M. C., Guo, H., & Chan, C. C. H. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.06.043 · Cited by 33
Knoll, A. T., Jiang, K., & Levitt, P. R. (2017) · Genes Brain & Behavior · doi:10.1111/gbb.12431 · Cited by 27
Ornoy, A., Echefu, B. E., & Becker, M. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms251910469 · Cited by 36
Intact and impaired executive abilities in the BTBR mouse model of autism
Rutz, H. L. H., & Rothblat, L. A. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.05.048 · Cited by 32
Low 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-citationShin, B., Cepeda, C., Estrada‐Sánchez, A. M., Levine, M. S., Hodaei, L., Dai, Y., Jung, J. W., Ganguly, A., Clark, P. M., & Devaskar, S. U. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.0503-18.2018 · Cited by 29
“11C,D), similar to findings in mouse models of autism spectrum disorders (Zhao et al., 2010; Wöhr et al., 2011; Roy et al., 2012). glut3 flox/flox/CaMK2 -Cre (glut3 KO) genotype expresses a late adult phenotype Given that the glut3 flox/flox/nestin - Cre mice displayed significant stunting and…”
BackgroundNovel inter-hemispheric white matter connectivity in the BTBR mouse model of autism
Miller, V. M., Gupta, D., Neu, N., Cotroneo, A., Boulay, C. B., & Seegal, R. F. (2013) · Brain Research · doi:10.1016/j.brainres.2013.04.001 · Cited by 28
Yang, M., Lewis, F., Foley, G., & Crawley, J. N. (2015) · Physiology & Behavior · doi:10.1016/j.physbeh.2015.04.023 · Cited by 28
Self-citationGarcia‐Lazaro, J. A., Shepard, K. N., Miranda, J. A., Liu, R. C., & Lesica, N. A. (2015) · PLoS ONE · doi:10.1371/journal.pone.0133251 · Cited by 28
“Moreover, mouse communication has become an important model for elucidating the neurobiology of social behaviour [1–4], and mouse vocalizations are being used by researchers as a phenotyping tool for models of neural disorders like autism [5, 6], fragile X syndrome [7], and speech and language disorders [8].”
Modeling Social Communication Deficits in Mouse Models of Autism
Michetti, C. (2012) · Autism - Open Access · doi:10.4172/2165-7890.s1-007 · Cited by 30
Social Reward and Empathy as Proximal Contributions to Altruism: The Camaraderie Effect
Lahvis, G. P. (2016) · Current topics in behavioral neurosciences · doi:10.1007/7854_2016_449 · Cited by 28
“Assessments of scent marking, and of subject responses to maternal scent, have been used to phenotype mouse models of autism (Kane et al. 2012; Wöhr et al. 2011a, b).”
MethodAnimal Models of Autism Spectrum Disorders and Behavioral Techniques of their Examination
Hrabovska, S. V., & Salyha, Y. T. (2016) · Neurophysiology · doi:10.1007/s11062-017-9613-2 · Cited by 22
“Adult male mice of strains BTBRT T+tf/J (BTBR), when allowed to sniff urine of females, produced fewer ultrasound signals and left fewer aromatic tags than wild-type animals [72].”
Grimsley, J. M. S., Gadziola, M. A., & Wenstrup, J. J. (2013) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2012.00089 · Cited by 22
“The isolation vocalizations of infant mice are used as behavioral markers of stress (Rupniak et al., 2000) or disease state (Ricceri et al., 2007; Scattoni et al., 2008; Young et al., 2010; Wohr et al., 2011a).”
MethodEndo, N., Makinodan, M., Somayama, N., Komori, T., Kishimoto, T., & Nishi, M. (2019) · EXPERIMENTAL ANIMALS · doi:10.1538/expanim.18-0177 · Cited by 24
“The BTBr mouse strain is a widely used model of aSd because of the animals’ reduced sociability, which is consistent with the most important features of the aSd phenotype [2–5, 7, 10, 20, 22, 23, 25–27, 30, 33, 35–38].”
Rodent ultrasonic communication and its relevance for models of neuropsychiatric disorders
Wöhr, M., & Schwarting, R. K. W. (2010) · e-Neuroforum · doi:10.1007/s13295-010-0012-z · Cited by 22
Self-citationArakawa, H. (2020) · Neuroscience · doi:10.1016/j.neuroscience.2020.02.002 · Cited by 21
“, 2013), and the olfactory context, such as scent marking (Wöhr et al., 2011), and the social transmission of food preferences (McFarlane et al.”
BackgroundUltrasonic vocalizations during male–female interaction in the mouse model of Down syndrome Ts65Dn
Zampieri, B. L., Fernandez, F., Pearson-Smith, J. N., Stasko, M. R., & Costa, A. C. S. (2014) · Physiology & Behavior · doi:10.1016/j.physbeh.2014.02.020 · Cited by 21
Amygdalar neurotransmission alterations in the BTBR mice model of idiopathic autism
Bové, M., Palmieri, M. A., Santoro, M., Agosti, L. P., Gaetani, S., Romano, A., Dimonte, S., Costantino, G., Sikora, V., Tucci, P., et al. (2024) · Translational Psychiatry · doi:10.1038/s41398-024-02905-z · Cited by 22
“Among the different ASD mice models, the BTBR mouse strain shows robust and pronounced de fi cits in reciprocal social interactions, altered ultrasonic vocalization and repetitive stereotyped repertoire [13, 14].”
Metadata
- Authors
- Wöhr, M., Roullet, F. I., & Crawley, J. N.
- Affiliations
- National Institutes of Health (US)
- Corresponding author
- Wöhr, M.
- Venue
- Genes, Brain and Behavior
- Publisher
- Wiley
- Published
- 2010-03-22
- Volume
- 10
- Issue
- 1
- Pages
- 35-43
- ISSN
- 1601-183X (ISSN-L)
- 1601-1848
- PMC
- PMC2903641
- OpenAlex
- W2003863298
- Cited by
- 169
- References
- 69
- Citations by year
- 2026: 1 · 2025: 5 · 2024: 8 · 2023: 6 · 2022: 11 · 2021: 7 · 2020: 11 · 2019: 4 · 2018: 9 · 2017: 6 · 2016: 11 · 2015: 20 · 2014: 16 · 2013: 13 · 2012: 22
- FWCI
- 10.47
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Genes Brain & Behavior (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute for Health and Care Research
- National Institutes of Health
- National Institute of Mental Health (ZIAMH002179)
- 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
- BTBR T+tf/J mice, autism spectrum disorder, mouse models of autism, scent marking, ultrasonic vocalizations, social communication deficits, social interaction, C57BL/6J mice, social cues
- MeSH terms
- Animals, Animal Communication, Autistic Disorder, Behavior, Animal, Female, Male, Mice, Inbred C57BL, Mice, Neurologic Mutants, Motor Activity, Odorants, Ultrasonics, Urine, Vocalization, Animal, Mice
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