Altered Forebrain Functional Connectivity and Neurotransmission in a Kinase-Inactive Met Mouse Model of Autism

Molecular Imaging

Volumn 18, Issue , 2019, Pages

  Tang, Shiyu ^a   Powell, Elizabeth M ^a,b   Zhu, Wenjun ^a   Lo, Fu Sun ^a   Erzurumlu, Reha S ^a   Xu, Su ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b NATIONAL INSTITUTE ON ALCOHOL ABUSE AND ALCOHOLISM   (United States)

Author keywords

autism; brain network; GABA; magnetic resonance spectroscopy; met null mice; resting state functional magnetic resonance imaging; somatosensory thalamocortical system

Indexed keywords

AMINO ACIDS; BRAIN; DISEASES; ENZYMES; GENE ENCODING; MAGNETIC RESONANCE IMAGING; MAGNETIC RESONANCE SPECTROSCOPY; MAGNETISM; MAMMALS; NEURAL NETWORKS; RESONANCE;

AUTISM; BRAIN NETWORKS; GABA; MET NULL MICE; RESTING-STATE FUNCTIONAL MAGNETIC RESONANCE IMAGING; SOMATOSENSORY;

FUNCTIONAL NEUROIMAGING;

4 AMINOBUTYRIC ACID; SCATTER FACTOR RECEPTOR; HGFR PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTISM; CONTROLLED STUDY; FEMALE; FOREBRAIN; FUNCTIONAL CONNECTIVITY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GENE INTERACTION; GENOTYPE; IN VIVO STUDY; MOUSE; NERVE CELL NETWORK; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; SENSITIVITY ANALYSIS; SENSORIMOTOR FUNCTION; SOCIAL BEHAVIOR; SOMATOSENSORY SYSTEM; ANIMAL; BRAIN MAPPING; C57BL MOUSE; DIAGNOSTIC IMAGING; DISEASE MODEL; GENETICS; HUMAN; MALE; METABOLISM; NUCLEAR MAGNETIC RESONANCE IMAGING; PROCEDURES; SOMATOSENSORY CORTEX; THALAMUS;

ANIMALS; AUTISM SPECTRUM DISORDER; BRAIN MAPPING; DISEASE MODELS, ANIMAL; FEMALE; GAMMA-AMINOBUTYRIC ACID; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MICE; MICE, INBRED C57BL; PROTO-ONCOGENE PROTEINS C-MET; SOMATOSENSORY CORTEX; THALAMUS;

EID: 85059629516     PISSN: 15353508     EISSN: 15360121     Source Type: Journal    
DOI: 10.1177/1536012118821034     Document Type: Article

References (74)

