The DOI matches its Crossref record; 69 of the 69 references it cites were found in a registry or an index.
Reduced scent marking and ultrasonic vocalizations in the BTBR T+tf/J mouse model of autism
Open accessAbstract
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.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“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]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Diagnostic and Statistical Manual of Mental Disorders
Williams, J. B. W., & First, M. B. (2013) · Oxford University Press eBooks · doi:10.1093/acrefore/9780199975839.013.104 · Cited by 109,845
Diagnostic and Statistical Manual of Mental Disorders.
Widiger, T. A. (2000) · Oxford University Press eBooks · doi:10.1037/10518-009 · Cited by 19,766
Autism From 2 to 9 Years of Age
Lord, C., Risi, S., DiLavore, P. S., Shulman, C., Thurm, A., & Pickles, A. (2006) · Archives of General Psychiatry · doi:10.1001/archpsyc.63.6.694 · Cited by 973 · cited 1×
“Qualitative impairments in communication, such as delayed language and poor conversational skills, are fundamental to the diagnosis of autism (DSM-IV 2000; Frith & Happé 1994; Lord et al. 2001, 2006; Losh & Piven 2007; Volkmar et al. 2004).”
BackgroundPheromones and Animal Behaviour: Communication by Smell and Taste
Wyatt, T. D. (2003) · doi:10.1017/cbo9780511615061 · Cited by 951
Autism and the pervasive developmental disorders
Volkmar, F. R., & Klin, A. (2012) · doi:10.1093/med/9780199696758.003.0214 · Cited by 931
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 · Cited by 812
Self-citationMouse behavioral tasks relevant to autism: Phenotypes of 10 inbred strains
MOY, S., NADLER, J., YOUNG, N., PEREZ, A., HOLLOWAY, L., BARBARO, R., BARBARO, J., WILSON, L., THREADGILL, D., & LAUDER, J. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.07.030 · Cited by 776
Autism and pervasive developmental disorders
Volkmar, F. R., Lord, C., Bailey, A., Schultz, R. T., & Klin, A. (2004) · Journal of Child Psychology and Psychiatry · doi:10.1046/j.0021-9630.2003.00317.x · Cited by 616
(2007) · PubMed · Cited by 597
Jamain, S., Radyushkin, K., Hammerschmidt, K., Granon, S., Boretius, S., Varoqueaux, F., Ramanantsoa, N., Gallego, J., Ronnenberg, A., Winter, D., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0711555105 · Cited by 556
Unusual repertoire of vocalizations in the BTBR T+tf/J mouse model of autism
Scattoni, M. L., Gandhy, S. U., Ricceri, L., & Crawley, J. N. (2008) · PLoS ONE · doi:10.1371/journal.pone.0003067 · Cited by 550
Self-citationMammalian social odours: attraction and individual recognition
Brennan, P., & Kendrick, K. M. (2006) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2006.1931 · Cited by 510
Desjardins, C., MARUNIAK, J. A., & Bronson, F. H. (1973) · Science · doi:10.1126/science.182.4115.939 · Cited by 449
Altered ultrasonic vocalization in mice with a disruption in the Foxp2 gene
Shu, W., Cho, J. Y., Jiang, Y., Zhang, M., Weisz, D. J., Elder, G. A., Schmeidler, J., Gasperi, R. D., Sosa, M. A. G., Rabidou, D., et al. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0503739102 · Cited by 415
Neuroligin‐3‐deficient mice: model of a monogenic heritable form of autism with an olfactory deficit
Radyushkin, K., Hammerschmidt, K., Boretius, S., Varoqueaux, F., El-Kordi, A., Ronnenberg, A., Winter, D., Frahm, J., Fischer, J., Brose, N., et al. (2009) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2009.00487.x · Cited by 362
Urine marking in populations of wild house mice Mus domesticus rutty. I. Communication between males
Hurst, J. L. (1990) · Animal Behaviour · doi:10.1016/s0003-3472(05)80916-9 · Cited by 335
