A Foxp2 mutation implicated in human speech deficits alters sequencing of ultrasonic vocalizations in adult male mice

Frontiers in Behavioral Neuroscience

Volumn 10, Issue OCT, 2016, Pages

  Chabout, Jonathan ^a,b   Sarkar, Abhra ^c   Patel, Sheel R ^a   Radden, Taylor ^a   Dunson, David B ^c   Fisher, Simon E ^d,e   Jarvis, Erich D ^a,b,f  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c Duke University   (United States)

^d MAX PLANCK INSTITUTE FOR PSYCHOLINGUISTICS   (Netherlands)

^e RADBOUD UNIVERSITY   (Netherlands)

^f ROCKEFELLER UNIVERSITY   (United States)

Author keywords

FoxP2; KE family; Song; Speech apraxia; Syntax; Ultrasonic vocalizations

Indexed keywords

TRANSCRIPTION FACTOR FOXP2;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUDITORY THRESHOLD; CONTROLLED STUDY; FEMALE; FOXP2 GENE; GENE MUTATION; GENE SEQUENCE; GENETIC ASSOCIATION; HETEROZYGOSITY; LARYNGEAL MOTOR CORTEX; LUNG GAS EXCHANGE; MALE; MOTOR CORTEX; MOUSE; NEUROPATHOLOGY; NONHUMAN; OXYGEN CONSUMPTION; SEQUENCE ANALYSIS; SOCIAL ENVIRONMENT; SPEECH DISORDER; VOCALIZATION; WHITE NOISE;

EID: 84992561349     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2016.00197     Document Type: Article

References (69)

