16p11.2 Deletion mice display cognitive deficits in touchscreen learning and novelty recognition tasks

Learning and Memory

Volumn 22, Issue 12, 2015, Pages 622-632

  Yang, Mu ^a   Lewis, Freeman C ^a   Sarvi, Michael S ^a   Foley, Gillian M ^a   Crawley, Jacqueline N ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; AMNESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CHROMOSOME 16P; CHROMOSOME DELETION; CHROMOSOME DELETION 16P11; COGNITIVE DEFECT; CONTROLLED STUDY; DISCRIMINATION LEARNING; FEAR; FEMALE; GENOTYPE; HABITUATION; HETEROZYGOTE; LEARNING; LEARNING DISORDER; MALE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RECOGNITION; SPATIAL LEARNING; VISUAL DISCRIMINATION; ANIMAL; ASSOCIATION; AUTISM; CHROMOSOME 16; CHROMOSOME DISORDER; COGNITION DISORDERS; COMPLICATION; CONDITIONING; GENETICS; INTELLECTUAL IMPAIRMENT; LEARNING DISORDERS; PATHOPHYSIOLOGY; PERCEPTION; PERCEPTIVE DISCRIMINATION; PSYCHOLOGIC TEST; PSYCHOLOGY; SPATIAL MEMORY; SWIMMING; TRANSGENIC MOUSE; VISION;

ANIMALS; AUTISTIC DISORDER; CHROMOSOME DELETION; CHROMOSOME DISORDERS; CHROMOSOMES, HUMAN, PAIR 16; COGNITION DISORDERS; CONDITIONING (PSYCHOLOGY); CUES; DISCRIMINATION (PSYCHOLOGY); FEAR; FEMALE; HETEROZYGOTE; INTELLECTUAL DISABILITY; LEARNING; LEARNING DISORDERS; MALE; MICE, TRANSGENIC; PSYCHOLOGICAL TESTS; RECOGNITION (PSYCHOLOGY); REVERSAL LEARNING; SOCIAL PERCEPTION; SPATIAL MEMORY; SWIMMING; VISUAL PERCEPTION;

EID: 84950155486     PISSN: 10720502     EISSN: 15495485     Source Type: Journal    
DOI: 10.1101/lm.039602.115     Document Type: Article

References (66)

1. Bijlsma EK, Gijsbers AC, Schuurs-Hoeijmakers JH, van Haeringen A, Fransen van de Putte DE, Anderlid BM, Lundin J, Lapunzina P, Perez Jurado LA, Delle Chiaie B, et al. 2009. Extending the phenotype of recurrent rearrangements of 16p11.2: deletions in mentally retarded patients without autism and in normal individuals. Eur J Med Genet 52: 77-87.
2. Bissonette GB, Martins GJ, Franz TM, Harper ES, Schoenbaum G, Powell EM 2008. Double dissociation of the effects of medial and orbital prefrontal cortical lesions on attentional and affective shifts in mice. J Neurosci 28: 11124-11130.
3. Bissonette GB, Schoenbaum G, Roesch MR, Powell EM 2015. Interneurons are necessary for coordinated activity during reversal learning in orbitofrontal cortex. Biol Psychiatry 77: 454-464.
4. 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.
5. Brigman JL, Daut RA, Wright T, Gunduz-Cinar O, Graybeal C, Davis MI, Jiang Z, Saksida LM, Jinde S, Pease M, et al 2013. GluN2B in corticostriatal circuits governs choice learning and choice shifting. Nat Neurosci 16: 1101-1110.
6. Brown MW, Warburton EC, Aggleton JP 2010. Recognition memory: material, processes, and substrates. Hippocampus 20: 1228-1244.
7. Bussey TJ, Duck J, Muir JL, Aggleton JP 2000. Distinct patterns of behavioural impairments resulting from fornix transection or neurotoxic lesions of the perirhinal and postrhinal cortices in the rat. Behav Brain Res 111: 187-202.
