Cognitive ability is associated with altered medial frontal cortical circuits in the LgDel mouse model of 22q11.2DS

Cerebral Cortex

Volumn 25, Issue 5, 2015, Pages 1143-1151

  Meechan, D W ^a,b   Rutz, H L H ^b   Fralish, M S ^a,b   Maynard, T M ^a,b   Rothblat, L A ^b   Lamantia, A S ^a,b  

^a GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

^b GEORGE WASHINGTON UNIVERSITY   (United States)

Author keywords

Anterior cingulate cortex; Cortical circuit disorders; Interneurons; Projection neurons; Reversal learning

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTERIOR CINGULATE; ARTICLE; AUTISM; BRAIN DISEASE; BRAIN HISTOLOGY; CHROMOSOME DELETION 22Q11; COGNITIVE DEFECT; CONFOCAL MICROSCOPE; CORTICAL CIRCUIT DISORDER; FRONTAL CORTEX; INTERNEURON; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SCHIZOPHRENIA; ANIMAL; ANIMAL BEHAVIOR; C57BL MOUSE; COGNITION; CYTOLOGY; DISCRIMINATION LEARNING; DISEASE MODEL; EXECUTIVE FUNCTION; FRONTAL LOBE; NERVE CELL; NERVE CELL NETWORK; PATHOLOGY; PSYCHOLOGY; SYNAPSE;

22Q11 DELETION SYNDROME; ANIMALS; BEHAVIOR, ANIMAL; COGNITION; DISCRIMINATION LEARNING; DISEASE MODELS, ANIMAL; EXECUTIVE FUNCTION; FRONTAL LOBE; INTERNEURONS; MALE; MICE; MICE, INBRED C57BL; NERVE NET; NEURONS; SYNAPSES;

EID: 84928911790     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bht308     Document Type: Article

References (59)

