Strains and stressors: An analysis of touchscreen learning in genetically diverse mouse strains

PLoS ONE

Volumn 9, Issue 2, 2014, Pages

  Graybeal, Carolyn ^a   Bachu, Munisa ^a   Mozhui, Khyobeni ^b   Saksida, Lisa M ^c   Bussey, Timothy J ^c   Sagalyn, Erica ^a   Williams, Robert W ^b   Holmes, Andrew ^a  

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

^b UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^c UK   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; C57BL 6 MOUSE; CONTROLLED STUDY; DBA 2 MOUSE; DISPLAY SYSTEM; ENVIRONMENTAL STRESS; FORCED SWIM TEST; GENETIC DIFFERENCE; GENETIC VARIABILITY; GENOTYPE PHENOTYPE CORRELATION; INSTRUMENTAL CONDITIONING; LEARNING; MALE; MOTIVATION; MOUSE; MOUSE STRAIN; NONHUMAN; PRINCIPAL COMPONENT ANALYSIS; QUANTITATIVE ANALYSIS; REINFORCEMENT; STIMULUS RESPONSE; STRAIN DIFFERENCE; TASK PERFORMANCE; TOUCHSCREEN SYSTEM; VISUAL DISCRIMINATION; ANIMAL; GENETICS; INBREEDING; MENTAL STRESS; PATHOPHYSIOLOGY; PERCEPTIVE DISCRIMINATION; PHYSIOLOGY; SPECIES DIFFERENCE; TECHNOLOGY;

ANIMALS; BEHAVIOR, ANIMAL; DISCRIMINATION (PSYCHOLOGY); INBREEDING; LEARNING; MALE; MICE; PRINCIPAL COMPONENT ANALYSIS; REVERSAL LEARNING; SPECIES SPECIFICITY; STRESS, PSYCHOLOGICAL; TECHNOLOGY;

EID: 84896753617     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0087745     Document Type: Article

References (61)

