Circuit-specific intracortical hyperconnectivity in mice with deletion of the autism-associated Met receptor tyrosine kinase

Journal of Neuroscience

Volumn 31, Issue 15, 2011, Pages 5855-5864

  Qiu, Shenfeng ^a   Anderson, Charles T ^b   Levitt, Pat ^a   Shepherd, Gordon M G ^b  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTAMIC ACID; SCATTER FACTOR RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTISM; BRAIN CORTEX; BRAIN MAPPING; CONTROLLED STUDY; ELECTROPHYSIOLOGY; EXCITATORY POSTSYNAPTIC POTENTIAL; FRONTAL CORTEX; GENE DELETION; GENE INACTIVATION; HETEROZYGOSITY; MOUSE; NERVE CELL MEMBRANE POTENTIAL; NERVE PROJECTION; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SYNAPTIC POTENTIAL;

ANIMALS; AUTISTIC DISORDER; BRAIN MAPPING; ELECTROPHYSIOLOGICAL PHENOMENA; FRONTAL LOBE; GENE DELETION; GLOBUS PALLIDUS; GLUTAMIC ACID; IMAGE PROCESSING, COMPUTER-ASSISTED; MICE; MICE, KNOCKOUT; NEURAL PATHWAYS; PHOTIC STIMULATION; PONS; PROTO-ONCOGENE PROTEINS C-MET; PYRAMIDAL CELLS; SIGNAL TRANSDUCTION; SYNAPSES;

EID: 79955763971     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.6569-10.2011     Document Type: Article

References (73)

