Ultrasonic vocalizations in Shank mouse models for autism spectrum disorders: Detailed spectrographic analyses and developmental profiles

Neuroscience and Biobehavioral Reviews

Volumn 43, Issue , 2014, Pages 199-212

  Wöhr, Markus ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

Animal model; Neurodevelopmental disorders; Postsynaptic density; Social behavior; Ultrasonic communication

Indexed keywords

AGGRESSION; AUTISM; BEHAVIOR DISORDER; BREEDING METHOD; COMMUNICATION DISORDER; DEVELOPMENTAL DISORDER; DEVELOPMENTAL STAGE; DISEASE MODEL; GENOTYPE; JUVENILE ANIMAL; MOUSE; MOUSE STRAIN; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REVIEW; SEX DIFFERENCE; SHANK MOUSE; SHANK1 MOUSE; SHANK2 MOUSE; SHANK3 MOUSE; SOCIAL BEHAVIOR; SOCIAL INTERACTION; SOCIAL ISOLATION; STRAIN DIFFERENCE; ULTRASONIC VOCALIZATION; VOCALIZATION; ANIMAL; GENETICS; HUMAN; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; CHILD DEVELOPMENT DISORDERS, PERVASIVE; DEVELOPMENTAL DISABILITIES; DISEASE MODELS, ANIMAL; HUMANS; MICE; PHENOTYPE; SOCIAL BEHAVIOR; VOCALIZATION, ANIMAL;

EID: 84899839947     PISSN: 01497634     EISSN: 18737528     Source Type: Journal    
DOI: 10.1016/j.neubiorev.2014.03.021     Document Type: Review

References (99)

1. Abrahams B.S., Geschwind D.H. Advances in autism genetics: on the threshold of a new neurobiology. Nat. Rev. Genet. 2008, 9:341-355.
2. American Psychiatric Association Diagnostic and Statistical Manual of Mental Disorders 2013, American Psychiatric Publishing, Arlington, VA. 5th ed.
3. Asperger H. Die "Autistischen Psychopathen" im Kindesalter. Archiv für Psychiatrie und Nervenkrankheiten 1944, 117:76-136.
4. Arakawa H., Blanchard D.C., Arakawa K., Dunlap C., Blanchard R.J. Scent marking behavior as an odorant communication in mice. Neurosci. Biobehav. Rev. 2008, 32:1236-1248.
5. Bangash M.A., Park J.M., Melnikova T., Wang D., Jeon S.K., Lee D., Syeda S., Kim J., Kouser M., Schwartz J., Cui Y., Zhao X., Speed H.E., Kee S.E., Tu J.C., Hu J.H., Petralia R.S., Linden D.J., Powell C.M., Savonenko A., Xiao B., Worley P.F. Enhanced polyubiquitination of Shank3 and NMDA receptor in a mouse model of autism. Cell 2011, 145:758-772.
6. Bangash M.A., Park J.M., Melnikova T., Wang D., Jeon S.K., Lee D., Syeda S., Kim J., Kouser M., Schwartz J., Cui Y., Zhao X., Speed H.E., Kee S.E., Tu J.C., Hu J.H., Petralia R.S., Linden D.J., Powell C.M., Savonenko A., Xiao B., Worley P.F. Retraction notice to: enhanced polyubiquitination of Shank3 and NMDA receptor in a mouse model of autism. Cell 2013, 152:367.
7. Bell R.W., Nitschke W., Zachman T.A. Ultra-sounds in three inbred strains of young mice. Behav. Biol. 1972, 7:805-814.
8. Benton D., Nastiti K. The influence of psychotropic drugs on the ultrasonic calling of mouse pups. Psychopharmacology (Berl) 1988, 95:99-102.
9. Berkel S., Marshall C.R., Weiss B., Howe J., Roeth R., Moog U., Endris V., Roberts W., Szatmari P., Pinto D., Bonin M., Riess A., Engels H., Sprengel R., Scherer S.W., Rappold G.A. Mutations in the SHANK2 synaptic scaffolding gene in autism spectrum disorder and mental retardation. Nat. Genet. 2010, 42:489-491.