1. Bussey TJ, Holmes A, Lyon L, Mar AC, McAllister KA, et al. (2011) New translational assays for preclinical modelling of cognition in schizophrenia: the touchscreen testing method for mice and rats. Neuropharmacology 62: 1191-1203.
2. Nithianantharajah J, Komiyama NH, McKechanie A, Johnstone M, Blackwood DH, et al. (2013) Synaptic scaffold evolution generated components of vertebrate cognitive complexity. Nat Neurosci 16: 16-24.
3. Brigman JL, Rothblat LA (2007) Stimulus specific deficit on visual reversal learning after lesions of medial prefrontal cortex in the mouse. Behav Brain Res.
4. Brigman JL, Daut RA, Wright T, Gunduz-Cinar O, Graybeal C, et al. (2013) GluN2B in corticostriatal circuits governs choice learning and choice shifting. Nat Neurosci.
5. Barkus C, Feyder M, Graybeal C, Wright T, Wiedholz L, et al. (2012) Do GluA1 knockout mice exhibit behavioral abnormalities relevant to the negative or cognitive symptoms of schizophrenia and schizoaffective disorder? Neuropharmacology 62: 1263-1272.
6. Karlsson RM, Tanaka K, Saksida LM, Bussey TJ, Heilig M, et al. (2009) Assessment of glutamate transporter GLAST (EAAT1)-deficient mice for phenotypes relevant to the negative and executive/cognitive symptoms of schizophrenia. Neuropsychopharmacology 34: 1578-1589.
7. Brigman JL, Padukiewicz KE, Sutherland ML, Rothblat LA (2006) Executive functions in the heterozygous reeler mouse model of schizophrenia. Behav Neurosci 120: 984-988.
8. Brigman JL, Mathur P, Harvey-White J, Izquierdo A, Saksida LM, et al. (2010) Pharmacological or genetic inactivation of the serotonin transporter improves reversal learning in mice. Cereb Cortex 20: 1955-1963.
9. Brigman JL, Feyder M, Saksida LM, Bussey TJ, Mishina M, et al. (2008) Impaired discrimination learning in mice lacking the NMDA receptor NR2A subunit. Learn Mem 15: 50-54. (Pubitemid 351281563)
10. Brigman JL, Daut R, Wright T, Gunduz Cinar O, Graybeal C, et al. (2013) GluN2B in corticostriatal circuits governs choice learning and choice shifting. Nat Neurosci in press.
11. Brigman JL, Ihne J, Saksida LM, Bussey TJ, Holmes A (2009) Effects of Subchronic Phencyclidine (PCP) Treatment on Social Behaviors, and Operant Discrimination and Reversal Learning in C57BL/6J Mice. Front Behav Neurosci 3: 2.
12. Izquierdo A, Jentsch JD (2012) Reversal learning as a measure of impulsive and compulsive behavior in addictions. Psychopharmacology (Berl) 219: 607-620.
13. Graybeal C, Feyder M, Schulman E, Saksida LM, Bussey TJ, et al. (2011) Paradoxical reversal learning enhancement by stress or prefrontal cortical damage: rescue with BDNF. Nat Neurosci 14: 1507-1509.
14. DePoy L, Daut R, Brigman JL, Macpherson K, Crowley N, et al. (2013) Chronic alcohol produces neuroadaptations to prime dorsal striatal learning. Proc Natl Acad Sci U S A 110: 14783-14788.
15. Lederle L, Weber S, Wright T, Feyder M, Brigman JL, et al. (2011) Reward-related behavioral paradigms for addiction research in the mouse: performance of common inbred strains. PLoS One 6: e15536.
16. Horner AE, Heath CJ, Hvoslef-Eide M, Kent BA, Kim CH, et al. (2013) The touchscreen operant platform for testing learning and memory in rats and mice. Nat Protoc 8: 1961-1984.
17. Mar AC, Horner AE, Nilsson SR, Alsio J, Kent BA, et al. (2013) The touchscreen operant platform for assessing executive function in rats and mice. Nat Protoc 8: 1985-2005.
18. Knapman A, Heinzmann JM, Holsboer F, Landgraf R, Touma C (2010) Modeling psychotic and cognitive symptoms of affective disorders: Disrupted latent inhibition and reversal learning deficits in highly stress reactive mice. Neurobiology of Learning and Memory 94: 145-152.
19. Francis DD, Zaharia MD, Shanks N, Anisman H (1995) Stress-induced disturbances in Morris water-maze performance: interstrain variability. Physiol Behav 58: 57-65.
20. Brooks SP, Pask T, Jones L, Dunnett SB (2005) Behavioural profiles of inbred mouse strains used as transgenic backgrounds. II: cognitive tests. Genes Brain Behav 4: 307-317. (Pubitemid 41002406)