Panksepp, J. B., Jochman, K. A., Kim, J. U., Koy, J. J., Wilson, E. D., Chen, Q., Wilson, C. R., & Lahvis, G. P. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000351 · Cited by 295
Groszer, M., Keays, D. A., Deacon, R. M. J., de Bono, J. P., Prasad-Mulcare, S., Gaub, S., Baum, M. G., French, C. A., Nicod, J., Coventry, J. A., et al. (2008) · Current Biology · doi:10.1016/j.cub.2008.01.060 · Cited by 288
Aggression, anxiety and vocalizations in animals: GABAA and 5-HT anxiolytics
Miczek, K. A., Weerts, E. M., Vivian, J. A., & Barros, H. M. T. (1995) · Psychopharmacology · doi:10.1007/bf02245590 · Cited by 277
Ultrasound and mating behaviour in rodents with some observations on other behavioural situations
Sales, G. (1972) · Journal of Zoology · doi:10.1111/j.1469-7998.1972.tb01345.x · Cited by 268
Assessing autism-like behavior in mice: Variations in social interactions among inbred strains
BOLIVAR, V, WALTERS, S., & PHOENIX, J. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.09.007 · Cited by 264
Mice: Individual Recognition by Olfactory Cues
Bowers, J. M., & ALEXANDER, B. K. (1967) · Science · doi:10.1126/science.158.3805.1208 · Cited by 257
Fujita, E., Tanabe, Y., Shiota, A., Ueda, M., Suwa, K., Momoi, M. Y., & Momoi, T. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0712298105 · Cited by 233
Scent marking behavior as an odorant communication in mice
Arakawa, H., Blanchard, D. C., Arakawa, K., Dunlap, C., & Blanchard, R. J. (2008) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.05.012 · Cited by 229
Female mice respond to male ultrasonic ‘songs’ with approach behaviour
Hammerschmidt, K., Radyushkin, K., Ehrenreich, H., & Fischer, J. (2009) · Biology Letters · doi:10.1098/rsbl.2009.0317 · Cited by 226
Ultrasonic Communication in Rodents
SEWELL, G. D. (1970) · Nature · doi:10.1038/227410a0 · Cited by 222
Rat pup ultrasonic isolation calls: Possible mediation by the benzodiazepine receptor complex
Insel, T. R., Hill, J., & Mayor, R. B. (1986) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(86)90182-6 · Cited by 215
Social‐cognition and the broad autism phenotype: identifying genetically meaningful phenotypes
Losh, M. C., & Piven, J. (2006) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2006.01594.x · Cited by 209
Female behavior is affected by male ultrasonic vocalizations in house mice
Pomerantz, S. M., Núñez, A. A., & Bean, N. J. (1983) · Physiology & Behavior · doi:10.1016/0031-9384(83)90101-4 · Cited by 198
Development of a mouse test for repetitive, restricted behaviors: Relevance to autism
Moy, S. S., Nadler, J. J., Poe, M. D., Nonneman, R. J., Young, N. B., Koller, B. H., Crawley, J. N., Duncan, G. E., & Bodfish, J. W. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.10.029 · Cited by 195
Self-citationUltrasonic communication of adult myomorph rodents
Nyby, J., & Whitney, G. (1978) · Neuroscience & Biobehavioral Reviews · doi:10.1016/0149-7634(78)90003-9 · Cited by 173
Wang, H., Liang, S., Burgdorf, J. S., Wess, J., & Yeomans, J. S. (2008) · PLoS ONE · doi:10.1371/journal.pone.0001893 · Cited by 172
Wöhr, M., & Schwarting, R. K. W. (2008) · Behavioral Neuroscience · doi:10.1037/0735-7044.122.2.310 · Cited by 161
Self-citationLanguage and communication in autistic disorders
Frith, U., & Happe, F. G. E. (1994) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.1994.0133 · Cited by 160
Ultrasonic vocalizations during sex behavior of male house mice (Mus musculus): A description
Nyby, J. (1983) · Behavioral and Neural Biology · doi:10.1016/s0163-1047(83)90722-7 · Cited by 142