10. Bishop S.L., Lahvis G.P. The autism diagnosis in translation: shared affect in children and mouse models of ASD. Autism Res. 2011, 4:317-335.
11. Boccuto L., Lauri M., Sarasua S.M., Skinner C.D., Buccella D., Dwivedi A., Orteschi D., Collins J.S., Zollino M., Visconti P., Dupont B., Tiziano D., Schroer R.J., Neri G., Stevenson R.E., Gurrieri F., Schwartz C.E. Prevalence of SHANK3 variants in patients with different subtypes of autism spectrum disorders. Eur. J. Hum. Genet. 2013, 21:310-316.
12. Boeckers T.M., Winter C., Smalla K.H., Kreutz M.R., Bockmann J., Seidenbecher C., Garner C.C., Gundelfinger E.D. Proline-rich synapse-associated proteins ProSAP1 and ProSAP2 interact with synaptic proteins of the SAPAP/GKAP family. Biochem. Biophys. Res. Commun. 1999, 264:247-252.
13. Bozdagi O., Sakurai T., Papapetrou D., Wang X., Dickstein D.L., Takahashi N., Kajiwara Y., Yang M., Katz A.M., Scattoni M.L., Harris M.J., Saxena R., Silverman J.L., Crawley J.N., Zhou Q., Hof P.R., Buxbaum J.D. Haploinsufficiency of the autism-associated Shank3 gene leads to deficits in synaptic function, social interaction, and social communication. Mol. Autism 2010, 1:15.
14. Branchi I., Santucci D., Vitale A., Alleva E. Ultrasonic vocalizations by infant laboratory mice: a preliminary spectrographic characterization under different conditions. Dev. Psychobiol. 1998, 33:249-256.
15. Brunner D., Buhot M.C., Hen R., Hofer M. Anxiety, motor activation, and maternal-infant interactions in 5HT1B knockout mice. Behav. Neurosci. 1999, 113:587-601.
16. Chabout J., Serreau P., Ey E., Bellier L., Aubin T., Bourgeron T., Granon S. Adult male mice emit context-specific ultrasonic vocalizations that are modulated by prior isolation or group rearing environment. PLoS ONE 2012, 7:e29401.
17. Cirulli F., Santucci D., Laviola G., Alleva E., Levine S. Behavioral and hormonal responses to stress in the newborn mouse: effects of maternal deprivation and chlordiazepoxide. Dev. Psychobiol. 1994, 27:301-316.
18. D'Amato F.R., Scalera E., Sarli C., Moles A. Pups call, mothers rush: does maternal responsiveness affect the amount of ultrasonic vocalizations in mouse pups?. Behav. Genet. 2005, 35:103-112.
19. Dhar S.U., del Gaudio D., German J.R., Peters S.U., Ou Z., Bader P.I., Berg J.S., Blazo M., Brown C.W., Graham B.H., Grebe T.A., Lalani S., Irons M., Sparagana S., Williams M., Phillips J.A., Beaudet A.L., Stankiewicz P., Patel A., Cheung S.W., Sahoo T. 22q13.3 deletion syndrome: clinical and molecular analysis using array CGH. Am. J. Med. Genet. A 2010, 152:573-581.
20. Dizinno G., Whitney G., Nyby J. Ultrasonic vocalizations by male mice (Mus musculus) to female sex pheromone: experimental determinants. Behav. Biol. 1978, 22:104-113.
21. Durand C.M., Betancur C., Boeckers T.M., Bockmann J., Chaste P., Fauchereau F., Nygren G., Rastam M., Gillberg I.C., Anckarsäter H., Sponheim E., Goubran-Botros H., Delorme R., Chabane N., Mouren-Simeoni M.C., de Mas P., Bieth E., Rogé B., Héron D., Burglen L., Gillberg C., Leboyer M., Bourgeron T. Mutations in the gene encoding the synaptic scaffolding protein SHANK3 are associated with autism spectrum disorders. Nat. Genet. 2007, 39:25-27.
