Altered functional connectivity networks in acallosal and socially impaired BTBR mice

Brain Structure and Function

Volumn 221, Issue 2, 2016, Pages 941-954

  Sforazzini, Francesco ^a   Bertero, Alice ^a,b   Dodero, Luca ^a   David, Gergely ^a   Galbusera, Alberto ^a   Scattoni, Maria Luisa ^c   Pasqualetti, Massimo ^a,b   Gozzi, Alessandro ^a  

^a ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

^b UNIVERSITY OF PISA   (Italy)

^c ISTITUTO SUPERIORE DI SANITÀ   (Italy)

Author keywords

Autism; BTBR; Connectivity; Corpus callosum; fMRI; Mouse retrograde tracing

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASSOCIATION CORTEX; AUTISM; AUTOREGULATION; BASAL GANGLION; BLOOD PRESSURE MEASUREMENT; BOLD SIGNAL; BRAIN BLOOD FLOW; BRAIN CORTEX; BRAIN FUNCTION; CONTROLLED STUDY; CORPUS CALLOSUM; DORSAL HIPPOCAMPUS; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GENICULATE NUCLEUS; LEFT HEMISPHERE; MALE; MONOSYNAPTIC REFLEX; MOUSE; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; RIGHT HEMISPHERE; SOCIAL BEHAVIOR; STRIATE CORTEX; VENTRAL HIPPOCAMPUS; VISUAL CORTEX; WHITE MATTER; ANIMAL; ANIMAL BEHAVIOR; C57BL MOUSE; CONNECTOME; CORPUS CALLOSUM AGENESIS; INBRED MOUSE STRAIN; NEOCORTEX; NERVE CELL NETWORK; NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PROCEDURES; THALAMUS;

AGENESIS OF CORPUS CALLOSUM; ANIMALS; BEHAVIOR, ANIMAL; CONNECTOME; MAGNETIC RESONANCE IMAGING; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED STRAINS; NEOCORTEX; NERVE NET; NEUROIMAGING; SOCIAL BEHAVIOR; THALAMUS; VISUAL CORTEX;

EID: 84959344922     PISSN: 18632653     EISSN: 18632661     Source Type: Journal    
DOI: 10.1007/s00429-014-0948-9     Document Type: Article

References (66)