8. Bussey TJ, Padain TL, Skillings EA, Winters BD, Morton AJ, Saksida LM 2008. The touchscreen cognitive testing method for rodents: howtoget the best out of your rat. Learn Mem 15: 516-523.
9. Bussey TJ, Holmes A, Lyon L, Mar AC, McAllister KA, Nithianantharajah J, Oomen CA, Saksida LM 2012. New translational assays for preclinical modelling of cognition in schizophrenia: the touchscreen testing method for mice and rats. Neuropharmacology 62: 1191-1203.
10. DePoy L, Daut R, Brigman JL, MacPherson K, Crowley N, Gunduz-Cinar O, Pickens CL, Cinar R, Saksida LM, Kunos G, et al 2013. Chronic alcohol produces neuroadaptations to prime dorsal striatal learning. Proc Natl Acad Sci 110: 14783-14788.
11. Dere E, Huston JP, De Souza Silva MA. 2007. The pharmacology, neuroanatomy and neurogenetics of one-trial object recognition in rodents. Neurosci Biobehav Rev 31: 673-704.
12. DeVito LM, Eichenbaum H. 2010. Distinct contributions of the hippocampus and medial prefrontal cortex to the "what-where-when" components of episodic-like memory in mice. Behav Brain Res 215: 318-325.
13. Duyzend MH, Eichler EE 2015. Genotype-first analysis of the 16p11.2 deletion defines a new type of "autism". Biol Psychiatry 77: 769-771.
14. Ennaceur A, Neave N, Aggleton JP 1997. Spontaneous object recognition and object location memory in rats: the effects of lesions in the cingulate cortices, the medial prefrontal cortex, the cingulum bundle and the fornix. Exp Brain Res 113: 509-519.
15. Fagan JF III, Singer LT, Montie JE, Shepherd PA. 1986. Selective screening device for the early detection of normal or delayed cognitive development in infants at risk for later mental retardation. Pediatrics 78: 1021-1026.
16. Ferguson JN, Aldag JM, Insel TR, Young LJ 2001. Oxytocin in the medial amygdala is essential for social recognition in the mouse. J Neurosci 21: 8278-8285.
17. Ferguson JN, Young LJ, Insel TR 2002. The neuroendocrine basis of social recognition. Front Neuroendocrinol 23: 200-224.
18. Fernandez BA, Roberts W, Chung B, Weksberg R, Meyn S, Szatmari P, Joseph-George AM, Mackay S, Whitten K, Noble B, et al. 2010. Phenotypic spectrum associated with de novo and inherited deletions and duplications at 16p11.2 in individuals ascertained for diagnosis of autism spectrum disorder. J Med Genet 47: 195-203.
19. Forwood SE, Winters BD, Bussey TJ 2005. Hippocampal lesions that abolish spatial maze performance spare object recognition memory at delays of up to 48 hours. Hippocampus 15: 347-355.
20. Goodyear RJ, Jones SM, Sharifi L, Forge A, Richardson GP 2012. Hair bundle defects and loss of function in the vestibular end organs of mice lacking the receptor-like inositol lipid phosphatase PTPRQ. J Neurosci 32: 2762-2772.
21. Guilmatre A, Dubourg C, Mosca AL, Legallic S, Goldenberg A, Drouin-Garraud V, Layet V, Rosier A, Briault S, Bonnet-Brilhault F, et al 2009. Recurrent rearrangements in synaptic and neurodevelopmental genes and shared biologic pathways in schizophrenia, autism, and mental retardation. Arch Gen Psychiatry 66: 947-956.
22. Hamilton DA, Brigman JL 2015. Behavioral flexibility in rats and mice: contributions of distinct frontocortical regions. Genes Brain Behav 14: 4-21.