22. Ehret G. Categorical perception of mouse-pup ultrasounds in the temporal domain. Anim. Behav. 1992, 43:409-416.
23. Ehret G., Haack B. Categorial perception of mouse pup ultrasound by lactating females. Naturwissenschaften 1981, 68:208.
24. Ehret G., Haack B. Ultrasound recognition in house mice: key-stimulus configuration and recognition mechanisms. J. Comp. Physiol. 1982, 148:245-251.
25. Ey E., Torquet N., Le Sourd A.M., Leblond C.S., Boeckers T.M., Faure P., Bourgeron T. The autism PROSAP1/Shank2 mouse model displays quantitative and structural abnormalities in ultrasonic vocalizations. Behev. Brain Res. 2013, 256:677-689.
26. Ey E., Yang M., Katz A.M., Woldeyohannes L., Silverman J.L., Leblond C.S., Faure P., Torquet N., Le Sourd A.M., Bourgeron T., Crawley J.N. Absence of deficits in social behaviors and ultrasonic vocalizations in later generations of mice lacking neuroligin4. Genes Brain Behav. 2012, 11:928-941.
27. Fish E.W., Faccidomo S., Gupta S., Miczek K.A. Anxiolytic-like effects of escitalopram, citalopram, and R-citalopram in maternally separated mouse pups. J. Pharmacol. Exp. Ther. 2004, 308:474-480.
28. Fish E.W., Sekinda M., Ferrari P.F., Dirks A., Miczek K.A. Distress vocalizations in maternally separated mouse pups: modulation via 5-HT(1A), 5-HT(1B) and GABA(A) receptors. Psychopharmacology (Berl) 2000, 149:277-285.
29. Folstein S., Rutter M. Genetic influences and infantile autism. Nature 1977, 265:726-728.
30. Frith U. Autism: Explaining the Enigma 2003, Blackwell Publishing, Oxford.
31. Gauthier J., Spiegelman D., Piton A., Lafrenière R.G., Laurent S., St-Onge J., Lapointe L., Hamdan F.F., Cossette P., Mottron L., Fombonne E., Joober R., Marineau C., Drapeau P., Rouleau G.A. Novel de novo SHANK3 mutation in autistic patients. Am. J. Med. Genet. B: Neuropsychiatr. Genet. 2009, 150:421-424.
32. Gauthier J., Champagne N., Lafrenière R.G., Xiong L., Spiegelman D., Brustein E., Lapointe M., Peng H., CÔté M., Noreau A., Hamdan F.F., Addington A.M., Rapoport J.L., Delisi L.E., Krebs M.O., Joober R., Fathalli F., Mouaffak F., Haghighi A.P., Néri C., Dubé M.P., Samuels M.E., Marineau C., Stone E.A., Awadalla P., Barker P.A., Carbonetto S., Drapeau P., Rouleau G.A. S2D Team, De novo mutations in the gene encoding the synaptic scaffolding protein SHANK3 in patients ascertained for schizophrenia. Proc. Natl. Acad. Sci. USA 2010, 107:7863-7868.
33. Gong X., Jiang Y.W., Zhang X., An Y., Zhang J., Wu Y., Wang J., Sun Y., Liu Y., Gao X., Shen Y., Wu X., Qiu Z., Jin L., Wu B.L., Wang H. High proportion of 22q13 deletions and SHANK3 mutations in Chinese patients with intellectual disability. PLoS ONE 2012, 7:e34739.
34. Grabrucker A.M., Schmeisser M.J., Schoen M., Boeckers T.M. Postsynaptic ProSAP/Shank scaffolds in the cross-hair of synaptopathies. Trends Cell Biol. 2011, 21:594-603.
35. Guilmatre A., Huguet G., Delorme R., Bourgeron T. The emerging role of SHANK genes in neuropsychiatric disorders. Dev. Neurobiol. 2014, 74:113-122.
36. Guo Z., Holy T.E. Sex selectivity of mouse ultrasonic songs. Chem. Senses 2007, 23:463-473.
37. Hamilton S.M., Spencer C.M., Harrison W.R., Yuva-Paylor L.A., Graham D.F., Daza R.A., Hevner R.F., Overbeek P.A., Paylor R. Multiple autism-like behaviors in a novel transgenic mouse model. Behav. Brain Res. 2011, 218:29-41.