21. Mineur YS, Belzung C, Crusio WE (2007) Functional implications of decreases in neurogenesis following chronic mild stress in mice. Neuroscience 150: 251-259. (Pubitemid 350198721)
22. Loos M, Staal J, Schoffelmeer AN, Smit AB, Spijker S, et al. (2010) Inhibitory control and response latency differences between C57BL/6J and DBA/2J mice in a Go/No-Go and 5-choice serial reaction time task and strain-specific responsivity to amphetamine. Behav Brain Res 214: 216-224.
23. Patel S, Stolerman IP, Asherson P, Sluyter F (2006) Attentional performance of C57BL/6 and DBA/2 mice in the 5-choice serial reaction time task. Behav Brain Res 170: 197-203. (Pubitemid 43732352)
24. Helms CM, Reeves JM, Mitchell SH (2006) Impact of strain and D-amphetamine on impulsivity (delay discounting) in inbred mice. Psychopharmacology (Berl) 188: 144-151. (Pubitemid 44371152)
25. Gubner NR, Wilhelm CJ, Phillips TJ, Mitchell SH (2010) Strain differences in behavioral inhibition in a Go/No-go task demonstrated using 15 inbred mouse strains. Alcohol Clin Exp Res 34: 1353-1362.
26. Isles AR, Humby T, Walters E, Wilkinson LS (2004) Common genetic effects on variation in impulsivity and activity in mice. J Neurosci 24: 6733-6740. (Pubitemid 38993893)
27. Baron SP, Meltzer LT (2001) Mouse strains differ under a simple schedule of operant learning. Behavioural Brain Research 118: 143-152. (Pubitemid 32063375)
28. Crusio WE, Goldowitz D, Holmes A, Wolfer D (2009) Standards for the publication of mouse mutant studies. Genes Brain Behav 8: 1-4.
29. Hefner K, Whittle N, Juhasz J, Norcross M, Karlsson RM, et al. (2008) Impaired fear extinction learning and cortico-amygdala circuit abnormalities in a common genetic mouse strain. J Neurosci 28: 8074-8085.
30. Taylor BA (1978) Recombinant inbred strains: use in gene mapping. In: Morse HC, editor. Origins of Inbred Mice. New York: Academic Press. pp. 423-438.
31. Mozhui K, Karlsson RM, Kash TL, Ihne J, Norcross M, et al. (2010) Strain differences in stress responsivity are associated with divergent amygdala gene expression and glutamate-mediated neuronal excitability. J Neurosci 30: 5357-5367.
32. Millstein RA, Holmes A (2007) Effects of repeated maternal separation on anxiety- and depression-related phenotypes in different mouse strains. Neurosci Biobehav Rev 31: 3-17. (Pubitemid 44880075)
33. Millstein RA, Ralph RJ, Yang RJ, Holmes A (2006) Effects of repeated maternal separation on prepulse inhibition of startle across inbred mouse strains. Genes Brain Behav 5: 346-354. (Pubitemid 43794817)
34. Bogue MA, Grubb SC (2004) The Mouse Phenome Project. Genetica 122: 71-74. (Pubitemid 39459526)
35. Izquierdo A, Wiedholz LM, Millstein RA, Yang RJ, Bussey TJ, et al. (2006) Genetic and dopaminergic modulation of reversal learning in a touchscreen-based operant procedure for mice. Behav Brain Res 171: 181-188. (Pubitemid 43946491)
36. Kiselycznyk C, Holmes A (2011) All (C57BL/6) Mice are not Created Equal. Front Neurosci 5: 10.
37. Siegmund A, Langnaese K, Wotjak CT (2005) Differences in extinction of conditioned fear in C57BL/6 substrains are unrelated to expression of alpha-synuclein. Behav Brain Res 157: 291-298. (Pubitemid 40082572)
38. Hegmann JP, Possidente B (1981) Estimating genetic correlations from inbred strains. Behav Genet 11: 103-114. (Pubitemid 11122657)
39. Brigman JL, Mathur P, Lu L, Williams RW, Holmes A (2009) Genetic relationship between anxiety-related and fear-related behaviors in BXD recombinant inbred mice. Behav Pharmacol 20: 204-209.
40. Holmes A, Rodgers RJ (1998) Responses of Swiss-Webster mice to repeated plus-maze experience: further evidence for a qualitative shift in emotional state? Pharmacol Biochem Behav 60: 473-488. (Pubitemid 28282689)
41. Afonso C, Paixao VB, Costa RM (2012) Chronic Toxoplasma infection modifies the structure and the risk of host behavior. PLoS ONE 7: e32489.
42. Lê S, Josse J, Husson F (2008) FactoMineR: An R Package for Multivariate Analysis. Journal of Statistical Software 25: 1-18.