1. Arriaga, G., and Jarvis, E. D. (2013). Mouse vocal communication system: are ultrasounds learned or innate? Brain Lang. 124, 96–116. doi: 10.1016/j.bandl.2012.10.002
2. Arriaga, G., Macopson, J. J., and Jarvis, E. D. (2015). Transsynaptic tracing from peripheral targets with pseudorabies virus followed by cholera toxin and biotinylated dextran amines double labeling. J. Vis. Exp. 103:e50672. doi: 10.3791/50672
3. Arriaga, G., Zhou, E. P., and Jarvis, E. D. (2012). Of mice, birds, and men: the mouse ultrasonic song system has some features similar to humans and song-learning birds. PloS ONE 7:e46610. doi: 10.1371/journal.pone.0046610
4. Bacon, C., and Rappold, G. A. (2012). The distinct and overlapping phenotypic spectra of FOXP1 and FOXP2 in cognitive disorders. Hum. Genet. 131, 1687–1698. doi: 10.1007/s00439-012-1193-z
5. Bishop, D. V., North, T., and Donlan, C. (1995). Genetic basis of specific language impairment: evidence from a twin study. Dev. Med. Child Neurol. 37, 56–71. doi: 10.1111/j.1469-8749.1995.tb11932.x
6. Campbell, P., Reep, R. L., Stoll, M. L., Ophir, A. G., and Phelps, S. M. (2009). Conservation and diversity of Foxp2 expression in muroid rodents: functional implications. J. Comp. Neurol. 512, 84–100. doi: 10.1002/cne.21881
7. Card, J. P., and Enquist, L. W. (2001). Transneuronal circuit analysis with pseudorabies viruses. Curr. Protoc. Neurosci. Chapter 1:Unit1.5. doi: 10.1002/0471142301.ns0105s09
8. Castellucci, G. A., McGinley, M. J., and McCormick, D. A. (2016). Knockout of Foxp2 disrupts vocal development in mice. Sci. Rep. 6:23305. doi: 10.1038/srep23305
9. Chabout, J., Macopson, J. J., and Jarvis, E. D. (in press). Eliciting Analyzing Male Mouse Ultrasonic Vocalization (USV) Songs. JoVE.
10. Chabout, J., Sarkar, A., Dunson, D. B., and Jarvis, E. D. (2015). Male mice song syntax depends on social contexts and influences female preferences. Front. Behav. Neurosci. 9:76. doi: 10.3389/fnbeh.2015.00076
11. Deriziotis, P., and Fisher, S. E. (2013). Neurogenomics of speech and language disorders: the road ahead. Genome Biol. 14:204. doi: 10.1186/gb-2013-14-4-204
12. Fee, M. S., Kozhevnikov, A. A., and Hahnloser, R. H. (2004). Neural mechanisms of vocal sequence generation in the songbird. Ann. N.Y Acad. Sci. 1016, 153–170. doi: 10.1196/annals.1298.022
13. Ferland, R. J., Cherry, T. J., Preware, P. O., Morrisey, E. E., and Walsh, C. A. (2003). Characterization of Foxp2 and Foxp1 mRNA and protein in the developing and mature brain. J. Comp. Neurol. 460, 266–279. doi: 10.1002/cne.10654
14. Fisher, S. E., Lai, C. S., and Monaco, A. P. (2003). Deciphering the genetic basis of speech and language disorders. Annu. Rev. Neurosci. 26, 57–80. doi: 10.1146/annurev.neuro.26.041002.131144
15. Fisher, S. E., and Marcus, G. F. (2006). The eloquent ape: genes, brains and the evolution of language. Nat. Rev. Genet. 7, 9–20. doi: 10.1038/nrg1747
16. Fisher, S. E., and Scharff, C. (2009). FOXP2 as a molecular window into speech and language. Trends Genet. 25, 166–177. doi: 10.1016/j.tig.2009.03.002
17. Fisher, S. E., Vargha-Khadem, F., Watkins, K. E., Monaco, A. P., and Pembrey, M. E. (1998). Localisation of a gene implicated in a severe speech and language disorder. Nat. Genet. 18, 168–170. doi: 10.1038/ng0298-168
18. French, C. A., and Fisher, S. E. (2014). What can mice tell us about Foxp2 function? Curr. Opin. Neurobiol. 28, 72–79. doi: 10.1016/j.conb.2014.07.003
19. French, C. A., Groszer, M., Preece, C., Coupe, A. M., Rajewsky, K., and Fisher, S. E. (2007). Generation of mice with a conditional Foxp2 null allele. Genesis 45, 440–446. doi: 10.1002/dvg.20305