1. Amodeo DA, Jones JH, Sweeney JA, Ragozzino ME (2012) Differences in BTBR T+tf/J and C57BL/6J mice on probabilistic reversal learning and stereotyped behaviors. Behav Brain Res 227:64–72
2. Anagnostou E, Taylor M (2011) Review of neuroimaging in autism spectrum disorders: what have we learned and where we go from here. Mol Autism 2:4
3. Badaruddin D, Andrews G, Bolte S, Schilmoeller K, Schilmoeller G, Paul L, Brown W (2007) Social and behavioral problems of children with agenesis of the corpus callosum. Child Psychiatry Hum Dev 38:287–302
4. Boly M, Tshibanda L, Vanhaudenhuyse A, Noirhomme Q, Schnakers C, Ledoux D, Boveroux P, Garweg C, Lambermont B, Phillips C, Luxen A, Moonen G, Bassetti C, Maquet P, Laureys S (2009) Functional connectivity in the default network during resting state is preserved in a vegetative but not in a brain dead patient. Hum Brain Mapp 30:2393–2400
5. Bourgeron T (2009) A synaptic trek to autism. Curr Opin Neurobiol 19:231–234
6. Cherkassky VL, Kana RK, Keller TA, Just MA (2006) Functional connectivity in a baseline resting-state network in autism. Neuro Rep 17:1687–1690
7. Dichter GS, Felder JN, Green SR, Rittenberg AM, Sasson NJ, Bodfish JW (2012) Reward circuitry function in autism spectrum disorders. Soc Cogn Affect Neurosci 7:160–172
8. Dodero L, Damiano M, Galbusera A, Bifone A, Tsaftsaris SA, Scattoni ML, Gozzi A (2013) Neuroimaging evidence of major morpho-anatomical and functional abnormalities in the BTBR T+TF/J mouse model of autism. PLoS One 8:e76655
9. Ebisch SJ, Gallese V, Willems RM, Mantini D, Groen WB, Romani GL, Buitelaar JK, Bekkering H (2010) Altered intrinsic functional connectivity of anterior and posterior insula regions in high-functioning participants with autism spectrum disorder. Hum Brain Mapp 32:1013–1028
10. Ferrari L, Turrini G, Crestan V, Bertani S, Cristofori P, Bifone A, Gozzi A (2012) A robust experimental protocol for pharmacological fMRI in rats and mice. J Neurosci Methods 204:9–18
11. Frazier TW, Hardan AY (2009) A meta-analysis of the corpus callosum in autism. Biol Psychiatry 66:935–941
12. Gogolla N, LeBlanc J, Quast K, Südhof TC, Fagiolini M, Hensch T (2009) Common circuit defect of excitatory-inhibitory balance in mouse models of autism. J Neurodev Disord 1:172–181
13. Gozzi A, Ceolin L, Schwarz A, Reese T, Bertani S, Bifone A (2007) A multimodality investigation of cerebral haemodynamics and autoregulation in phMRI. Magn Reson Imaging 25:826–833
14. Greicius MD, Kiviniemi V, Tervonen O, Vainionpää V, Alahuhta S, Reiss AL, Menon V (2008) Persistent default-mode network connectivity during light sedation. Human Brain Mapping 29:839–847
15. Han S, Tai C, Jones C, Scheuer T, Catterall W (2014) Enhancement of inhibitory neurotransmission by gabaa receptors ameliorates behavioral deficits in a mouse model of autism. Neuron 81:1282–1289
16. Hutchison RM, Leung LS, Mirsattari SM, Gati JS, Menon RS, Everling S (2011) Resting-state networks in the macaque at 7 Tesla. NeuroImage 56:1546–1555
17. + tf/J mouse model of autism. PLoS One 8:e61829
18. Just MA, Keller TA, Malave VL, Kana RK, Varma S (2012) Autism as a neural systems disorder: a theory of frontal-posterior underconnectivity. Neurosci Biobehav Rev 36:1292–1313
19. Kennedy DP, Courchesne E (2008) The intrinsic functional organization of the brain is altered in autism. NeuroImage 39:1877–1885
20. Lau YC, Hinkley LB, Bukshpun P, Strominger ZA, Wakahiro ML, Baron-Cohen S, Allison C, Auyeung B, Jeremy RJ, Nagarajan SS, Sherr EH, Marco EJ (2012) Autism traits in individuals with agenesis of the corpus callosum. J Autism Dev Disord 43:1106–1118
21. Liang Z, King J, Zhang N (2011) Uncovering intrinsic connectional architecture of functional networks in awake rat brain. J Neurosci 31:3776–3783
22. Liang Z, King J, Zhang N (2012) Intrinsic organization of the anesthetized brain. J Neurosci 32:10183–10191
23. Liang Z, Li T, King J, Zhang N (2013) Mapping thalamocortical networks in rat brain using resting-state functional connectivity. NeuroImage 83:237–244