38. Hammerschmidt K., Radyushkin K., Ehrenreich H., Fischer J. Female mice respond to male ultrasonic 'songs' with approach behaviour. Biol. Lett. 2009, 5:589-592.
39. Han K., Holder J.L., Schaaf C.P., Lu H., Chen H., Kang H., Tang J., Wu Z., Hao S., Cheung S.W., Yu P., Sun H., Breman A.M., Patel A., Lu H.C., Zoghbi H.Y. SHANK3 overexpression causes manic-like behaviour with unique pharmacogenetic properties. Nature 2013, 503:72-77.
40. Jiang Y.H., Ehlers M.D. Modeling autism by SHANK gene mutations in mice. Neuron 2013, 78:8-27.
41. Jones R.M., Lord C. Diagnosing autism in neurobiological research studies. Behav. Brain Res. 2013, 251:113-124.
42. Kanner L. Autistic disturbances of affective contact. Nervous Child 1943, 2:217-253.
43. Kim E., Sheng M. PDZ domain proteins of synapses. Nat. Rev. Neurosci. 2004, 5:771-781.
44. Kreienkamp H.J. Scaffolding proteins at the postsynaptic density: shank as the architectural framework. Handb. Exp. Pharmacol. 1983, 365-380.
45. Krömer S.A., Kessler M.S., Milfay D., Birg I.N., Bunck M., Czibere L., Panhuysen M., Pütz B., Deussing J.M., Holsboer F., Landgraf R., Turck C.W. Identification of glyoxalase-I as a protein marker in a mouse model of extremes in trait anxiety. J. Neurosci. 2005, 25:4375-4384.
46. Kouser M., Speed H.E., Dewey C.M., Reimers J.M., Widman A.J., Gupta N., Liu S., Jaramillo T.C., Bangash M., Xiao B., Worley P.F., Powell C.M. Loss of predominant Shank3 isoforms results in hippocampus-dependent impairments in behavior and synaptic transmission. J. Neurosci. 2013, 33:18448-18468.
47. Leblond C.S., Heinrich J., Delorme R., Proepper C., Betancur C., Huguet G., Konyukh M., Chaste P., Ey E., Rastam M., Anckarsäter H., Nygren G., Gillberg I.C., Melke J., Toro R., Regnault B., Fauchereau F., Mercati O., Lemière N., Skuse D., Poot M., Holt R., Monaco A.P., Järvelä I., Kantojärvi K., Vanhala R., Curran S., Collier D.A., Bolton P., Chiocchetti A., Klauck S.M., Poustka F., Freitag C.M., Waltes R., Kopp M., Duketis E., Bacchelli E., Minopoli F., Ruta L., Battaglia A., Mazzone L., Maestrini E., Sequeira A.F., Oliveira B., Vicente A., Oliveira G., Pinto D., Scherer S.W., Zelenika D., Delepine M., Lathrop M., Bonneau D., Guinchat V., Devillard F., Assouline B., Mouren M.C., Leboyer M., Gillberg C., Boeckers T.M., Bourgeron T. Genetic and functional analyses of SHANK2 mutations suggest a multiple hit model of autism spectrum disorders. PLoS Genet. 2012, 8:e1002521.
48. Liu H.X., Lopatina O., Higashida C., Fujimoto H., Akther S., Inzhutova A., Liang M., Zhong J., Tsuji T., Yoshihara T., Sumi K., Ishiyama M., Ma W.J., Ozaki M., Yagitani S., Yokoyama S., Mukaida N., Sakurai T., Hori O., Yoshioka K., Hirao A., Kato Y., Ishihara K., Kato I., Okamoto H., Cherepanov S.M., Salmina A.B., Hirai H., Asano M., Brown D.A., Nagano I., Higashida H. Displays of paternal mouse pup retrieval following communicative interaction with maternal mates. Nat. Commun. 2013, 4:1346.
49. Lord C., Luyster R.J., Gotham K., Guthrie W. Autism diagnostic observation schedule, second edition (ADOS-2) manual (part 2): toddler module 2012, Western Psychological Services, Torrence, CA.