1. Abrahams BS, Geschwind DH (2010) Connecting genes to brain in the autism spectrum disorders. Arch Neurol 67:395-399.
2. Anderson CT, Sheets PL, Kiritani T, Shepherd GM (2010) Sublayer-specific microcircuits of corticospinal and corticostriatal neurons in motor cortex. Nat Neurosci 13:739-744.
3. Baron-Cohen S, Ashwin E, Ashwin C, Tavassoli T, Chakrabarti B (2009) Talent in autism: hyper-systemizing, hyper-attention to detail and sensory hypersensitivity. Philos Trans R Soc Lond B Biol Sci 364:1377-1383.
4. Blue ME, Parnavelas JG (1983) The formation and maturation of synapses in the visual cortex of the rat. II. Quantitative analysis. J Neurocytol 12:697-712.
5. Bronner-Fraser M (1995) Hepatocyte growth factor/scatter factor (HGF/ SF) in early development: evidence for a role in neural induction. Trends Genet 11:423-425.
6. Brown SP, Hestrin S (2009) Intracortical circuits of pyramidal neurons reflect their long-range axonal targets. Nature 457:1133-1136.
7. Bureau I, Shepherd GM, Svoboda K (2004) Precise development of functional and anatomical columns in the neocortex. Neuron 42:789-801.
8. Bureau I, Shepherd GM, Svoboda K (2008) Circuit and plasticity defects in the developing somatosensory cortex of FMR1 knock-out mice. J Neuro-sci 28:5178-5188.
9. Callaway EM, Katz LC (1993) Photostimulation using caged glutamate reveals functional circuitry in living brain slices. Proc Natl Acad Sci USA 90:7661-7665.
10. Campbell DB, Sutcliffe JS, Ebert PJ, Militerni R, Bravaccio C, Trillo S, Elia M, Schneider C, Melmed R, Sacco R, Persico AM, Levitt P (2006) A genetic variant that disrupts MET transcription is associated with autism. Proc Natl Acad Sci USA 103:16834-16839.
11. Campbell DB, D'Oronzio R, Garbett K, Ebert PJ, Mirnics K, Levitt P, Persico AM (2007) Disruption of cerebral cortex MET signaling in autism spectrum disorder. Ann Neurol 62:243-250.
12. Campbell DB, Buie TM, Winter H, Bauman M, Sutcliffe JS, Perrin JM, Levitt P (2009) Distinct genetic risk based on association of MET in families with co-occurring autism and gastrointestinal conditions. Pediatrics 123:1018-1024.
13. Campbell DB, Warren D, Sutcliffe JS, Lee EB, Levitt P (2010) Association of MET with social and communication phenotypes in individuals with autism spectrum disorder. Am J Med Genet B Neuropsychiatr Genet 153B:438-446.
14. Caviness VS (1975) Architectonic mapof neocortex ofthe normal mouse. J Comp Neurol 164:247-263.
15. Chao HT, Zoghbi HY, Rosenmund C (2007) MeCP2 controls excitatory synaptic strength by regulating glutamatergic synapse number. Neuron 56:58-65.
16. Courchesne E, Pierce K (2005) Why the frontal cortex in autism might be talking only to itself: local over-connectivity but long-distance disconnection. Curr Opin Neurobiol 15:225-230.
17. Dani VS, Nelson SB (2009) Intact long-term potentiation but reduced connectivity between neocortical layer 5 pyramidal neurons in a mouse model of Rett syndrome. J Neurosci 29:11263-11270.
18. Dani VS, Chang Q, Maffei A, Turrigiano GG, Jaenisch R, Nelson SB (2005) Reduced cortical activity due to a shift in the balance between excitation and inhibition in a mouse model of Rett Syndrome. Proc Natl Acad Sci USA 102:12560-12565.
19. Ehninger D, Li W, Fox K, Stryker MP, Silva AJ (2008) Reversing neurode-velopmental disorders in adults. Neuron 60:950-960.
20. Frith C (2004) Is autism a disconnection disorder? Lancet Neurol 3:577.
21. Geschwind DH, Levitt P (2007) Autism spectrum disorders: developmental disconnection syndromes. Curr Opin Neurobiol 17:103-111.
22. Gibson JR, Bartley AF, Hays SA, Huber KM (2008) Imbalance ofneocortical excitation and inhibition and altered UP states reflect network hyperex-citability in the mouse model of fragile X syndrome. J Neurophysiol 100:2615-2626.
23. Gogolla N, Leblanc JJ, Quast KB, Sudhof T, Fagiolini M, Hensch TK (2009) Common circuit defect of excitatory-inhibitory balance in mouse models of autism. J Neurodev Disord 1:172-181.
24. Gorski JA, Talley T, Qiu M, Puelles L, Rubenstein JL, Jones KR (2002) Cortical excitatory neurons and glia, but not GABAergic neurons, are produced in the Emx1-expressing lineage. J Neurosci 22:6309-6314.
25. Gutierrez H, Dolcet X, Tolcos M, Davies A (2004) HGF regulates the development of cortical pyramidal dendrites. Development 131:3717-3726.
26. Hallett M, Lebiedowska MK, Thomas SL, Stanhope SJ, Denckla MB, Rumsey J (1993) Locomotion of autistic adults. Arch Neurol 50:1304-1308.