Hurst, J. L. (1990) · Animal Behaviour · doi:10.1016/s0003-3472(05)80918-2 · Cited by 136
Pheromonal regulation of male mouse ultrasonic courtship (Mus musculus)
Nyby, J., Wysocki, C. J., Whitney, G., & Dizinno, G. A. (1977) · Animal Behaviour · doi:10.1016/0003-3472(77)90009-4 · Cited by 135
Social deficits in BTBR T + tf/J mice are unchanged by cross‐fostering with C57BL/6J mothers
Yang, M., Zhodzishsky, V., & Crawley, J. N. (2007) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2007.09.008 · Cited by 132
Self-citationDizinno, G., Whitney, G., & Nyby, J. (1978) · Behavioral Biology · doi:10.1016/s0091-6773(78)92094-1 · Cited by 131
Ultrasound recognition in house mice: Key-Stimulus configuration and recognition mechanism
Ehret, G., & Haack, B. (1982) · Journal of Comparative Physiology A · doi:10.1007/bf00619131 · Cited by 124
Yang, M. (2007) · Frontiers in Behavioral Neuroscience · doi:10.3389/neuro.08.001.2007 · Cited by 124
Postnatal lesion evidence against a primary role for the corpus callosum in mouse sociability
Yang, M., Clarke, A. M., & Crawley, J. N. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06714.x · Cited by 117
Self-citationElicitation of male mouse (Mus musculus) ultrasonic vocalizations: I. Urinary cues.
Nyby, J., Wysocki, C. J., Whitney, G., Dizinno, G. A., & Schneider, J. E. (1979) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0077623 · Cited by 110
Social status and ultrasonic vocalizations of male mice
Nyby, J., Dizinno, G. A., & Whitney, G. (1976) · Behavioral Biology · doi:10.1016/s0091-6773(76)92198-2 · Cited by 102
Female odors evoke ultrasounds from male mice
Whitney, G., Alpern, M., Dizinno, G. A., & Horowitz, G. P. (1974) · Animal Learning & Behavior · doi:10.3758/bf03199109 · Cited by 101
Wöhr, M., Dahlhoff, M., Wolf, E., Holsboer, F., Schwarting, R. K. W., & Wotjak, C. T. (2008) · Behavior Genetics · doi:10.1007/s10519-008-9221-4 · Cited by 99
Self-citationHurst, J. L. (1989) · Animal Behaviour · doi:10.1016/0003-3472(89)90057-2 · Cited by 93
Cirulli, F., Santucci, D., Giovanni Laviola, A., Alleva, E., & Levine, S. D. (1994) · Developmental Psychobiology · doi:10.1002/dev.420270505 · Cited by 90
Urinary marking in male house mice: Responses to novel environmental and social stimuli☆
MARUNIAK, J. A., Owen, K., Bronson, F. H., & Desjardins, C. D. (1974) · Physiology & Behavior · doi:10.1016/0031-9384(74)90151-6 · Cited by 89
Fish, E. W., Sekinda, M., Ferrari, P. F., Dirks, A., & Miczek, K. A. (2000) · Psychopharmacology · doi:10.1007/s002130000370 · Cited by 87
Arakawa, H., Arakawa, K., Blanchard, D. C., & Blanchard, R. J. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.02.009 · Cited by 80
Experience-based vocalization of male mice to female chemosignals
Maggio, J. C., Maggio, J. C., & Whitney, G. (1983) · Physiology & Behavior · doi:10.1016/0031-9384(83)90186-5 · Cited by 76
Nyby, J., Bigelow, J., Kerchner, M., & Barbehenn, F. W. (1983) · Behavioral and Neural Biology · doi:10.1016/s0163-1047(83)90354-0 · Cited by 74
Exaggerated responses to stress in the BTBR T+tf/J mouse: An unusual behavioral phenotype
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
Scent marking behavior in male C57BL/6J mice: Sexual and developmental determination
Arakawa, H., ARAKAWA, K., Blanchard, D. C., & Blanchard, R. J. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.05.007 · Cited by 64
Nastiti, K., Benton, D., & Pf, B. (1991) · PubMed · Cited by 62
Effects of medial preoptic lesions on male mouse ultrasonic vocalizations and copulatory behavior
Bean, N. J., Núñez, A. A., & Conner, R. L. (1981) · Brain Research Bulletin · doi:10.1016/s0361-9230(81)80033-0 · Cited by 60