50. Lord C., Rutter M., DiLavore P.C., Risi S., Gotham K., Bishop S.L. Autism diagnostic observation schedule, second edition (ADOS-2) manual (part 1): modules 1-4 2012, Western Psychological Services, Torrence, CA.
51. Maggio J.C., Maggio J.H., Whitney G. Experience-based vocalization of male mice to female chemosignals. Physiol. Behav. 1983, 31:269-272.
52. Marshall C.R., Noor A., Vincent J.B., Lionel A.C., Feuk L., Skaug J., Shago M., Moessner R., Pinto D., Ren Y., Thiruvahindrapduram B., Fiebig A., Schreiber S., Friedman J., Ketelaars C.E., Vos Y.J., Ficicioglu C., Kirkpatrick S., Nicolson R., Sloman L., Summers A., Gibbons C.A., Teebi A., Chitayat D., Weksberg R., Thompson A., Vardy C., Crosbie V., Luscombe S., Baatjes R., Zwaigenbaum L., Roberts W., Fernandez B., Szatmari P., Scherer S.W. Structural variation of chromosomes in autism spectrum disorder. Am. J. Hum. Genet. 2008, 82:477-488.
53. Meyza K.Z., Defensor E.B., Jensen A.L., Corley M.J., Pearson B.L., Pobbe R.L., Bolivar V.J., Blanchard D.C., Blanchard R.J. The BTBR T+ tf/J mouse model for autism spectrum disorders-in search of biomarkers. Behav. Brain Res. 2013, 251:25-34.
54. Michetti C., Ricceri L., Scattoni M.L. Modeling social communication deficits in mouse models of autism. Autism 2012, S1:007.
55. Moessner R., Marshall C.R., Sutcliffe J.S., Skaug J., Pinto D., Vincent J., Zwaigenbaum L., Fernandez B., Roberts W., Szatmari P., Scherer S.W. Contribution of SHANK3 mutations to autism spectrum disorder. Am. J. Hum. Genet. 2007, 81:1289-1297.
56. Moles A., Kieffer B.L., D'Amato F.R. Deficit in attachment behavior in mice lacking the mu-opioid receptor gene. Science 2004, 304:1983-1986.
57. Musolf K., Hoffmann F., Penn D.J. Ultrasonic courtship vocalizations in wild house mice Mus musculus. Anim. Behav. 2010, 79:757-764.
58. Naisbitt S., Kim E., Tu J.C., Xiao B., Sala C., Valtschanoff J., Weinberg R.J., Worley P.F., Sheng M. Shank, a novel family of postsynaptic density proteins that binds to the NMDA receptor/PSD-95/GKAP complex and cortactin. Neuron 1999, 23:569-582.
59. Nastiti K., Benton D., Brain P.F. The effects of compounds acting at the benzodiazepine receptor complex on the ultrasonic calling of mouse pups. Behav. Pharmacol. 1991, 2:121-128.
60. Nyby J. Ultrasonic vocalizations during sex behavior of male house mice (Mus musculus): a description. Behav. Neural Biol. 1983, 39:128-134.
61. Nyby J., Bigelow J., Kerchner M., Barbehenn F. Male mouse (Mus musculus) ultrasonic vocalizations to female urine: why is heterosexual experience necessary?. Behav. Neural Biol. 1983, 38:32-46.
62. Panksepp J.B., Jochman K.A., Kim J.U., Koy J.J., Wilson E.D., Chen Q., Wilson C.R., Lahvis G.P. Affiliative behavior, ultrasonic communication and social reward are influenced by genetic variation in adolescent mice. PLoS ONE 2007, 2:e351.
63. Peça J., Feliciano C., Ting J.T., Wang W., Wells M.F., Venkatraman T.N., Lascola C.D., Fu Z., Feng G. Shank3 mutant mice display autistic-like behaviours and striatal dysfunction. Nature 2011, 472:437-442.