43. Tsang SH, Woodruff ML, Jun L, Mahajan V, Yamashita CK, et al. (2007) Transgenic mice carrying the H258N mutation in the gene encoding the betasubunit of phosphodiesterase-6 (PDE6B) provide a model for human congenital stationary night blindness. Hum Mutat 28: 243-254.
44. Wong AA, Brown RE (2006) Visual detection, pattern discrimination and visual acuity in 14 strains of mice. Genes Brain Behav 5: 389-403. (Pubitemid 44000924)
45. Nguyen PV, Abel T, Kandel ER, Bourtchouladze R (2000) Strain-dependent differences in LTP and hippocampus-dependent memory in inbred mice. Learn Mem 7: 170-179. (Pubitemid 30407782)
46. O'Leary TP, Savoie V, Brown RE (2011) Learning, memory and search strategies of inbred mouse strains with different visual abilities in the Barnes maze. Behav Brain Res 216: 531-542.
47. Camp M, Norcross M, Whittle N, Feyder M, D'Hanis W, et al. (2009) Impaired Pavlovian fear extinction is a common phenotype across genetic lineages of the 129 inbred mouse strain. Genes Brain Behav 8: 744-752.
48. Brown RE, Wong AA (2007) The influence of visual ability on learning and memory performance in 13 strains of mice. Learn Mem 14: 134-144. (Pubitemid 46495190)
49. Owen EH, Logue SF, Rasmussen DL, Wehner JM (1997) Assessment of learning by the Morris water task and fear conditioning in inbred mouse strains and F1 hybrids: implications of genetic background for single gene mutations and quantitative trait loci analyses. Neuroscience 80: 1087-1099. (Pubitemid 27359794)
50. Holmes A, Wrenn CC, Harris AP, Thayer KE, Crawley JN (2002) Behavioral profiles of inbred strains on novel olfactory, spatial and emotional tests for reference memory in mice. Genes Brain Behav 1: 55-69. (Pubitemid 37121824)
51. Paylor R, Baskall L, Wehner JM (1993) Behavioral dissociations between C57BL/6 and DBA/2 mice on learning and memory tasks: A hippocampal dysfunction hypothesis. Psychobiology 21: 11-26. (Pubitemid 23105849)
52. Sokoloff G, Parker CC, Lim JE, Palmer AA (2011) Anxiety and fear in a cross of C57BL/6J and DBA/2J mice: mapping overlapping and independent QTL for related traits. Genes Brain Behav 10: 604-614.
53. Passino E, Middei S, Restivo L, Bertaina-Anglade V, Ammassari-Teule M (2002) Genetic approach to variability of memory systems: analysis of place vs. response learning and fos-related expression in hippocampal and striatal areas of C57BL/6 and DBA/2 mice. Hippocampus 12: 63-75. (Pubitemid 34211248)
54. Crusio WE, Schwegler H, Lipp HP (1987) Radial-maze performance and structural variation of the hippocampus in mice: a correlation with mossy fibre distribution. Brain Res 425: 182-185. (Pubitemid 17159383)
55. Mihalick SM, Langlois JC, Krienke JD (2000) Strain and sex differences on olfactory discrimination learning in C57BL/6J and DBA/2J inbred mice (Mus musculus). J Comp Psychol 114: 365-370.
56. D'Este L, Casini A, Puglisi-Allegra S, Cabib S, Renda TG (2007) Comparative immunohistochemical study of the dopaminergic systems in two inbred mouse strains (C57BL/6J and DBA/2J). J Chem Neuroanat 33: 67-74. (Pubitemid 46350748)
57. Puglisi-Allegra S, Cabib S (1997) Psychopharmacology of dopamine: the contribution of comparative studies in inbred strains of mice. Prog Neurobiol 51: 637-661. (Pubitemid 27244540)
58. Colelli V, Fiorenza MT, Conversi D, Orsini C, Cabib S (2010) Strain-specific proportion of the two isoforms of the dopamine D2 receptor in the mouse striatum: associated neural and behavioral phenotypes. Genes Brain Behav 9: 703-711.
59. Hitzemann R, Hitzemann B, Rivera S, Gatley J, Thanos P, et al. (2003) Dopamine D2 receptor binding, Drd2 expression and the number of dopamine neurons in the BXD recombinant inbred series: genetic relationships to alcohol and other drug associated phenotypes. Alcohol Clin Exp Res 27: 1-11. (Pubitemid 36164241)
60. Boyce-Rustay JM, Cameron HA, Holmes A (2007) Chronic swim stress alters sensitivity to acute behavioral effects of ethanol in mice. Physiol Behav 91: 77-86. (Pubitemid 46616879)
61. Laughlin RE, Grant TL, Williams RW, Jentsch JD (2011) Genetic dissection of behavioral flexibility: reversal learning in mice. Biol Psychiatry 69: 1109-1116.