20. French, C. A., Jin, X., Campbell, T. G., Gerfen, E., Groszer, M., Fisher, S. E., et al. (2012). An aetiological Foxp2 mutation causes aberrant striatal activity and alters plasticity during skill learning. Mol. Psychiatry 17, 1077–1085. doi: 10.1038/mp.2011.105
21. Fujita, E., Tanabe, Y., Shiota, A., Ueda, M., Suwa, K., Momoi, M. Y., et al. (2008). Ultrasonic vocalization impairment of Foxp2 (R552H) knockin mice related to speech-language disorder and abnormality of Purkinje cells. Proc. Natl. Acad. Sci. U.S.A. 105, 3117–3122. doi: 10.1073/pnas.0712298105
22. Fujita, H., and Sugihara, I. (2012). FoxP2 expression in the cerebellum and inferior olive: development of the transverse stripe-shaped expression pattern in the mouse cerebellar cortex. J. Comp. Neurol. 520, 656–677. doi: 10.1002/cne.22760
23. Garcia-Calero, E., Botella-Lopez, A., Bahamonde, O., Perez-Balaguer, A., and Martinez, S. (2016). FoxP2 protein levels regulate cell morphology changes and migration patterns in the vertebrate developing telencephalon. Brain Struct. Funct. 221, 2905–2917. doi: 10.1007/s00429-015-1079-7
24. Gaub, S., Fisher, S. E., and Ehret, G. (2016). Ultrasonic vocalizations of adult male Foxp2-mutant mice: behavioral contexts of arousal and emotion. Genes Brain Behav. 15, 243–259. doi: 10.1111/gbb.12274
25. Gaub, S., Groszer, M., Fisher, S. E., and Ehret, G. (2010). The structure of innate vocalizations in Foxp2-deficient mouse pups. Genes Brain Behav. 9, 390–401. doi: 10.1111/j.1601-183X.2010.00570.x
26. Graham, S. A., and Fisher, S. E. (2013). Decoding the genetics of speech and language. Curr. Opin. Neurobiol. 23, 43–51. doi: 10.1016/j.conb.2012.11.006
27. Grimsley, J. M. S., Monaghan, J. J. M., and Wenstrup, J. J. (2011). Development of social vocalizations in mice. PloS ONE 6:e17460. doi: 10.1371/journal.pone.0017460
28. Groszer, M., Keays, D. A., Deacon, R. M., de Bono, J. P., Prasad-Mulcare, S., Gaub, S., et al. (2008). Impaired synaptic plasticity and motor learning in mice with a point mutation implicated in human speech deficits. Curr. Biol. 18, 354–362. doi: 10.1016/j.cub.2008.01.060
29. Haesler, S., Rochefort, C., Georgi, B., Licznerski, P., Osten, P., and Scharff, C. (2007). Incomplete and inaccurate vocal imitation after knockdown of FoxP2 in songbird basal ganglia nucleus Area, X. PLoS Biol. 5:e321. doi: 10.1371/journal.pbio.0050321
30. Haesler, S., Wada, K., Nshdejan, A., Morrisey, E. E., Lints, T., Jarvis, E. D., et al. (2004). FoxP2 expression in avian vocal learners and non-learners. J. Neurosci. 24, 3164–3175. doi: 10.1523/JNEUROSCI.4369-03.2004
31. Hahnloser, R. H. R., Kozhevnikov, A. A., and Fee, M. S. (2002). An ultra-sparse code underlies the generation of neural sequences in a songbird. Nature 419, 65–70. doi: 10.1038/nature00974
32. Hammerschmidt, K., Reisinger, E., Westekemper, K., Ehrenreich, L., Strenzke, N., and Fischer, J. (2012). Mice do not require auditory input for the normal development of their ultrasonic vocalizations. BMC Neurosci. 13:40. doi: 10.1186/1471-2202-13-40
33. Hammerschmidt, K., Whelan, G., Eichele, G., and Fischer, J. (2015). Mice lacking the cerebral cortex develop normal song: insights into the foundations of vocal learning. Sci. Rep. 5:8808. doi: 10.1038/srep08808
34. Hinckley, C. A., Alaynick, W. A., Gallarda, B. W., Hayashi, M., Hilde, K. L., Driscoll, S. P., et al. (2015). Spinal locomotor circuits develop using hierarchical rules based on motorneuron position and identity. Neuron 87, 1008–1021. doi: 10.1016/j.neuron.2015.08.005
35. Hisaoka, T., Nakamura, Y., Senba, E., and Morikawa, Y. (2010). The forkhead transcription factors, Foxp1 and Foxp2, identify different subpopulations of projection neurons in the mouse cerebral cortex. Neuroscience 166, 551–563. doi: 10.1016/j.neuroscience.2009.12.055