1. Naldini L, Weidner KM, Vigna E. Scatter factor and hepatocyte growth factor are indistinguishable ligands for the MET receptor. EMBO J. 1991;10(10):2867–2878
2. Campbell DB, Sutcliffe JS, Ebert PJ. A genetic variant that disrupts MET transcription is associated with autism. Proc Natl Acad Sci U S A. 2006;103(45):16834–16839
3. Sousa I, Clark TG, Toma C. MET and autism susceptibility: family and case-control studies. Eur J Hum Genet. 2009;17(6):749–758
4. Jackson PB, Boccuto L, Skinner C. Further evidence that the rs1858830 C variant in the promoter region of the MET gene is associated with autistic disorder. Autism Res. 2009;2(4):232–236
5. Thanseem I, Nakamura K, Miyachi T. Further evidence for the role of MET in autism susceptibility. Neurosci Res. 2010;68(2):137–141
6. Judson MC, Eagleson KL, Wang L, Levitt P. Evidence of cell-nonautonomous changes in dendrite and dendritic spine morphology in the met-signaling-deficient mouse forebrain. J Comp Neurol. 2010;518(21):4463–4478
7. Martins GJ, Plachez C, Powell EM. Loss of embryonic MET signaling alters profiles of hippocampal interneurons. Dev Neurosci. 2007;29(1-2):143–158
8. Martins GJ, Shahrokh M, Powell EM. Genetic disruption of Met signaling impairs GABAergic striatal development and cognition. Neuroscience. 2011;176:199–209
9. Powell EM, Campbell DB, Stanwood GD, Davis C, Noebels JL, Levitt P. Genetic disruption of cortical interneuron development causes region- and GABA cell type-specific deficits, epilepsy, and behavioral dysfunction. J Neurosci. 2003;23(2):622–631
10. Rudie JD, Hernandez LM, Brown JA. Autism-associated promoter variant in MET impacts functional and structural brain networks. Neuron. 2012;75(5):904–915
11. Cascio CJ. Somatosensory processing in neurodevelopmental disorders. J Neurodev Disord. 2010;2(2):62–69
12. Erzurumlu RS, Gaspar P. Development and critical period plasticity of the barrel cortex. Eur J Neurosci. 2012;35(10):1540–1553
13. Bladt F, Riethmacher D, Isenmann S, Aguzzi A, Birchmeier C. Essential role for the c-met receptor in the migration of myogenic precursor cells into the limb bud. Nature. 1995;376(6543):768–771
14. Judson MC, Bergman MY, Campbell DB, Eagleson KL, Levitt P. Dynamic gene and protein expression patterns of the autism-associated met receptor tyrosine kinase in the developing mouse forebrain. J Comp Neurol. 2009;513(5):511–531
15. Smith JM, Xu J, Powell EM. Age dependent forebrain structural changes in mice deficient in the autism associated gene Met tyrosine kinase. Neuroimage Clin. 2012;1(1):66–74
16. Lo FS, Erzurumlu RS, Powell EM. Insulin-Independent GABAA receptor-mediated response in the barrel cortex of mice with impaired met activity. J Neurosci. 2016;36(13):3691–3697
17. Nelson SB, Valakh V. Excitatory/inhibitory balance and circuit homeostasis in autism spectrum disorders. Neuron. 2015;87(4):684–698
18. Thompson BL, Levitt P. Complete or partial reduction of the Met receptor tyrosine kinase in distinct circuits differentially impacts mouse behavior. J Neurodev Disord. 2015;7:35
19. Smith JM, Powell EM. Mice with impaired met tyrosine kinase signaling demonstrate characteristics relevant to autism. Autism. 2012;S1:002
20. Biswal BB, Van Kylen J, Hyde JS. Simultaneous assessment of flow and BOLD signals in resting-state functional connectivity maps. NMR Biomed. 1997;10(4-5):165–170
21. Cordes D, Haughton VM, Arfanakis K. Mapping functionally related regions of brain with functional connectivity MR imaging. AJNR Am J Neuroradiol. 2000;21(9):1636–1644
22. Jiang T, He Y, Zang Y, Weng X. Modulation of functional connectivity during the resting state and the motor task. Hum Brain Mapp. 2004;22(1):63–71
23. Deco G, Ponce-Alvarez A, Mantini D, Romani GL, Hagmann P, Corbetta M. Resting-state functional connectivity emerges from structurally and dynamically shaped slow linear fluctuations. J Neurosci. 2013;33(27):11239–11252
24. Damoiseaux JS, Rombouts SA, Barkhof F. Consistent resting-state networks across healthy subjects. Proc Natl Acad Sci U S A. 2006;103(37):13848–13853
25. Fox MD, Raichle ME. Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat Rev Neurosci. 2007;8(9):700–711