64. Phelan M.C. Deletion 22q13.3 syndrome. Orphanet J. Rare Dis. 2008, 3:14.
65. Pinto D., Pagnamenta A.T., Klei L., Anney R., Merico D., Regan R., Conroy J., Magalhaes T.R., Correia C., Abrahams B.S., Almeida J., Bacchelli E., Bader G.D., Bailey A.J., Baird G., Battaglia A., Berney T., Bolshakova N., Bölte S., Bolton P.F., Bourgeron T., Brennan S., Brian J., Bryson S.E., Carson A.R., Casallo G., Casey J., Chung B.H., Cochrane L., Corsello C., Crawford E.L., Crossett A., Cytrynbaum C., Dawson G., de Jonge M., Delorme R., Drmic I., Duketis E., Duque F., Estes A., Farrar P., Fernandez B.A., Folstein S.E., Fombonne E., Freitag C.M., Gilbert J., Gillberg C., Glessner J.T., Goldberg J., Green A., Green J., Guter S.J., Hakonarson H., Heron E.A., Hill M., Holt R., Howe J.L., Hughes G., Hus V., Igliozzi R., Kim C., Klauck S.M., Kolevzon A., Korvatska O., Kustanovich V., Lajonchere C.M., Lamb J.A., Laskawiec M., Leboyer M., Le Couteur A., Leventhal B.L., Lionel A.C., Liu X.Q., Lord C., Lotspeich L., Lund S.C., Maestrini E., Mahoney W., Mantoulan C., Marshall C.R., McConachie H., McDougle C.J., McGrath J., McMahon W.M., Merikangas A., Migita O., Minshew N.J., Mirza G.K., Munson J., Nelson S.F., Noakes C., Noor A., Nygren G., Oliveira G., Papanikolaou K., Parr J.R., Parrini B., Paton T., Pickles A., Pilorge M., Piven J., Ponting C.P., Posey D.J., Poustka A., Poustka F., Prasad A., Ragoussis J., Renshaw K., Rickaby J., Roberts W., Roeder K., Roge B., Rutter M.L., Bierut L.J., Rice J.P., Salt J., Sansom K., Sato D., Segurado R., Sequeira A.F., Senman L., Shah N., Sheffield V.C., Soorya L., Sousa I., Stein O., Sykes N., Stoppioni V., Strawbridge C., Tancredi R., Tansey K., Thiruvahindrapduram B., Thompson A.P., Thomson S., Tryfon A., Tsiantis J., Van Engeland H., Vincent J.B., Volkmar F., Wallace S., Wang K., Wang Z., Wassink T.H., Webber C., Weksberg R., Wing K., Wittemeyer K., Wood S., Wu J., Yaspan B.L., Zurawiecki D., Zwaigenbaum L., Buxbaum J.D., Cantor R.M., Cook E.H., Coon H., Cuccaro M.L., Devlin B., Ennis S., Gallagher L., Geschwind D.H., Gill M., Haines J.L., Hallmayer J., Miller J., Monaco A.P., Nurnberger J.I., Paterson A.D., Pericak-Vance M.A., Schellenberg G.D., Szatmari P., Vicente A.M., Vieland V.J., Wijsman E.M., Scherer S.W., Sutcliffe J.S., Betancur C. Functional impact of global rare copy number variation in autism spectrum disorders. Nature 2010, 466:368-372.
66. Pomerantz S.M., Nunez A.A., Bean N.J. Female behavior is affected by male ultrasonic vocalizations in house mice. Physiol. Behav. 1983, 31:91-96.
67. Posthuma D., Polderman T.J. What have we learned from recent twin studies about the etiology of neurodevelopmental disorders?. Curr. Opin. Neurol. 2013, 26:111-121.
68. Robinson D.J., D'Udine B. Ultrasonic calls produced by three laboratory strains of Mus musculus. J. Zool. Lond. 1982, 197:383-389.
69. Roullet F.I., Wöhr M., Crawley J.N. Female urine-induced male mice ultrasonic vocalizations, but not scent-marking, is modulated by social experience. Behav. Brain Res. 2011, 216:19-28.