1. Abraham A, Windmann S, McKenna P, Gunturkun O. 2007. Creative thinking in schizophrenia: the role of executive dysfunction and symptom severity. Cogn Neuropsychiatry. 12:235-258.
2. Bearden CE, van Erp TG, Dutton RA, Lee AD, Simon TJ, Cannon TD, Emanuel BS, McDonald-McGinn D, Zackai EH, Thompson PM. 2009. Alterations in midline cortical thickness and gyrification patterns mapped in children with 22qll.2 deletions. Cereb Cortex. 19:115-126.
3. Brigman JL, Graybeal C, Holmes A. 2010. Predictably irrational: assaying cognitive inflexibility in mouse models of schizophrenia. Front Neurosci. 4:19-28.
4. Brigman JL, Powell EM, Mittleman G, Young JW. 2012. Examining the genetic and neural components of cognitive flexibility using mice. Physiol Behav. 107:666-669.
5. Brigman JL, Rothblat LA. 2008. Stimulus specific deficit on visual reversal learning after lesions of medial prefrontal cortex in the mouse. Behav Brain Res. 187:405-410.
6. Bussey TJ, Everitt BJ, Robbins TW. 1997. Dissociable effects of cingu-late and medial frontal cortex lesions on stimulus-reward learning using a novel Pavlovian autoshaping procedure for the rat: implications for the neurobiology of emotion. Behav Neurosci. 111:908-919.
7. Bussey TJ, Muir JL, Everitt BJ, Robbins TW. 1997. Triple dissociation of anterior cingulate, posterior cingulate, and medial frontal cortices on visual discrimination tasks using a touchscreen testing procedure for the rat. Behav Neurosci. 111:920-936.
8. Bussey TJ, Saksida LM, Rothblat LA. 2001. Discrimination of computer-graphic stimuli by mice: a method for the behavioral characterization of transgenic and gene-knockout models. Behav Neurosci. 115:957-960.
9. Campbell LE, Azuma R, Ambery F, Stevens A, Smith A, Morris RG, Murphy DG, Murphy KC. 2010. Executive functions and memory abilities in children with 22qll.2 deletion syndrome. Aust N Z J Psychiatry. 44:364-371.
10. Campbell LE, Daly E, Toal F, Stevens A, Azuma R, Catani M, Ng V, van Amelsvoort T, Chitnis X, Cutter W et al. 2006. Brain and behaviour in children with 22qll.2 deletion syndrome: a volumetric and voxel-based morphometry MRI study. Brain. 129:1218-1228.
11. Caviness VS Jr. 1975. Architectonic map of neocortex of the normal mouse. J Comp Neurol. 164:247-263.
12. Chudasama Y, Robbins TW. 2003. Dissociable contributions of the orbitofrontal and infralimbic cortex to pavlovian autoshaping and discrimination reversal learning: further evidence for the functional heterogeneity of the rodent frontal cortex. J Neurosci. 23:8771-8780.
13. Dufour F, Schaer M, Debbane M, Farhoumand R, Glaser B, Eliez S. 2008. Cingulate gyral reductions are related to low executive functioning and psychotic symptoms in 22q 11.2 deletion syndrome. Neuropsychologia. 46:2986-2992.
14. Elsen GE, Hodge RD, Bedogni F, Daza RA, Nelson BR, Shiba N, Reiner SL, Hevner RF. 2013. The protomap is propagated to cortical plate neurons through an Eomes-dependent intermediate map. Proc Natl Acad Sci USA. 110:4081-4086.
15. Fukuchi-Shimogori T, Grove EA. 2001. Neocortex patterning by the secreted signaling molecule FGF8. Science. 294:1071-1074.
16. Gerdes M, Solot C, Wang PP, Moss E, LaRossa D, Randall P, Goldmuntz E, Clark BJ 3rd, Driscoll DA, Jawad A et al. 1999. Cognitive and behavior profile of preschool children with chromosome 22ql 1.2 deletion. Am J Med Genet. 85:127-133.
17. Geschwind DH, Levitt P. 2007. Autism spectrum disorders: developmental disconnection syndromes. Curr Opin Neurobiol. 17:103-111.
18. Glascher J, Adolphs R, Damasio H, Bechara A, Rudrauf D, Calamia M, Paul LK, Tranel D. 2012. Lesion mapping of cognitive control and value-based decision making in the prefrontal cortex. Proc Natl Acad Sci USA. 109:14681-14686.
19. Gonzalez-Burgos G, Fish KN, Lewis DA. 2011. GABA Neuron alterations, cortical circuit dysfunction and cognitive deficits in schizophrenia. Neural Plast. 2011:723184.