24. Liu X, Zhu XH, Zhang Y, Chen W (2011) Neural origin of spontaneous hemodynamic fluctuations in rats under burst-suppression anesthesia condition. Cereb Cortex 21:374–384
25. Livy DJ, Schalomon PM, Roy M, Zacharias MC, Pimenta J, Lent R, Wahlsten D (1997) Increased axon number in the anterior commissure of mice lacking a corpus callosum. Exp Neurol 146:491–501
26. Lu H, Zou Q, Gu H, Raichle ME, Stein EA, Yang Y (2012) Rat brains also have a default mode network. PNAS 109:3979–3984
27. McFarlane HG, Kusek GK, Yang M, Phoenix JL, Bolivar VJ, Crawley JN (2008) Autism-like behavioral phenotypes in BTBR T+tf/J mice. Genes Brain Behav 7:152–163
28. Meye BU, Ruricht O (1998) In vivo visualisation of the longitudinal callosal fascicle (Probst’s bundle) and other abnormalities in an acallosal brain. J Neurol Neurosurg Psychiatry 64:138–139
29. Miller VM, Gupta D, Neu N, Cotroneo A, Boulay CD, Seegal RF (2013) Novel inter-hemispheric white matter connectivity in the BTBR mouse model of autism. pp 26–33
30. Mohajerani MH, McVea DA, Fingas M, Murphy TH (2010) Mirrored bilateral slow-wave cortical activity within local circuits revealed by fast bihemispheric voltage-sensitive dye imaging in anesthetized and awake mice. J Neurosci 30:3745–3751
31. Monk CS, Peltier SJ, Wiggins JL, Weng SJ, Carrasco M, Risi S, Lord C (2009) Abnormalities of intrinsic functional connectivity in autism spectrum disorders. Neuroimage 47:764–772
32. Mori S, Crain BJ, Chacko VP, van Zijl PC (1999) Three-dimensional tracking of axonal projections in the brain by magnetic resonance imaging. Ann Neurol 45:265–269
33. Osakada F, Callaway EM (2013) Design and generation of recombinant rabies virus vectors. Nat Protoc 8:1583–1601
34. Owen JP, Li YO, Yang FG, Shetty C, Bukshpun P, Vora S, Wakahiro M, Hinkley LB, Nagarajan SS, Sherr EH (2013) Resting-state networks and the functional connectome of the human brain in agenesis of the corpus callosum. Brain Connect 3:547–562
35. Paul LK, Brown WS, Adolphs R, Tyszka JM, Richards LJ, Mukherjee P, Sherr EH (2007) Agenesis of the corpus callosum: genetic, developmental and functional aspects of connectivity. Nat Rev Neurosci 8:287–299
36. Paul LK, Corsello C, Kennedy DP, Adolphs R (2014) Agenesis of the corpus callosum and autism: a comprehensive comparison. Brain 137:1813–1829
37. Paxinos G, Franklin K (2003) The mouse brain in stereotaxic coordinates. Academic Press, Sydney
38. Probst FP (1973) Congenital defects of the corpus callosum. Morphology and encephalographic appearances. Acta Radiol Suppl 331:1
39. Quigley M, Cordes D, Turski P, Moritz C, Haughton V, Seth R, Meyerand ME (2003) Role of the corpus callosum in functional connectivity. AJNR Am J Neuroradiol 24:208–212
40. Rancz EA, Franks KM, Schwarz MK, Pichler B, Schaefer AT, Margrie TW (2011) Transfection via whole-cell recording in vivo: bridging single-cell physiology, genetics and connectomics. Nat Neurosci 14:527–532
41. Ren T, Zhang J, Plachez C, Mori S, Richards LJ (2007) Diffusion tensor magnetic resonance imaging and tract-tracing analysis of probst bundle structure in netrin1- and DCC-deficient mice. J Neurosci 27:10345–10349
42. Rinaldi T, Perrodin C, Markram H (2008) Hyper-connectivity and hyper-plasticity in the medial prefrontal cortex in the valproic acid animal model of autism. Frontiers in Neural Circuits 2
43. Sannino T, Gozzi A, Cerasa A, Schegga D, Manago F, Damiano M, Galbusera A, Dodero L, Tonelli D, Bifone A, Tsaftaris AS, Weinberger DR, Spalletta G, Papaleo F (2013) Sexual dimorphisms in COMT modulation of cortical anatomy and behavior in mice and humans. Cereb Cortex (ahead of print)
44. Sasaki M, Nakagawa E, Sugai K, Shimizu Y, Hattori A, Nonoda Y, Sato N (2010) Brain perfusion SPECT and EEG findings in children with autism spectrum disorders and medically intractable epilepsy. Brain Dev 32:776–782
45. Scattoni ML, Gandhy SU, Ricceri L, Crawley JN (2008) Unusual repertoire of vocalizations in the BTBR T+tf/J mouse model of autism. PLoS One 3(8):e3067