23. Hanson E, Nasir RH, Fong A, Lian A, Hundley R, Shen Y, Wu BL, Holm IA, Miller DT 2010. Cognitive and behavioral characterization of 16p11.2 deletion syndrome. J Dev Behav Pediatr 31: 649-657.
24. Hanson E, Bernier R, Porche K, Jackson FI, Goin-Kochel RP, Snyder LG, Snow AV, Wallace AS, Campe KL, Zhang Y, et al 2015. The cognitive and behavioral phenotype of the 16p11.2 deletion in a clinically ascertained population. Biol Psychiatry 77: 785-793.
25. Horev G, Ellegood J, Lerch JP, Son YE, Muthuswamy L, Vogel H, Krieger AM, Buja A, Henkelman RM, Wigler M, et al 2011. Dosage-dependent phenotypes in models of 16p11.2 lesions found in autism. Proc Natl Acad Sci 108: 17076-17081.
26. Horner AE, Heath CJ, Hvoslef-Eide M, Kent BA, Kim CH, Nilsson SR, Alsiö J, Oomen CA, Holmes A, Saksida LM, et al. 2013. The touchscreen operant platform for testing learning and memory in rats and mice. Nat Protoc 8: 1961-1984.
27. Kesner RP, Hunsaker MR 2010. The temporal attributes of episodic memory. Behav Brain Res 215: 299-309.
28. Kesner RP, Hunt ME, Williams JM, Long JM 1996. Prefrontal cortex and working memory for spatial response, spatial location, and visual object information in the rat. Cereb Cortex 6: 311-318.
29. B receptor antagonists. J Neurosci 32: 9217-9227.
30. Manns JR, Eichenbaum H. 2009. A cognitive map for object memory in the hippocampus. Learn Mem 16: 616-624.
31. Marshall CR, Noor A, Vincent JB, Lionel AC, Feuk L, Skaug J, Shago M, Moessner R, Pinto D, Ren Y, et al. 2008. Structural variation of chromosomes in autism spectrum disorder. Am J Hum Genet 82: 477-488.
32. Moreno-De-Luca A, Evans DW, Boomer KB, Hanson E, Bernier R, Goin-Kochel RP, Myers SM, Challman TD, Moreno-De-Luca D, Slane MM, et al. 2015. The role of parental cognitive, behavioral, and motor profiles in clinical variability in individuals with chromosome 16p11.2 deletions. JAMA Psychiatry 72: 119-126.
33. Moy SS, Nadler JJ, Perez A, Barbaro RP, Johns JM, Magnuson TR, Piven J, Crawley JN 2004. Sociability and preference for social novelty in five inbred strains: an approach to assess autistic-like behavior in mice. Genes Brain Behav 3: 287-302.
34. Owen JP, Chang YS, Pojman NJ, Bukshpun P, Wakahiro ML, Marco EJ, Berman JI, Spiro JE, Chung WK, Buckner RL, et al 2014. Aberrant white matter microstructureinchildren with 16p11.2 deletions. J Neurosci 34: 6214-6223.
35. Paffenholz R, Bergstrom RA, Pasutto F, Wabnitz P, Munroe RJ, Jagla W, Heinzmann U, Marquardt A, Bareiss A, Laufs J, et al 2004. Vestibular defects in head-tilt mice result from mutations in Nox3, encoding an NADPH oxidase. Genes Dev 18: 486-491.
36. Petkov PM, Ding Y, Cassell MA, Zhang W, Wagner G, Sargent EE, Asquith S, Crew V, Johnson KA, Robinson P, et al. 2004. An efficient SNP system for mouse genome scanning and elucidating strain relationships. Genome Res 14: 1806-1811.
37. Poplawski SG, Schoch H, Wimmer ME, Hawk JD, Walsh JL, Giese KP, Abel T. 2014. Object-location training elicits an overlapping but temporally distinct transcriptional profile from contextual fear conditioning. Neurobiol Learn Mem 116: 90-95.