27. Haswell CC, Izawa J, Dowell LR, Mostofsky SH, Shadmehr R (2009) Representation of internal models of action in the autistic brain. Nat Neurosci 12:970-972.
28. Hattox AM, Nelson SB (2007) Layer V neurons in mouse cortex projecting to different targets have distinct physiological properties. J Neurophysiol 98:3330-3340.
29. Haznedar MM, Buchsbaum MS, Hazlett EA, LiCalzi EM, Cartwright C, Hollander E (2006) Volumetric analysis and three-dimensional glucose metabolic mapping of the striatum and thalamus in patients with autism spectrum disorders. Am J Psychiatry 163:1252-1263.
30. Iarocci G, McDonald J (2006) Sensory integration and the perceptual experience of persons with autism. J Autism Dev Disord 36:77-90.
31. Jackson PB, Boccuto L, Skinner C, Collins JS, Neri G, Gurrieri F, Schwartz CE (2009) Further evidence that the rs1858830 C variant in the promoter region of the MET gene is associated with autistic disorder. Autism Res 2:232-236.
32. Judson MC, Bergman MY, Campbell DB, Eagleson KL, Levitt P (2009) Dynamic gene and protein expression patterns of the autism-associated met receptor tyrosine kinase in the developing mouse forebrain. J Comp Neu-rol 513:511-531.
33. Judson MC, Eagleson KL, Wang L, Levitt P (2010) Evidence of cell-nonautonomous changes in dendrite and dendritic spine morphology in the met-signaling-deficient mouse forebrain. J Comp Neurol 518:4463-4478.
34. Judson MC, Amaral DG, Levitt P (2011) Conserved subcortical and divergent cortical of proteins encoded by orthologs of the autism risk gene MET. Cereb Cortex, in press.
35. Just MA, Cherkassky VL, Keller TA, Minshew NJ (2004) Cortical activation and synchronization during sentence comprehension in high-functioning autism: evidence of underconnectivity. Brain 127:1811-1821.
36. Just MA, Cherkassky VL, Keller TA, Kana RK, Minshew NJ (2007) Functional and anatomical cortical underconnectivity in autism: evidence from an FMRI study of an executive function task and corpus callosum morphometry. Cereb Cortex 17:951-961.
37. Katz LC, Dalva MB (1994) Scanning laser photostimulation: a new approach for analyzing brain circuits. J Neurosci Methods 54:205-218.
38. Lefort S, Tomm C, Sarria JCF, Petersen CC (2009) The excitatory neu-ronal network of the C2 barrel column in mouse primary somatosensory cortex. Neuron 61:301-316.
39. Levitt P, Eagleson KL, Powell EM (2004) Regulation of neocortical in-terneuron development and the implications for neurodevelopmental disorders. Trends Neurosci 27:400-406.
40. Maina F, Hilton MC, Andres R, Wyatt S, Klein R, Davies AM (1998) Multiple roles for hepatocyte growth factor in sympathetic neuron development. Neuron 20:835-846.
41. Markram H, Rinaldi T, Markram K (2007) The intense world syndrome-an alternative hypothesis for autism. Front Neurosci 1:77-96.
42. Markram K, Markram H (2010) The intense world theory-a unifying theory of the neurobiology of autism. Front Hum Neurosci 4:224.
43. Marshall CR, Noor A, Vincent JB, Lionel AC, Feuk L, Skaug J, Shago M, Moessner R, Pinto D, Ren Y, Thiruvahindrapduram B, Fiebig A, Schreiber S, Friedman J, Ketelaars CE, Vos YJ, Ficicioglu C, Kirkpatrick S, Nicolson R, Sloman L, et al. (2008) Structural variation of chromosomes in autism spectrum disorder. Am J Hum Genet 82:477-488.
44. Micheva KD, Beaulieu C (1996) Quantitative aspects of synaptogenesis in the rat barrel field cortex with special referencetoGABA circuitry.J Comp Neurol 373:340-354.
45. Milutinovic S, D'Alessio AC, Detich N, Szyf M (2007) Valproate induces widespread epigenetic reprogramming which involves demethylation of specific genes. Carcinogenesis 28:560-571.
46. Morishima M, Kawaguchi Y (2006) Recurrent connection patterns of cor-ticostriatal pyramidal cells in frontal cortex. J Neurosci 26:4394-4405.
47. Mostofsky SH, Powell SK, Simmonds DJ, Goldberg MC, Caffo B, Pekar JJ (2009) Decreased connectivity and cerebellar activity in autism during motor task performance. Brain 132:2413-2425.
48. Moy SS, Nadler JJ (2008) Advances in behavioral genetics: mouse models of autism. Mol Psychiatry 13:4-26.
49. Neymotin SA, Jacobs KM, Fenton AA, Lytton WW (2010) Synaptic information transfer in computer models of neocortical columns. J Comput Neurosci 30:69-84.
50. Otsuka T, Kawaguchi Y (2008) Firing-pattern-dependent specificity of cortical excitatory feed-forward subnetworks. J Neurosci 28:11186-11195.