36. Holy, T. E., and Guo, Z. (2005). Ultrasonic songs of male mice. PLoS Biol. 3, 2177–2186. doi: 10.1371/journal.pbio.0030386
37. Hurst, J. A., Baraitser, M., Auger, E., Graham, F., and Norell, S. (1990). An extended family with a dominantly inherited speech disorder. Dev. Med. Child Neurol. 32, 352–355. doi: 10.1111/j.1469-8749.1990.tb16948.x
38. Jarvis, E. D., Scharff, C., Grossman, M. R., Ramos, J. A., and Nottebohm, F. (1998). For whom the bird sings: context-dependent gene expression. Neuron 21, 775–788. doi: 10.1016/S0896-6273(00)80594-2
39. Jin, X., and Costa, R. M. (2015). Shaping action sequences in basal ganglia circuits. Curr. Opin. Neurobiol. 33, 188–196. doi: 10.1016/j.conb.2015.06.011
40. Kikusui, T., Nakanishi, K., Nakagawa, R., Nagasawa, M., Mogi, K., and Okanoya, K. (2011). Cross fostering experiments suggest that mice songs are innate. PLoS ONE 6:e17721. doi: 10.1371/journal.pone.0017721
41. Kubikova, L., Turner, E. A., and Jarvis, E. D. (2007). The pallial basal ganglia pathway modulates the behaviorally driven gene expression of the motor pathway. Eur. J. Neurosci. 25, 2145–2160. doi: 10.1111/j.1460-9568.2007.05368.x
42. Lai, C. S., Fisher, S. E., Hurst, J. A., Vargha-Khadem, F., and Monaco, A. P. (2001). A forkhead-domain gene is mutated in a severe speech and language disorder. Nature 413, 519–523. doi: 10.1038/35097076
43. Lai, C. S., Gerrelli, D., Monaco, A. P., Fisher, S. E., and Copp, A. J. (2003). FOXP2 expression during brain development coincides with adult sites of pathology in a severe speech and language disorder. Brain 126, 2455–2462. doi: 10.1093/brain/awg247
44. Law, J., Boyle, J., Harris, F., Harkness, A., and Nye, C. (2000). Prevalence and natural history of primary speech and language delay: findings from a systematic review of the literature. Int. J. Lang. Commun. Disord. 35, 165–188. doi: 10.1080/136828200247133
45. Liégeois, F., Baldeweg, T., Connelly, A., Gadian, D. G., Mishkin, M., and Vargha-Khadem, F. (2003). Language fMRI abnormalities associated with FOXP2 gene mutation. Nat. Neurosci. 6, 1230–1237. doi: 10.1038/nn1138
46. Liu, W. C., Wada, K., Jarvis, E. D., and Nottebohm, F. (2013). Rudimentary substrates for vocal learning in a suboscine. Nat. Commun. 4, 2082. doi: 10.1038/ncomms3082
47. Mahrt, E. J., Perkel, D. J., Tong, L., Rubel, E. W., and Portfors, C. V. (2013). Engineered deafness reveals that mouse courtship vocalizations do not require auditory experience. J. Neurosci. 33, 5573–5583. doi: 10.1523/JNEUROSCI.5054-12.2013
48. Murugan, M., Harward, S., Scharff, C., and Mooney, R. (2013). Diminished FoxP2 levels affect dopaminergic modulation of corticostriatal signaling important to song variability. Neuron 80, 1464–1476. doi: 10.1016/j.neuron.2013.09.021
49. Neunuebel, J. P., Taylor, A. L., Arthur, B. J., and Egnor, S. E. (2015). Female mice ultrasonically interact with males during courtship displays. Elife 4:e06203. doi: 10.7554/eLife.06203
50. NIDCD (2010). Statistics about Voice, Speech and Language. NIDCD (NIH) Report. Available online at: https://www.nidcd.nih.gov/health/statistics/statistics-voice-speech-and-language
51. Okobi, J. D. E., Phelps, S. M., and Long, M. A. (2013). Cortical Modules Contribute to Stereotyped Vocalizations in a Tropical Rodent. San Diego, CA: Society for Neuroscience.
52. Petkov, C. I., and Jarvis, E. D. (2012). Birds, primates, and spoken language origins: behavioral phenotypes and neurobiological substrates. Front. Evol. Neurosci. 4:12. doi: 10.3389/fnevo.2012.00012
53. Pfenning, A. R., Hara, E., Whitney, O., Rivas, M. V., Wang, R., Roulhac, P. L., et al. (2014). Convergent transcriptional specializations in the brains of humans and song-learning birds. Science 346:1256846. doi: 10.1126/science.1256846