70. Rowlett J.K., Tornatzky W., Cook J.M., Ma C., Miczek K.A. Zolpidem, triazolam, and diazepam decrease distress vocalizations in mouse pups: differential antagonism by flumazenil and beta-Carboline-3-carboxylate-t-butyl ester (beta-CCt). J. Pharmacol. Exp. Ther. 2001, 297:247-253.
71. Sales G.D. Ultrasound and aggressive behaviour in rats and other small mammals. Anim. Behav. 1972, 20:88-100.
72. Sato D., Lionel A.C., Leblond C.S., Prasad A., Pinto D., Walker S., O'Connor I., Russell C., Drmic I.E., Hamdan F.F., Michaud J.L., Endris V., Roeth R., Delorme R., Huguet G., Leboyer M., Rastam M., Gillberg C., Lathrop M., Stavropoulos D.J., Anagnostou E., Weksberg R., Fombonne E., Zwaigenbaum L., Fernandez B.A., Roberts W., Rappold G.A., Marshall C.R., Bourgeron T., Szatmari P., Scherer S.W. SHANK1 deletions in males with autism spectrum disorder. Am. J. Hum. Genet. 2012, 90:879-887.
73. Scattoni M.L., Crawley J., Ricceri L. Ultrasonic vocalizations: a tool for behavioural phenotyping of mouse models of neurodevelopmental disorders. Neurosci. Biobehav. Rev. 2009, 33:508-515.
74. Scattoni M.L., Gandhy S.U., Ricceri L., Crawely J.N. Unusual repertoire of vocalizations in the BTBR T+tf/J mouse model of autism. PLoS ONE 2008, 3:e3067.
75. Scattoni M.L., Martire A., Cartocci G., Ferrante A., Ricceri L. Reduced social interaction, behavioural flexibility and BDNF signalling in the BTBR T+ tf/J strain, a mouse model of autism. Behav. Brain Res. 2013, 251:35-40.
76. Schaaf C.P., Sabo A., Sakai Y., Crosby J., Muzny D., Hawes A., Lewis L., Akbar H., Varghese R., Boerwinkle E., Gibbs R.A., Zoghbi H.Y. Oligogenic heterozygosity in individuals with high-functioning autism spectrum disorders. Hum. Mol. Genet. 2011, 20:3366-3375.
77. Schmeisser M.J., Ey E., Wegener S., Bockmann J., Stempel A.V., Kuebler A., Janssen A.L., Udvardi P.T., Shiban E., Spilker C., Balschun D., Skryabin B.V., Dieck St, Smalla K.H., Montag D., Leblond C.S., Faure P., Torquet N., Le Sourd A.M., Toro R., Grabrucker A.M., Shoichet S.A., Schmitz D., Kreutz M.R., Bourgeron T., Gundelfinger E.D., Boeckers T.M. Autistic-like behaviours and hyperactivity in mice lacking ProSAP1/Shank2. Nature 2012, 486:256-260.
78. Sewell G.D. Ultrasound in adult rodents. Nature 1967, 215:512.
79. Sewell G.D. Ultrasonic communication in rodents. Nature 1970, 227:410.
80. Sheng M., Kim E. The Shank family of scaffold proteins. J. Cell Sci. 2000, 113:1851-1856.
81. Silverman J.L., Yang M., Lord C., Crawley J.N. Behavioural phenotyping assays for mouse models of autism. Nat. Rev. Neurosci. 2010, 11:490-502.
82. State M.W. The genetics of child psychiatric disorders: focus on autism and Tourette syndrome. Neuron 2010, 68:254-269.
83. Ssucharewa G.E. Die schizoiden Psychopathien im Kindesalter. Monatsschrift für Psychiatrie und Neurologie 1926, 60:235-261.
84. Takahashi A., Yap J.J., Bohager D.Z., Faccidomo S., Clayton T., Cook J.M., Miczek K.A. Glutamatergic and GABAergic modulations of ultrasonic vocalizations during maternal separation distress in mouse pups. Psychopharmacology (Berl) 2009, 204:61-71.
85. Ting J.T., Peça J., Feng G. Functional consequences of mutations in postsynaptic scaffolding proteins and relevance to psychiatric disorders. Annu. Rev. Neurosci. 2012, 35:49-71.