51. Persico AM, Bourgeron T (2006) Searching for ways out of the autism maze: genetic, epigenetic and environmental clues. Trends Neurosci 29:349-358.
52. Pfeiffer BE, Huber KM (2009) The state of synapses in fragile X syndrome. Neuroscientist 15:549-567.
53. Pinto D, Pagnamenta AT, Klei L, Anney R, Merico D, Regan R, Conroy J, Magalhaes TR, Correia C, Abrahams BS, Almeida J, Bacchelli E, Bader GD, Bailey AJ, Baird G, Battaglia A, Berney T, Bolshakova N, Bölte S, Bolton PF, et al. (2010) Functional impact of global rare copy number variation in autism spectrum disorders. Nature 466:368-372.
54. Rasalam AD, Hailey H, Williams JH, Moore SJ, Turnpenny PD, Lloyd DJ, Dean JC (2005) Characteristics of fetal anticonvulsant syndrome associated autistic disorder. Dev Med Child Neurol 47:551-555.
55. Rinaldi T, Silberberg G, Markram H (2008a) Hyperconnectivity of local neocortical microcircuitry induced by prenatal exposure to valproic acid. Cereb Cortex 18:763-770.
56. Rinaldi T, Perrodin C, Markram H (2008b) Hyper-connectivity and hyper-plasticityinthe medial prefrontal cortexin the valproic acid animal model of autism. Front Neural Circuits 2:4.
57. Rubenstein JL, Merzenich MM (2003) Model of autism: increased ratio of excitation/inhibition in key neural systems. Genes Brain Behav 2: 255-267.
58. Scott-Van Zeeland AA, Abrahams BS, Alvarez-Retuerto AI, Sonnenblick LI, Rudie JD, Ghahremani D, Mumford JA, Poldrack RA, Dapretto M, Ge-schwind DH, Bookheimer SY (2010) Altered functional connectivity in frontal lobe circuits is associated with variation in the autism risk gene CNTNAP2. Sci Transl Med 2:56ra80.
59. Shepherd GMG (2009) Intracortical cartography in an agranular area. Front Neurosci 3:337-343.
60. Shepherd GMG (2011) Circuit mapping by ultraviolet uncaging of gluta-mate. In: Imaging in neuroscience: a laboratory manual (Helmchen F, Konnerth A, Yuste R, eds), pp 417-427. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
61. Shepherd GMG, Pologruto TA, Svoboda K (2003) Circuit analysis of experience-dependent plasticity in the developing rat barrel cortex. Neuron 38:277-289.
62. Shepherd GMG, Stepanyants A, Bureau I, Chklovskii DB, Svoboda K (2005) Geometric and functional organization of cortical circuits. Nat Neurosci 8:782-790.
63. Sousa I, Clark TG, Toma C, Kobayashi K, Choma M, Holt R, Sykes NH, Lamb JA, Bailey AJ, Battaglia A, Maestrini E, Monaco AP (2009) MET and autism susceptibility: family and case-control studies. Eur J Hum Genet 17:749-758.
64. Sudhof TC (2008) Neuroligins and neurexins link synaptic function to cognitive disease. Nature 455:903-911.
65. Suter BA, O'Connor T, Iyer V, Petreanu LT, Hooks BM, Kiritani T, Svoboda K, Shepherd GMG (2010) Ephus: multipurpose data acquisition software for neuroscience experiments. Front Neurosci Methods 4:1-12.
66. Teitelbaum P, Teitelbaum O, Nye J, Fryman J, Maurer RG (1998) Movement analysis in infancy may be useful for early diagnosis of autism. Proc Natl Acad Sci USA 95:13982-13987.
67. Tennant KA, Adkins DL, Donlan NA, Asay AL, Thomas N, Kleim JA, Jones TA (2010) The organization of the forelimb representation of the C57BL/6 mouse motor cortex as defined by intracortical microstimula-tion and cytoarchitecture. Cereb Cortex 21:865-876.
68. Thanseem I, Nakamura K, Miyachi T, Toyota T, Yamada S, Tsujii M, Tsuchiya KJ, Anitha A, Iwayama Y, Yamada K, Hattori E, Matsuzaki H, Matsumoto K, Iwata Y, Suzuki K, Suda S, Kawai M, Sugihara G, Take-bayashi K, Takei N, et al. (2010) Further evidence for the role of MET in autism susceptibility. Neurosci Res 68:137-141.
69. Van De Werd HJ, Rajkowska G, Evers P, Uylings HB (2010) Cytoarchitec-tonic and chemoarchitectonic characterization of the prefrontal cortical areas in the mouse. Brain Struct Funct 214:339-353.
70. Weiler N, Wood L, Yu J, Solla SA, Shepherd GMG (2008) Top-down laminar organization of the excitatory network in motor cortex. Nat Neurosci 11:360-366.
71. Wood L, Shepherd GM (2010) Synaptic circuit abnormalities of motor-frontal layer 2/3 pyramidal neurons in a mutant mouse model of Rett syndrome. Neurobiol Dis 38:281-287.
72. Wood L, Gray NW, Zhou Z, Greenberg ME, Shepherd GM (2009) Synaptic circuit abnormalities of motor-frontal layer 2/3 pyramidal neurons in an RNA interference model of methyl-CpG-binding protein 2 deficiency. J Neurosci 29:12440-12448.
73. Zoghbi HY (2003) Postnatal neurodevelopmental disorders: meeting at the synapse? Science 302:826-830.