20. Hamasaki T, Leingartner A, Ringstedt T, O'Leary DD. 2004. EMX2 Regulates sizes and positioning of the primary sensory and motor areas in neocortex by direct specification of cortical progenitors. Neuron. 43:359-372.
21. Haskell GT, LaMantia AS. 2005. Retinoic acid signaling identifies a distinct precursor population in the developing and adult forebrain. J Neurosci. 25:7636-7647.
22. Jones MW. 2002. A comparative review of rodent prefrontal cortex and working memory. Curr Mol Med. 2:639-647.
23. Kao MH, Doupe AJ, Brainard MS. 2005. Contributions of an avian basal ganglia-forebrain circuit to real-time modulation of song. Nature. 433:638-643.
24. Karayiorgou M, Simon TJ, Gogos JA. 2010. 22qll.2 Microdeletions: linking DNA structural variation to brain dysfunction and schizophrenia. Nat Rev Neurosci. 11:402-416.
25. Kellendonk C, Simpson EH, Kandel ER. 2009. Modeling cognitive en-dophenotypes of schizophrenia in mice. Trends Neurosci. 32:347-358.
26. Kowalczyk T, Pontious A, Englund C, Daza RA, Bedogni F, Hodge R, Attardo A, Bell C, Huttner WB, Hevner RF. 2009. Intermediate neuronal progenitors (basal progenitors) produce pyramidal-projection neurons for all layers of cerebral cortex. Cereb Cortex. 19:2439-2450.
27. Lewis DA, Curley AA, Glausier JR, Volk DW. 2012. Cortical paralbumin interneurons and cognitive dysfunction in schizophrenia. Trends Neurosci. 35:57-67.
28. Lewis DA, Hashimoto T, Volk DW. 2005. Cortical inhibitory neurons and schizophrenia. Nat Rev Neurosci. 6:312-324.
29. Lewis DA, Volk DW, Hashimoto T. 2004. Selective alterations in prefrontal cortical GABA neurotransmission in schizophrenia: a novel target for the treatment of working memory dysfunction. Psychopharmacology (Berl). 174:143-150.
30. Long JM, LaPorte P, Merscher S, Funke B, Saint-Jore B, Puech A, Kucherlapati R, Morrow BE, Skoultchi AI, Wynshaw-Boris A. 2006. Behavior of mice with mutations in the conserved region deleted in velocardiofacial/DiGeorge syndrome. Neurogenetics. 7:247-257.
31. Matzel LD, Kolata S. 2010. Selective attention, working memory, and animal intelligence. Neurosci Biobehav Rev. 34:23-30.
32. Meechan DW, Maynard TM, Tucker ES, LaMantia AS. 2011. Three phases of DiGeorge/22qll deletion syndrome pathogenesis during brain development: patterning, proliferation, and mitochondrial functions of 22qll genes. Int J Dev Neurosci. 29:283-294.
33. Meechan DW, Tucker ES, Maynard TM, LaMantia AS. 2012. Cxcr4 regulation of interneuron migration is disrupted in 22qll.2 deletion syndrome. Proc Natl Acad Sci USA. 109:18601-18606.
34. Meechan DW, Tucker ES, Maynard TM, LaMantia AS. 2009. Diminished dosage of 22qll genes disrupts neurogenesis and cortical development in a mouse model of 22ql 1 deletion/DiGeorge syndrome. Proc Natl Acad Sci USA. 106:16434-16445.
35. Merscher S, Funke B, Epstein JA, Heyer J, Puech A, Lu MM, Xavier RJ, Demay MB, Russell RG, Factor S et al. 2001. TBX1 Is responsible for cardiovascular defects in velo-cardio-facial/DiGeorge syndrome. Cell. 104:619-629.
36. Molyneaux BJ, Arlotta P, Menezes JR, Macklis JD. 2007. Neuronal subtype specification in the cerebral cortex. Nat Rev Neurosci. 8:427-437.
37. Niklasson L, Rasmussen P, Oskarsdottir S, Gillberg C. 2009. Autism, ADHD, mental retardation and behavior problems in 100 individuals with 22qll deletion syndrome. Res Dev Disabil. 30:763-773.
38. Nonaka-Kinoshita M, Reillo I, Artegiani B, Angeles Martinez-Martinez M, Nelson M, Borrell V, Calegari F. 2013. Regulation of cerebral cortex size and folding by expansion of basal progenitors. EMBO J. 32:1817-1828.
39. Oram J, Geffen GM, Geffen LB, Kavanagh DJ, McGrath JJ. 2005. Executive control of working memory in schizophrenia. Psychiatry Res. 135:81-90.