38. Portmann T, Yang M, Mao R, Panagiotakos G, Ellegood J, Bader P, Dolen G, Grueter BA, Fisher E, Rengarajan P, et al. 2014. Behavioral abnormalities and circuit defects in the basal ganglia of a mouse model of 16p11.2 deletion syndrome. Cell Rep 7: 1077-1092.
39. Pucilowska J, Vithayathil J, Tavares EJ, Kelly C, Karlo JC, Landreth GE 2015. The 16p11.2 deletion mouse model of autism exhibits altered cortical progenitor proliferation and brain cytoarchitecture linked to the ERK MAPK pathway. J Neurosci 35: 3190-3200.
40. Puvabanditsin S, Nagar MS, Joshi M, Lambert G, Garrow E, Brandsma E. 2010. Microdeletion of 16p11.2 associated with endocardial fibroelastosis. Am J Med Genet A 152A: 2383-2386.
41. Qureshi AY, Mueller S, Snyder AZ, Mukherjee P, Berman JI, Roberts TPL, Nagarajan SS, Spiro JE, Chung WK, Sherr EH, et al 2014. Opposing brain differencesin16p11.2 deletion and duplication carriers. J Neurosci 34: 11199-11211.
42. Raca G, Baas BS, Kirmani S, Laffin JJ, Jackson CA, Strand EA, Jakielski KJ, Shriberg LD 2013. Childhood Apraxia of Speech (CAS) in two patients with 16p11.2 microdeletion syndrome. Eur J Hum Genet 21: 455-459.
43. Ragozzino ME. 2007. The contribution of the medial prefrontal cortex, orbitofrontal cortex, and dorsomedial striatumtobehavioralflexibility. Ann N Y Acad Sci 1121: 355-375.
44. Richter K, Wolf G, Engelmann M. 2005. Social recognition memory requires two stages of protein synthesis in mice. Learn Mem 12: 407-413.
45. Robbins TW, James M, Owen AM, Sahakian BJ, McInnes L, Rabbitt P. 1994. Cambridge Neuropsychological Test Automated Battery (CANTAB): a factor analytic study of a large sample of normal elderly volunteers. Dementia 5: 266-281.
46. Rosenberg C, Knijnenburg J, Bakker E, Vianna-Morgante AM, Sloos W, Otto PA, Kriek M, Hansson K, Krepischi-Santos AC, Fiegler H, et al 2006. Array-CGH detection of micro rearrangements in mentally retarded individuals: clinical significance of imbalances present both in affected children and normal parents. J Med Genet 43: 180-186.
47. Rosenfeld JA, Coppinger J, Bejjani BA, Girirajan S, Eichler EE, Shaffer LG, Ballif BC 2010. Speech delays and behavioral problems are the predominant features in individuals with developmental delays and 16p11.2 microdeletions and microduplications. J Neurodev Disord 2: 26-38.
48. Ross HE, Young LJ 2009. Oxytocin and the neural mechanisms regulating social cognition and affiliative behavior. Front Neuroendocrinol 30: 534-547.
49. Shinawi M, Liu P, Kang SH, Shen J, Belmont JW, Scott DA, Probst FJ, Craigen WJ, Graham BH, Pursley A, et al 2010. Recurrent reciprocal 16p11.2 rearrangements associated with global developmental delay, behavioural problems, dysmorphism, epilepsy, and abnormal head size. J Med Genet 47: 332-341.
50. Silverman JL, Turner SM, Barkan CL, Tolu SS, Saxena R, Hung AY, Sheng M, Crawley JN 2011. Sociability and motor functions in Shank1 mutant mice. Brain Res 1380: 120-137.
51. Silverman JL, Gastrell PT, Karras MN, Solomon M, Crawley JN 2015. Cognitive abilities on transitive inference using a novel touchscreen technology for mice. Cereb Cortex 25: 1133-1142.