46. Scattoni ML, Ricceri L, Crawley JN (2011) Unusual repertoire of vocalizations in adult BTBR T+tf/J mice during three types of social encounters. Genes Brain Behav 10:44–56
47. Schwarz AJ, Gass N, Sartorius A, Risterucci C, Spedding M, Schenker E, Meyer-Lindenberg A, Weber-Fahr W (2013) Anti-correlated cortical networks of intrinsic connectivity in the rat brain. Brain Connect 3:503–511
48. Sforazzini F, Schwarz AJ, Galbusera A, Bifone A, Gozzi A (2014) Distributed BOLD and CBV-weighted resting-state networks in the mouse brain. Neuroimage 15:403–415
49. Shevell MI (2002) Clinical and diagnostic profile of agenesis of the corpus callosum. J Child Neurol 17:895–899
50. Silverman JL, Tolu SS, Barkan CL, Crawley JN (2009) Repetitive self-grooming behavior in the BTBR mouse model of autism is blocked by the mGluR5 antagonist MPEP. Neuropsychopharmacology
51. Silverman JL, Yang M, Lord C, Crawley JN (2010) Behavioural phenotyping assays for mouse models of autism. Nat Rev Neurosci 11:490–502
52. Silverman JL, Smith DG, Rizzo SJ, Karras MN, Turner SM, Tolu SS, Bryce DK, Smith DL, Fonseca K, Ring RH, Crawley JN (2012) Negative allosteric modulation of the mGluR5 receptor reduces repetitive behaviors and rescues social deficits in mouse models of autism. Sci Trans Med 4:131ra51
53. Silverman JL, Gastrell PT, Karras MN, Solomon M, Crawley JN (2013) Cognitive abilities on transitive inference using a novel touchscreen technology for mice. Cereb Cortex. doi:10.1093/cercor/bht293
54. Squillace M, Dodero L, Federici M, Migliarini S, Errico F, Napolitano F, Krashia P, Di Maio A, Galbusera A, Bifone A, Scattoni ML, Pasqualetti M, Mercuri NB, Usiello A, Gozzi A (2014) Dysfunctional dopaminergic neurotransmission in asocial BTBR mice. Trans Psychiatry (in press)
55. Steffey MA, Brosnan RJ, Steffey EP (2003) Assessment of halothane and sevoflurane anesthesia in spontaneously breathing rats. Am J Vet Res 64:470–474
56. Testa-Silva G, Loebel A, Giugliano M, de Kock CPJ, Mansvelder HD, Meredith RM (2012) Hyperconnectivity and slow synapses during early development of medial prefrontal cortex in a mouse model for mental retardation and autism. Cereb Cortex 22:1333–1342
57. Tyszka JM, Kennedy DP, Adolphs R, Paul LK (2011) Intact bilateral resting-state networks in the absence of the corpus callosum. J Neurosci 31:15154–15162
58. Uddin LQ, Menon V (2009) The anterior insula in autism: under-connected and under-examined. Neurosci Biobehav Rev 33:1198–1203
59. Vertes RP (2004) Differential projections of the infralimbic and prelimbic cortex in the rat. Synapse 51:32–58
60. Wahlsten D, Metten P, Crabbe JC (2003) Survey of 21 inbred mouse strains in two laboratories reveals that BTBR T/+ tf/tf has severely reduced hippocampal commissure and absent corpus callosum. Brain Res 971:47–54
61. Wickersham IR, Finke S, Conzelmann KK, Callaway EM (2006) Retrograde neuronal tracing with a deletion-mutant rabies virus. Nat Methods 4:47–49
62. Yang M, Clarke AM, Crawley JN (2009) Postnatal lesion evidence against a primary role for the corpus callosum in mouse sociability. Eur J Neurosci 29:1663–1677
63. Yizhar O, Fenno LE, Prigge M, Schneider F, Davidson TJ, ‘Shea DJ, Sohal VS, Goshen I, Finkelstein J, Paz JT, Stehfest K, Fudim R, Ramakrishnan C, Huguenard JR, Hegemann P, Deisseroth K (2011) Neocortical excitation/inhibition balance in information processing and social dysfunction. Nature 477:171–178
64. Zhan Y, Paolicelli R, Sforazzini F, Weinhard L, Bolasco G, Pagani F, Vissosktsy A, Bifone A, Gozzi A, Ragozzino D, Gross C (2014) Deficient neuron-microglia signaling results in impaired functional brain connectivity and social behavior. Nat Neurosci 17:400–406
65. Zikopoulos B, Barbas H (2013) Altered neural connectivity in excitatory and inhibitory cortical circuits in autism. Frontiers in human neuroscience 7
66. Zingg B, Hintiryan H, Gou L, Song MY, Bay M, Bienkowski MS, Foster NN, Yamashita S, Bowman I, Toga AW, Dong HW (2014) Neural networks of the mouse neocortex. Cell 156:1096–1111