54. Portfors, C. V., and Perkel, D. J. (2014). The role of ultrasonic vocalizations in mouse communication. Curr. Opin. Neurobiol. 28C, 115–120. doi: 10.1016/j.conb.2014.07.002
55. R Development Core Team (2011). R: A Language and Environment for Statistical Computing. Vienna: The R Foundation for Statistical Computing. Available online at: http://www.R-project.org/
56. Shriberg, L. D., Tomblin, J. B., and McSweeny, J. L. (1999). Prevalence of speech delay in 6-year-old children and comorbidity with language impairment. J. Speech Lang. Hear. Res. 42, 1461–1481. doi: 10.1044/jslhr.4206.1461
57. Shu, W., Cho, J. Y., Jiang, Y., Zhang, M., Weisz, D., Elder, G. A., et al. (2005). Altered ultrasonic vocalization in mice with a disruption in the Foxp2 gene. Proc. Natl. Acad. Sci. U.S.A. 102, 9643–9648. doi: 10.1073/pnas.0503739102
58. Simmonds, A. J., Leech, R., Iverson, P., and Wise, R. J. (2014). The response of the anterior striatum during adult human vocal learning. J. Neurophysiol. 112, 792–801. doi: 10.1152/jn.00901.2013
59. Smith, B. N., Banfield, B. W., Smeraski, C. A., Wilcox, C. L., Dudek, F. E., Enquist, L. W., et al. (2000). Pseudorabies virus expressing enhanced green fluorescent protein: a tool for in vitro electrophysiological analysis of transsynaptically labeled neurons in identified central nervous system circuits. Proc. Natl. Acad. Sci. U.S.A. 97, 9264–9269. doi: 10.1073/pnas.97.16.9264
60. Tanji, J. (2001). Sequential organization of multiple movements: involvement of cortical motor areas. Annu. Rev. Neurosci. 24, 631–651. doi: 10.1146/annurev.neuro.24.1.631
61. Teramitsu, I., Kudo, L. C., London, S. E., Geschwind, D. H., and White, S. A. (2004). Parallel FoxP1 and FoxP2 expression in songbird and human brain predicts functional interaction. J. Neurosci. 24, 3152–3163. doi: 10.1523/JNEUROSCI.5589-03.2004
62. Teramitsu, I., and White, S. A. (2006). FoxP2 regulation during undirected singing in adult songbirds. J. Neurosci. 26, 7390–7394. doi: 10.1523/JNEUROSCI.1662-06.2006
63. Thupari, J. N., Landree, L. E., Ronnett, G. V., and Kuhajda, F. P. (2002). C75 increases peripheral energy utilization and fatty acid oxidation in diet-induced obesity. Proc. Natl. Acad. Sci. U.S.A. 99, 9498–9502. doi: 10.1073/pnas.132128899
64. Turner, S. J., Hildebrand, M. S., Block, S., Damiano, J., Fahey, M., Reilly, S., et al. (2013). Small intragenic deletion in FOXP2 associated with childhood apraxia of speech and dysarthria. Am. J. Med. Genet. A 161A, 2321–2326. doi: 10.1002/ajmg.a.36055
65. Vernes, S. C., Nicod, J., Elahi, F. M., Coventry, J. A., Kenny, N., Coupe, A. M., et al. (2006). Functional genetic analysis of mutations implicated in a human speech and language disorder. Hum. Mol. Genet. 15, 3154–3167. doi: 10.1093/hmg/ddl392
66. Vernes, S. C., Oliver, P. L., Spiteri, E., Lockstone, H. E., Puliyadi, R., Taylor, J. M., et al. (2011). Foxp2 regulates gene networks implicated in neurite outgrowth in the developing brain. PLoS Genet. 7:e1002145. doi: 10.1371/journal.pgen.1002145
67. Watkins, K. E., Dronkers, N. F., and Vargha-Khadem, F. (2002a). Behavioural analysis of an inherited speech and language disorder: comparison with acquired aphasia. Brain 125, 452–464. doi: 10.1093/brain/awf058
68. Watkins, K. E., Vargha-Khadem, F., Ashburner, J., Passingham, R. E., Connelly, A., Friston, K. J., et al. (2002b). Analysis of an inherited speech and language disorder: structural brain abnormalities. Brain 125, 465–478. doi: 10.1093/brain/awf057
69. Zaykin, D. V., Zhivotovsky, L. A., Westfall, P. H., and Weir, B. S. (2002). Truncated product method for combining P-values. Genet. Epidemiol. 22, 170–185. doi: 10.1002/gepi.0042