An ephemeral sex pheromone in the urine of female house mice (Mus domesticus)
Sipos, M. L., Kerchner, M., & Nyby, J. (1992) · Behavioral and Neural Biology · doi:10.1016/0163-1047(92)90375-e · Cited by 59
The influence of psychotropic drugs on the ultrasonic calling of mouse pups
Benton, D., & Nastiti, K. (1988) · Psychopharmacology · doi:10.1007/bf00212775 · Cited by 56
Takahashi, A., Yap, J. J., Bohager, D. Z., Faccidomo, S., Clayton, T., Cook, J. M., & Miczek, K. A. (2008) · Psychopharmacology · doi:10.1007/s00213-008-1437-8 · Cited by 56
Cues that Elicit Ultrasounds from Adult Male Mice
Whitney, G., & Nyby, J. (1979) · American Zoologist · doi:10.1093/icb/19.2.457 · Cited by 54
Ultrasonic vocalizations in mice and rats： social contexts and functions
Costantini, F., & D'Amato, F. R. (2006) · Europe PMC (PubMed Central) · Cited by 54
Urination as a Social Response in Mice
REYNOLDS, E. (1971) · Nature · doi:10.1038/234481a0 · Cited by 53
Sex Selectivity of Mouse Ultrasonic Songs
Guo, Z., & Holy, T. E. (2007) · Chemical Senses · doi:10.1093/chemse/bjm015 · Cited by 53
THE OLFACTORY RESPONSE OF MICE TO URINE AND EFFECTS OF GONADECTOMY
DAVIES, V. J., & Bellamy, D. (1972) · Journal of Endocrinology · doi:10.1677/joe.0.0550011 · Cited by 46
Courtship ultrasonic vocalizations and social status in mice
D'Amato, F. R. (1991) · Animal Behaviour · doi:10.1016/s0003-3472(05)80354-9 · Cited by 45
Effect of altricial pup ultrasonic vocalization on maternal behavior
Wöhr, M., Oddi, D., & D'Amato, F. R. (2010) · Handbook of behavioral neuroscience · doi:10.1016/b978-0-12-374593-4.00016-4 · Cited by 26
Self-citationElicitation of male mouse ultrasounds: Bladder urine and aged urine from females
Nyby, J., & Zakeski, D. M. (1980) · Physiology & Behavior · doi:10.1016/0031-9384(80)90405-9 · Cited by 26
Research works printed but not linked: 1
- Roberts, 2007, Rodent Societies. An Ecological and Evolutionary Perspective, 255
Cited by
Sorted by citations
Behavioural phenotyping assays for mouse models of autism
Silverman, J. L., Yang, M., Lord, C., & Crawley, J. N. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2851 · Cited by 1,462
Self-citationMalkova, N. V., Yu, C. Z., Hsiao, E. Y., Moore, M. J., & Patterson, P. H. (2012) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2012.01.011 · Cited by 662
“In addition to deficits in auditory communication, MIA males exhibit a reduction in female urine-induced scent marking, which was also found in BTBR and Shank1 KO males (Wohr et al., 2011a; 2011b).”
BackgroundMethodIn utero exposure to valproic acid and autism — A current review of clinical and animal studies
Roullet, F., Lai, J., & Foster, J. A. (2013) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2013.01.004 · Cited by 444
Self-citationYang, M., Bozdagi, O., Scattoni, M. L., Wöhr, M., Roullet, F. I., Katz, A. M., Abrams, D. N., Kalikhman, D., Simon, H., Woldeyohannes, L., et al. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.6107-11.2012 · Cited by 369
“One week after the male–female social interaction test, male subjects of the WT-HET group and Cohort 1 were tested for scent marking behaviors and ultrasonic vocalizations in the presence of female urinary pheromones, as previously described (Roullet et al., 2011; Wöhr et al., 2011).”
BackgroundMethodInfluentialSelf-citationScattoni, M. L., Ricceri, L., & Crawley, J. N. (2010) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2010.00623.x · Cited by 340
Self-citation
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
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
