Degraded neural and behavioral processing of speech sounds in a rat model of Rett syndrome

Neurobiology of Disease

Volumn 83, Issue , 2015, Pages 26-34

  Engineer, Crystal T ^a   Rahebi, Kimiya C ^a   Borland, Michael S ^a   Buell, Elizabeth P ^a   Centanni, Tracy M ^a   Fink, Melyssa K ^a   Im, Kwok W ^a   Wilson, Linda G ^a   Kilgard, Michael P ^a  

^a UNIVERSITY OF TEXAS AT DALLAS   (United States)

Author keywords

Auditory processing; Cortex; Mecp2; Plasticity; Rett syndrome; Speech therapy

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUDITORY CORTEX; BRAIN DEPTH STIMULATION; BRAIN FUNCTION; CONSONANT; CONTROLLED STUDY; FEMALE; HEARING IMPAIRMENT; KNOCKOUT RAT; MENTAL CAPACITY; MENTAL TASK; NERVE CELL PLASTICITY; NERVE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; RAT; RETT SYNDROME; SOUND DETECTION; SPEECH DISCRIMINATION; SPEECH SOUND DISORDER; SPEECH THERAPY; VOWEL; ANIMAL; AUDITORY EVOKED POTENTIAL; AUDITORY STIMULATION; DISEASE MODEL; GENE INACTIVATION; GENETICS; HEARING; NERVE CELL; NOISE; PATHOPHYSIOLOGY; PERCEPTIVE DISCRIMINATION; PHONETICS; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

MECP2 PROTEIN, MOUSE; METHYL CPG BINDING PROTEIN 2;

ACOUSTIC STIMULATION; ANIMALS; AUDITORY CORTEX; AUDITORY PERCEPTION; DISCRIMINATION (PSYCHOLOGY); DISEASE MODELS, ANIMAL; EVOKED POTENTIALS, AUDITORY; FEMALE; GENE KNOCKOUT TECHNIQUES; METHYL-CPG-BINDING PROTEIN 2; NEURONS; NOISE; PHONETICS; RATS; RATS, SPRAGUE-DAWLEY; RETT SYNDROME;

EID: 84941009691     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2015.08.019     Document Type: Article

References (53)