40. Ottet MC, Schaer M, Cammoun L, Schneider M, Debbane M, Thiran JP, Eliez S. 2013. Reduced fronto-temporal and limbic connectivity in the 22qll.2 deletion syndrome: vulnerability markers for developing schizophrenia? PLoS One. 8:e58429.
41. Paylor R, Glaser B, Mupo A, Ataliotis P, Spencer C, Sobotka A, Sparks C, Choi CH, Oghalai J, Curran S et al. 2006. Tbxl haploinsufficiency is linked to behavioral disorders in mice and humans: implications for 22qll deletion syndrome. Proc Natl Acad Sci USA. 103:7729-7734.
42. Paylor R, Mcllwain KL, McAninch R, Nellis A, Yuva-Paylor LA, Baldini A, Lindsay EA. 2001. Mice deleted for the DiGeorge/velocardiofacial syndrome region show abnormal sensorimotor gating and learning and memory impairments. Hum Mol Genet. 10:2645-2650.
43. Powell SB, Zhou X, Geyer MA. 2009. Prepulse inhibition and genetic mouse models of schizophrenia. Behav Brain Res. 204:282-294.
44. Rutz HL, Rothblat LA. 2012. Intact and impaired executive abilities in the BTBR mouse model of autism. Behav Brain Res. 234:33-37.
45. Schaer M, Schmitt JE, Glaser B, Lazeyras F, Delavelle J, Eliez S. 2006. Abnormal patterns of cortical gyrification in velo-cardio-facial syndrome (deletion 22qll.2): anMRI study. Psychiatry Res. 146:1-11.
46. Shapiro HM, Wong LM, Simon TJ. 2013. A cross-sectional analysis of the development of response inhibition in children with chromosome 22qll.2 deletion syndrome. Front Psychiatry. 4:81.
47. Shashi V, Kwapil TR, Kaczorowski J, Berry MN, Santos CS, Howard TD, Goradia D, Prasad K, Vaibhav D, Rajarethinam R et al. 2010. Evidence of gray matter reduction and dysfunction in chromosome 22qll.2 deletion syndrome. Psychiatry Res. 181:1-8.
48. Sidman RL, Angevine JB, Pierce ET. 1971. Atlas of the mouse brain and spinal cord. Cambridge (MA): Harvard University Press, xi, 26l p. (chiefly illus.).
49. Siegenthaler JA, Ashique AM, Zarbalis K, Patterson KP, Hecht JH, Kane MA, Folias AE, Choe Y, May SR, Kume T et al. 2009. Retinoic acid from the meninges regulates cortical neuron generation. Cell. 139:597-609.
50. Sigurdsson T, Stark KL, Karayiorgou M, Gogos JA, Gordon JA. 2010. Impaired hippocampal-prefrontal synchrony in a genetic mouse model of schizophrenia. Nature. 464:763-767.
51. Simon TJ, Ding L, Bish JP, McDonald-McGinn DM, Zackai EH, Gee J. 2005. Volumetric, connective, and morphologic changes in the brains of children with chromosome 22qll.2 deletion syndrome: an integrative study. Neuroimage. 25:169-180.
52. Stark KL, Xu B, Bagchi A, Lai WS, Liu H, Hsu R, Wan X, Pavlidis P, Mills AA, Karayiorgou M et al. 2008. Altered brain microRNA biogenesis contributes to phenotypic deficits in a 22qll-deletion mouse model. Nat Genet. 40:751-760.
53. Swillen A, Vandeputte L, Cracco J, Maes B, Ghesquiere P, Devriendt K, Fryns JP. 1999. Neuropsychological, learning and psychosocial profile of primary school aged children with the velo-cardio-facial syndrome (22qll deletion): evidence for a nonverbal learning disability? Child Neuropsychol. 5:230-241.
54. van der Staay FJ, Steckler T. 2001. Behavioural phenotyping of mouse mutants. Behav Brain Res. 125:3-12.
55. Van De Werd HJ, Rajkowska G, Evers P, Uylings HB. 2010. Cytoarchi-tectonic and chemoarchitectonic characterization of the prefrontal cortical areas in the mouse. Brain Struct Funct. 214:339-353.
56. Volk DW, Lewis DA. 2005. GABA Targets for the treatment of cognitive dysfunction in schizophrenia. Curr Neuropharmacol. 3:45-62.
57. Wang F, Zhu J, Zhu H, Zhang Q, Lin Z, Hu H. 2011. Bidirectional control of social hierarchy by synaptic efficacy in medial prefrontal cortex. Science. 334:693-697.
58. Woo NH, Lu B. 2006. Regulation of cortical interneurons by neurotro-phins: from development to cognitive disorders. Neuroscientist. 12:43-56.
59. Woodin M, Wang PP, Aleman D, McDonald-McGinn D, Zackai E, Moss E. 2001. Neuropsychological profile of children and adolescents with the 22ql 1.2 microdeletion. Genet Med. 3:34-39.