52. Smith GK, Kesner RP, Korenberg JR 2014. Dentate gyrus mediates cognitive function in the Ts65Dn/DnJ mouse model of Down syndrome. Hippocampus 24: 354-362.
53. Stefansson H, Meyer-Lindenberg A, Steinberg S, Magnusdottir B, Morgen K, Arnarsdottir S, Bjornsdottir G, Walters GB, Jonsdottir GA, Doyle OM, et al. 2014. CNVs conferring risk of autism or schizophrenia affect cognition in controls. Nature 505: 361-366.
54. Steinberg S, de Jong S, Mattheisen M, Costas J, Demontis D, Jamain S, Pietiläinen OP, Lin K, Papiol S, Huttenlocher J, et al. 2014. Common variant at 16p11.2 conferring risk of psychosis. Mol Psychiatry 19: 108-114.
55. Sutcliffe JS, Marshall KM, Neill JC 2007. Influence of gender on working and spatial memory in the novel object recognition task in the rat. Behav Brain Res 177: 117-125.
56. Tian D, Stoppel LJ, Heynen AJ, Lindemann L, Jaeschke G, Mills AA, Bear MF. 2015. Contribution of mGluR5 to pathophysiology in a mouse model of human chromosome 16p11.2 microdeletion. Nat Neurosci 18: 182-184.
57. Vogel-Ciernia A, Wood MA 2014. Examining object location and object recognition memory in mice. Curr Protoc Neurosci 69: 83131-383117.
58. Walsh KM, Bracken MB 2011. Copy number variation in the dosage-sensitive 16p11.2 interval accounts for only a small proportion of autism incidence: a systematic review and meta-analysis. Genet Med 13: 377-384.
59. Weiss LA, Shen Y, Korn JM, Arking DE, Miller DT, Fossdal R, Saemundsen E, Stefansson H, Ferreira MA, Green T, et al 2008. Association between microdeletion and microduplication at 16p11.2 and autism. N Engl J Med 358: 667-675.
60. Wimmer ME, Hernandez PJ, Blackwell J, Abel T. 2012. Aging impairs hippocampus-dependent long-term memory for object location in mice. Neurobiol Aging 33: 2220-2224.
61. Winters BD, Forwood SE, Cowell RA, Saksida LM, Bussey TJ 2004. Double dissociation between the effects of peri-postrhinal cortex and hippocampal lesionsontests of object recognition and spatial memory: heterogeneity of function within the temporal lobe. J Neurosci 24: 5901-5908.
62. Yang M, Silverman JL, Crawley JN 2011. Automated three-chambered social approach task for mice. Curr Protoc Neurosci Chapter 8: Unit 8 26.
63. Yang M, Bozdagi O, Scattoni ML, Wöhr M, Roullet FI, Katz AM, Abrams DN, Kalikhman D, Simon H, Woldeyohannes L, et al. 2012. Reduced excitatory neurotransmission and mild autism-relevant phenotypes in adolescent Shank3 null mutant mice. J Neurosci 32: 6525-6541.
64. Yang M, Lewis FC, Foley G, Crawley JN 2015a. In tribute to Bob Blanchard: divergent behavioral phenotypes of 16p11.2 deletion mice reared in same-genotype versus mixed-genotype cages. Physiol Behav 146: 16-27.
65. Yang M, Mahrt EJ, Lewis F, Foley G, Portmann T, Dolmetsch RE, Portfors CV, Crawley JN 2015b. 16p11.2 deletion syndrome mice display sensory and ultrasonic vocalization deficits during social interactions. Autism Res doi: 10.1002/aur.1465.
66. Zufferey F, Sherr EH, Beckmann ND, Hanson E, Maillard AM, Hippolyte L, Macé A, Ferrari C, Kutalik Z, Andrieux J, et al. 2012. A 600 kb deletion syndrome at 16p11.2 leads to energy imbalance and neuropsychiatric disorders. J Med Genet 49: 660-668.