1. Amir R.E., Van den Veyver I.B., Wan M., Tran C.Q., Francke U., Zoghbi H.Y. Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2. Nat. Genet. 1999, 23:185-188.
2. Bader G.G., Witt-Engerström I., Hagberg B. Neurophysiological findings in the Rett syndrome, II: visual and auditory brainstem, middle and late evoked responses. Brain Dev. 1989, 11:110-114.
3. Beauchemin M., De Beaumont L., Vannasing P., Turcotte A., Arcand C., Belin P., Lassonde M. Electrophysiological markers of voice familiarity. Eur. J. Neurosci. 2006, 23:3081-3086.
4. Beauchemin M., González-Frankenberger B., Tremblay J., Vannasing P., Martínez-Montes E., Belin P., Béland R., Francoeur D., Carceller A.M., Wallois F., Lassonde M. Mother and stranger: an electrophysiological study of voice processing in newborns. Cereb. Cortex 2011, 21:1705-1711.
5. Centanni T.M., Chen F., Booker A.M., Engineer C.T., Sloan A.M., Rennaker R.L., LoTurco J.J., Kilgard M.P. Speech sound processing deficits and training-induced neural plasticity in rats with dyslexia gene knockdown. PLoS One 2014, 9.
6. Chahrour M., Zoghbi H.Y. The story of Rett syndrome: from clinic to neurobiology. Neuron 2007, 56:422-437.
7. Chao H.-T., Chen H., Samaco R.C., Xue M., Chahrour M., Yoo J., Neul J.L., Gong S., Lu H.-C., Heintz N., Ekker M., Rubenstein J.L.R., Noebels J.L., Rosenmund C., Zoghbi H.Y. Dysfunction in GABA signalling mediates autism-like stereotypies and Rett syndrome phenotypes. Nature 2010, 468:263-269.
8. Dawson G., Jones E.J.H., Merkle K., Venema K., Lowy R., Faja S., Kamara D., Murias M., Greenson J., Winter J., Smith M., Rogers S.J., Webb S.J. Early behavioral intervention is associated with normalized brain activity in young children with autism. J. Am. Acad. Child Adolesc. Psychiatry 2012, 51:1150-1159.
9. Dawson G., Rogers S., Munson J., Smith M., Winter J., Greenson J., Donaldson A., Varley J. Randomized, controlled trial of an intervention for toddlers with autism: the Early Start Denver Model. Pediatrics 2010, 125:e17-e23.
10. Della Sala G., Pizzorusso T. Synaptic plasticity and signaling in Rett syndrome. Dev. Neurobiol. 2014, 74:178-196.
11. Engineer C.T., Centanni T.M., Im K.W., Borland M.S., Moreno N.A., Carraway R.S., Wilson L.G., Kilgard M.P. Degraded auditory processing in a rat model of autism limits the speech representation in non-primary auditory cortex. Dev. Neurobiol. 2014, 74:972-986.
12. Engineer C.T., Centanni T.M., Im K.W., Kilgard M.P. Speech sound discrimination training improves auditory cortex responses in a rat model of autism. Front. Syst. Neurosci. 2014, 8:137.
13. Engineer C.T., Centanni T.M., Im K.W., Rahebi K.C., Buell E.P., Kilgard M.P. Degraded speech sound processing in a rat model of fragile X syndrome. Brain Res. 2014, 1564:72-84.
14. Engineer C.T., Perez C.A., Carraway R.S., Chang K.Q., Roland J.L., Kilgard M.P. Speech training alters tone frequency tuning in rat primary auditory cortex. Behav. Brain Res. 2014, 258:166-178.
15. Engineer C.T., Perez C.A., Chen Y.H., Carraway R.S., Reed A.C., Shetake J.A., Jakkamsetti V., Chang K.Q., Kilgard M.P. Cortical activity patterns predict speech discrimination ability. Nat. Neurosci. 2008, 11:603-608.
16. Engineer C.T., Rahebi K.C., Buell E.P., Fink M.K., Kilgard M.P. Speech training alters consonant and vowel responses in multiple auditory cortex fields. Behav. Brain Res. 2015, 287:256-264.
17. Engineer N.D., Engineer C.T., Reed A.C., Pandya P.K., Jakkamsetti V., Moucha R., Kilgard M.P. Inverted-U function relating cortical plasticity and task difficulty. Neuroscience 2012, 205:81-90.
18. Glaze D.G. Neurophysiology of Rett syndrome. J. Child Neurol. 2005, 20:740-746.
19. Goffin D., Allen M., Zhang L., Amorim M., Wang I.-T.J., Reyes A.-R.S., Mercado-Berton A., Ong C., Cohen S., Hu L., Blendy J.a, Carlson G.C., Siegel S.J., Greenberg M.E., Zhou Z. Rett syndrome mutation MeCP2 T158A disrupts DNA binding, protein stability and ERP responses. Nat. Neurosci. 2011, 15:274-283.
20. Goffin D., Brodkin E.S., Blendy J.a, Siegel S.J., Zhou Z. Cellular origins of auditory event-related potential deficits in Rett syndrome. Nat. Neurosci. 2014, 17:804-806.
21. Johnston M.V., Ammanuel S., O'Driscoll C., Wozniak A., Naidu S., Kadam S.D. Twenty-four hour quantitative-EEG and in-vivo glutamate biosensor detects activity and circadian rhythm dependent biomarkers of pathogenesis in Mecp2 null mice. Front. Syst. Neurosci. 2014, 8:1-13.
22. Kálmánchey R. Evoked potentials in the Rett syndrome. Brain Dev. 1990, 12:73-76.
23. Kaufmann W.E., Tierney E., Rohde C.a, Suarez-Pedraza M.C., Clarke M.a, Salorio C.F., Bibat G., Bukelis I., Naram D., Lanham D.C., Naidu S. Social impairments in Rett syndrome: characteristics and relationship with clinical severity. J. Intellect. Disabil. Res. 2012, 56:233-247.
24. Kawahara H. Speech representation and transformation using adaptive interpolation of weighted spectrum: vocoder revisited. Proc. ICASSP 1997, 2:1303-1306.
25. Landa R.J., Holman K.C., O'Neill A.H., Stuart E.a Intervention targeting development of socially synchronous engagement in toddlers with autism spectrum disorder: a randomized controlled trial. J. Child Psychol. Psychiatry 2011, 52:13-21.
26. Lenn N.J., Olsho L.W., Turk W.R. Auditory processing deficit in a patient with Rett syndrome. Am. J. Med. Genet. Suppl. 1986, 1:153-156.