26. Raichle ME. Two views of brain function. Trends Cogn Sci. 2010;14(4):180–190
27. Guerra-Carrillo B, Mackey AP, Bunge SA. Resting-state fMRI: a window into human brain plasticity. Neuroscientist. 2014;20(5):522–533
28. Xu S, Zhuo J, Racz J. Early microstructural and metabolic changes following controlled cortical impact injury in rat: a magnetic resonance imaging and spectroscopy study. J Neurotrauma. 2011;28(10):2091–2102
29. Xu S, Gullapalli RP, Frost DO. Olanzapine antipsychotic treatment of adolescent rats causes long term changes in glutamate and GABA levels in the nucleus accumbens. Schizophr Res. 2015;161(2-3):452–457
30. Xu S, Waddell J, Zhu W. In vivo longitudinal proton magnetic resonance spectroscopy on neonatal hypoxic-ischemic rat brain injury: neuroprotective effects of acetyl-L-carnitine. Magn Reson Med. 2015;74(6):1530–1542
31. D.I.HornC.YuJ.Steiner. Glutamatergic and resting-state functional connectivity correlates of severity in major depression – the role of pregenual anterior cingulate cortex and anterior insula. Front Syst Neurosci. 2010;4:pii: 33
32. Hu Y, Chen X, Gu H, Yang Y. Resting-state glutamate and GABA concentrations predict task-induced deactivation in the default mode network. J Neurosci. 2013;33(47):18566–18573
33. Kwon SH, Scheinost D, Lacadie C. GABA, resting-state connectivity and the developing brain. Neonatology. 2014;106(2):149–155
34. Sampaio-Baptista C, Filippini N, Stagg CJ, Near J, Scholz J, Johansen-Berg H. Changes in functional connectivity and GABA levels with long-term motor learning. Neuroimage. 2015;106:15–20
35. Rubinov M, Sporns O. Complex network measures of brain connectivity: uses and interpretations. Neuroimage. 2010;52(3):1059–1069
36. Bressler SL, Menon V. Large-scale brain networks in cognition: emerging methods and principles. Trends Cogn Sci. 2010;14(6):277–290
37. Sporns O. From simple graphs to the connectome: networks in neuroimaging. Neuroimage. 2012;62(2):881–886
38. Telesford QK, Laurienti PJ, Friedman DP, Kraft RA, Daunais JB. The effects of alcohol on the nonhuman primate brain: a network science approach to neuroimaging. Alcohol Clin Exp Res. 2013;37(11):1891–1900
39. van den Heuvel MP, Scholtens LH, de Reus MA. Topological organization of connectivity strength in the rat connectome. Brain Struct Funct. 2016;221(3):1719–1736
40. Verhoeven JS, De Cock P, Lagae L, Sunaert S. Neuroimaging of autism. Neuroradiology. 2010;52(1):3–14
41. Kennedy DP, Adolphs R. The social brain in psychiatric and neurological disorders. Trends Cogn Sci. 2012;16(11):559–572
42. Bardella G, Bifone A, Gabrielli A, Gozzi A, Squartini T. Hierarchical organization of functional connectivity in the mouse brain: a complex network approach. Sci Rep. 2016;6:32060
43. Liska A, Galbusera A, Schwarz AJ, Gozzi A. Functional connectivity hubs of the mouse brain. Neuroimage. 2015;115:281–291
44. Huh CG, Factor VM, Sanchez A, Uchida K, Conner EA, Thorgeirsson SS. Hepatocyte growth factor/c-met signaling pathway is required for efficient liver regeneration and repair. Proc Natl Acad Sci U S A. 2004;101(13):4477–4482
45. Ferron JF, Kroeger D, Chever O, Amzica F. Cortical inhibition during burst suppression induced with isoflurane anesthesia. J Neurosci. 2009;29(31):9850–9860
46. Liu X, Zhu XH, Zhang Y, Chen W. The change of functional connectivity specificity in rats under various anesthesia levels and its neural origin. Brain Topogr. 2013;26(3):363–377
47. DeSimone JC, Pappas SS, Febo M. Forebrain knock-out of torsinA reduces striatal free-water and impairs whole-brain functional connectivity in a symptomatic mouse model of DYT1 dystonia. Neurobiol Dis. 2017;106:124–132
48. Xu S, Ji Y, Chen X, Yang Y, Gullapalli RP, Masri R. In vivo high-resolution localized (1) H MR spectroscopy in the awake rat brain at 7 T. Magn Reson Med. 2013;69(4):937–943
49. Paxinos G, Franklin K. The Mouse Brain in Stereotaxic Coordinates. 4th ed. Cambridge, MA: Academic Press; 2012
50. Bernhardt BC, Chen Z, He Y, Evans AC, Bernasconi N. Graph-theoretical analysis reveals disrupted small-world organization of cortical thickness correlation networks in temporal lobe epilepsy. Cereb Cortex. 2011;21(9):2147–2157