86. White S.W., Oswald D., Ollendick T., Scahill L. Anxiety in children and adolescents with autism spectrum disorders. Clin. Psychol. Rev. 2009, 29:216-229.
87. Whitney G., Coble J.R., Stockton M.D., Tilson E.T. Ultrasonic emissions: do they facilitate courtship of mice?. J. Comp. Physiol. Psychol. 1973, 84:445-452.
88. Whitney G., Alpern M., Dizinno G., Horowitz G. Female odors evoke ultrasounds from male mice. Anim. Learn. Behav. 1974, 2:13-18.
89. Waga C., Okamoto N., Ondo Y., Fukumura-Kato R., Goto Y., Kohsaka S., Uchino S. Novel variants of the SHANK3 gene in Japanese autistic patients with severe delayed speech development. Psychiatr. Genet. 2011, 21:208-211.
90. Wang X., McCoy P.A., Rodriguiz R.M., Pan Y., Je H.S., Roberts A.C., Kim C.J., Berrios J., Colvin J.S., Bousquet-Moore D., Lorenzo I., Wu G., Weinberg R.J., Ehlers M.D., Philpot B.D., Beaudet A.L., Wetsel W.C., Jiang Y.H. Synaptic dysfunction and abnormal behaviors in mice lacking major isoforms of Shank3. Hum. Mol. Genet. 2011, 20:3093-3108.
91. Wilson H.L., Wong A.C., Shaw S.R., Tse W.Y., Stapleton G.A., Phelan M.C., Hu S., Marshall J., McDermid H.E. Molecular characterisation of the 22q13 deletion syndrome supports the role of haploinsufficiency of SHANK3/PROSAP2 in the major neurological symptoms. J. Med. Genet. 2003, 40:575-584.
92. Wöhr M., Dahlhoff M., Wolf E., Holsboer F., Schwarting R.K.W., Wotjak C.T. Effects of genetic background, gender, and early environmental factors on isolation-induced ultrasonic calling in mouse pups: an embryo-transfer study. Behav. Genet. 2008, 38:579-595.
93. Wöhr M., Oddi D., D'Amato Effects of altricial pup ultrasonic vocalization on maternal behavior. Handbook of Mammalian Vocalization. An Integrative Neuroscience Approach 2009, 159-166. Elsevier. S.M. Brudzynski (Ed.).
94. Wöhr M., Moles A., Schwarting R.K., D'Amato F.R. Lack of social exploratory activation in male μ-opioid receptor KO mice in response to playback of female ultrasonic vocalizations. Soc. Neurosci. 2011, 6:76-87.
95. Wöhr M., Roullet F.I., Hung A.Y., Sheng M., Crawley J.N. Communication impairments in mice lacking Shank1: reduced levels of ultrasonic vocalizations and scent marking behavior. PLoS ONE 2011, 6:e20631.
96. Won H., Lee H.R., Gee H.Y., Mah W., Kim J.I., Lee J., Ha S., Chung C., Jung E.S., Cho Y.S., Park S.G., Lee J.S., Lee K., Kim D., Bae Y.C., Kaang B.K., Lee M.G., Kim E. Autistic-like social behaviour in Shank2-mutant mice improved by restoring NMDA receptor function. Nature 2012, 486:261-265.
97. Yang M., Bozdagi O., Scattoni M.L., Wöhr M., Roullet F.I., Katz A.M., Abrams D.N., Kalikhman D., Simon H., Woldeyohannes L., Zhang J.Y., Harris M.J., Saxena R., Silverman J.L., Buxbaum J.D., Crawley J.N. Reduced excitatory neurotransmission and mild autism-relevant phenotypes in adolescent Shank3 null mutant mice. J. Neurosci. 2012, 32:6525-6541.
98. Yang M., Loureiro D., Kalikhman D., Crawley J.N. Male mice emit distinct ultrasonic vocalizations when the female leaves the social interaction arena. Front. Behav. Neurosci. 2013, 7:159.
99. Zippelius H.M., Schleidt W.M. Ultraschall-Laute bei jungen Mäusen. Naturwissenschaften 1956, 43:502.