27. Liao W., Gandal M.J., Ehrlichman R.S., Siegel S.J., Carlson G.C. MeCP2+/- mouse model of RTT reproduces auditory phenotypes associated with Rett syndrome and replicate select EEG endophenotypes of autism spectrum disorder. Neurobiol. Dis. 2012, 46:88-92.
28. Marschik P.B., Kaufmann W.E., Sigafoos J., Wolin T., Zhang D., Bartl-Pokorny K.D., Pini G., Zappella M., Tager-Flusberg H., Einspieler C., Johnston M.V. Changing the perspective on early development of Rett syndrome. Res. Dev. Disabil. 2013, 34:1236-1239.
29. McEachin J., Smith T., Lovaas O.I. Long-term outcome for children with autism who received early intensive behavioral treatment. Am. J. Ment. Retard. 1993, 97:359-372.
30. Medrihan L., Tantalaki E., Aramuni G., Sargsyan V., Dudanova I., Missler M., Zhang W. Early defects of GABAergic synapses in the brain stem of a MeCP2 mouse model of Rett syndrome. J. Neurophysiol. 2008, 99:112-121.
31. Na E.S., Nelson E.D., Kavalali E.T., Monteggia L.M. The impact of MeCP2 loss- or gain-of-function on synaptic plasticity. Neuropsychopharmacology 2013, 38:212-219.
32. Neul J.L., Lane J.B., Lee H.-S., Geerts S., Barrish J.O., Annese F., Baggett L.M., Barnes K., Skinner S.a, Motil K.J., Glaze D.G., Kaufmann W.E., Percy A.K. Developmental delay in Rett syndrome: data from the natural history study. J. Neurodev. Disord. 2014, 6:20.
33. Oram Cardy J.E., Flagg E.J., Roberts W., Roberts T.P. Delayed mismatch field for speech and non-speech sounds in children with autism. Neuroreport 2005, 16:521-525.
34. Oram Cardy J.E., Flagg E.J., Roberts W., Roberts T.P. Auditory evoked fields predict language ability and impairment in children. Int. J. Psychophysiol. 2008, 68:170-175.
35. Perez C.A., Engineer C.T., Jakkamsetti V., Carraway R.S., Perry M.S., Kilgard M.P. Different timescales for the neural coding of consonant and vowel sounds. Cereb. Cortex 2013, 23:670-683.
36. Peters S.U., Gordon R.L., Key A.P. Induced gamma oscillations differentiate familiar and novel voices in children with MECP2 duplication and Rett syndromes. J. Child Neurol. 2015, 30:145-152.
37. Purhonen M., Kilpeläinen-Lees R., Valkonen-Korhonen M., Karhu J., Lehtonen J. Cerebral processing of mother's voice compared to unfamiliar voice in 4-month-old infants. Int. J. Psychophysiol. 2004, 52:257-266.
38. Roberts T.P.L., Cannon K.M., Tavabi K., Blaskey L., Khan S.Y., Monroe J.F., Qasmieh S., Levy S.E., Edgar J.C. Auditory magnetic mismatch field latency: a biomarker for language impairment in autism. Biol. Psychiatry 2011, 70:263-269.
39. Russo N., Zecker S., Trommer B., Chen J., Kraus N. Effects of background noise on cortical encoding of speech in autism spectrum disorders. J. Autism Dev. Disord. 2009, 39:1185-1196.
40. Russo N.M., Hornickel J., Nicol T., Zecker S., Kraus N. Biological changes in auditory function following training in children with autism spectrum disorders. Behav. Brain Funct. 2010, 6:60.
41. Shetake J.A., Wolf J.T., Cheung R.J., Engineer C.T., Ram S.K., Kilgard M.P. Cortical activity patterns predict robust speech discrimination ability in noise. Eur. J. Neurosci. 2011, 34:1823-1838.
42. Sigafoos J., Green V.a., Schlosser R., O'eilly M.F., Lancioni G.E., Rispoli M., Lang R. Communication intervention in Rett syndrome: a systematic review. Res. Autism Spectr. Disord. 2009, 3:304-318.
43. Stach B.A., Stoner W.R., Smith S.L., Jerger J.F. Auditory evoked potentials in Rett syndrome. J. Am. Acad. Audiol. 1994, 5:226-230.
44. Stanislaw H., Todorov N. Calculation of signal detection theory measures. Behav. Res. Methods Instrum. Comput. 1999, 31:137-149.
45. Stauder J.E.a, Smeets E.E.J., van Mil S.G.M., Curfs L.G.M. The development of visual- and auditory processing in Rett syndrome: an ERP study. Brain Dev. 2006, 28:487-494.
46. Stearns N.a, Schaevitz L.R., Bowling H., Nag N., Berger U.V., Berger-Sweeney J. Behavioral and anatomical abnormalities in Mecp2 mutant mice: a model for Rett syndrome. Neuroscience 2007, 146:907-921.
47. Urbanowicz A., Downs J., Girdler S., Ciccone N., Leonard H. Aspects of speech-language abilities are influenced by MECP2 mutation type in girls with Rett syndrome. Am. J. Med. Genet. A 2015, 167:354-362.
48. Verma N.P., Nigro M.A., Hart Z.H. Rett syndrome-a gray matter disease? Electrophysiologic evidence. Electroencephalogr. Clin. Neurophysiol. 1987, 67:327-329.
49. Wöhr M., Scattoni M.L. Behavioural methods used in rodent models of autism spectrum disorders: current standards and new developments. Behav. Brain Res. 2013, 251:5-17.
50. Wulffaert J., Van Berckelaer-Onnes I.A., Scholte E.M. Autistic disorder symptoms in Rett syndrome. Autism 2009, 13:567-581.
51. Yamanouchi H., Kaga M., Arima M. Abnormal cortical excitability in Rett syndrome. Pediatr. Neurol. 1993, 9:202-206.
52. Zhou X., Lu J.Y.-F., Darling R.D., Simpson K.L., Zhu X., Wang F., Yu L. Behavioral training reverses global cortical network dysfunction induced by perinatal antidepressant exposure. Proc. Natl. Acad. Sci. U. S. A. 2015, 112:201416582.
53. Zhu X., Liu X., Wei F., Wang F., Merzenich M.M., Schreiner C.E., Sun X., Zhou X. Perceptual training restores impaired cortical temporal processing due to lead exposure. Cereb. Cortex 2014, 1-12.