51. Lu FM, Zhou JS, Zhang J, Wang XP, Yuan Z. Disrupted small-world brain network topology in pure conduct disorder. Oncotarget. 2017;8(39):65506–65524
52. Smit DJ, Stam CJ, Posthuma D, Boomsma DI, de Geus EJ. Heritability of “small-world” networks in the brain: a graph theoretical analysis of resting-state EEG functional connectivity. Hum Brain Mapp. 2008;29(12):1368–1378
53. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc. 1995;57(1):289–300
54. Bennett CM, Wolford GL, Miller MB. The principled control of false positives in neuroimaging. Soc Cogn Affect Neurosci. 2009;4(4):4174–4122
55. Provencher SW. Automatic quantitation of localized in vivo 1 H spectra with LCModel. NMR Biomed. 2001;14(4):260–264
56. Morgan JJ, Kleven GA, Tulbert CD, Olson J, Horita DA, Ronca AE. Longitudinal 1 H MRS of rat forebrain from infancy to adulthood reveals adolescence as a distinctive phase of neurometabolite development. NMR Biomed. 2013;26(6):683–691
57. Harris JL, Yeh HW, Choi IY. Altered neurochemical profile after traumatic brain injury: (1)H-MRS biomarkers of pathological mechanisms. J Cereb Blood Flow Metab. 2012;32(12):2122–2134
58. Shi F, Wang L, Peng Z, Wee CY, Shen D. Altered modular organization of structural cortical networks in children with autism. PLoS One. 2013;8(5):e63131
59. Barttfeld P, Amoruso L, Ais J. Organization of brain networks governed by long-range connections index autistic traits in the general population. J Neurodev Disord. 2013;5(1):16
60. Fair DA, Cohen AL, Power JD. Functional brain networks develop from a “local to distributed” organization. PLoS Comput Biol. 2009;5(5):e1000381
61. Yap PT, Fan Y, Chen Y, Gilmore JH, Lin W, Shen D. Development trends of white matter connectivity in the first years of life. PLoS One. 2011;6(9):e24678
62. Hagmann P, Sporns O, Madan N. White matter maturation reshapes structural connectivity in the late developing human brain. Proc Natl Acad Sci U S A. 2010;107(44):19067–19072
63. Nair A, Carper RA, Abbott AE. Regional specificity of aberrant thalamocortical connectivity in autism. Hum Brain Mapp. 2015;36(11):4497–4511
64. Woodward ND, Giraldo-Chica M, Rogers B, Cascio CJ. Thalamocortical dysconnectivity in autism spectrum disorder: an analysis of the Autism brain imaging data exchange. Biol Psychiatry Cogn Neurosci Neuroimaging. 2017;2(1):76–84
65. Werling DM, Geschwind DH. Sex differences in autism spectrum disorders. Curr Opin Neurol. 2013;26(2):146–153
66. Werling DM, Geschwind DH. Understanding sex bias in autism spectrum disorder. Proc Natl Acad Sci U S A. 2013;110(13):4868–4869
67. Ratto AB, Kenworthy L, Yerys BE. What about the girls? Sex-based differences in Autistic traits and adaptive skills. J Autism Dev Disord. 2018;48(5): 1698–1711
68. Ormond S, Brownlow C, Garnett MS, Rynkiewicz A, Attwood T. Profiling Autism symptomatology: an exploration of the Q-ASC parental report scale in capturing sex differences in Autism. J Autism Dev Disord. 2018;48(2): 389–403
69. Dworzynski K, Ronald A, Bolton P, Happe F. How different are girls and boys above and below the diagnostic threshold for autism spectrum disorders? J Am Acad Child Adolesc Psychiatry. 2012;51(8):788–797
70. Kopp S, Gillberg C. The Autism Spectrum Screening Questionnaire (ASSQ)-Revised Extended Version (ASSQ-REV): an instrument for better capturing the autism phenotype in girls? A preliminary study involving 191 clinical cases and community controls. Res Dev Disabil. 2011;32(6):2875–2888
71. White EI, Wallace GL, Bascom J. Sex differences in parent-reported executive functioning and adaptive behavior in children and young adults with autism spectrum disorder. Autism Res. 2017;10(10):1653–1662
72. Lai MC, Lombardo MV, Auyeung B, Chakrabarti B, Baron-Cohen S. Sex/gender differences and autism: setting the scene for future research. J Am Acad Child Adolesc Psychiatry. 2015;54(1):11–24
73. Masamoto K, Fukuda M, Vazquez A, Kim SG. Dose-dependent effect of isoflurane on neurovascular coupling in rat cerebral cortex. Eur J Neurosci. 2009;30(2):242–250
74. Hutchison RM, Mirsattari SM, Jones CK, Gati JS, Leung LS. Functional networks in the anesthetized rat brain revealed by independent component analysis of resting-state FMRI. J Neurophysiol. 2010;103(6):3398–3406