Impulsivity, decreased social exploration, and executive dysfunction in a mouse model of frontotemporal dementia

Neurobiology of Learning and Memory

Volumn 130, Issue , 2016, Pages 34-43

  Van der Jeugd, Ann ^a,b   Vermaercke, Ben ^b   Halliday, Glenda M ^c   Staufenbiel, Matthias ^d   Götz, Jürgen ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b UNIVERSITY OF LEUVEN   (Belgium)

^c NEUROSCIENCE RESEARCH AUSTRALIA   (Australia)

^d UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Behavior; Executive function; Frontotemporal dementia; Frontotemporal lobar degeneration; Social exploration; Tau

Indexed keywords

TAU PROTEIN;

AGED; AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY DISORDER; AROUSAL; ARTICLE; BODY WEIGHT; BRAIN CORTEX; CEREBELLUM; COGNITIVE DEFECT; CONTROLLED STUDY; EXECUTIVE DYSFUNCTION; EXPLORATORY BEHAVIOR; FEMALE; FRONTOTEMPORAL DEMENTIA; GRIP STRENGTH; HEARING ACUITY; HIGH RISK BEHAVIOR; HIPPOCAMPUS; IMPULSIVENESS; MALE; MEMORY DISORDER; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SEX DIFFERENCE; SHORT TERM MEMORY; SOCIAL EXPLORATION; SPATIAL WORKING MEMORY; TAUOPATHY; TREMOR; WORKING MEMORY; ANIMAL; ANIMAL BEHAVIOR; DISEASE MODEL; EXECUTIVE FUNCTION; GENETICS; MUTATION; PATHOLOGY; PHYSIOLOGY; PSYCHOLOGY; SOCIAL BEHAVIOR;

ANIMALS; BEHAVIOR, ANIMAL; CEREBRAL CORTEX; DISEASE MODELS, ANIMAL; EXECUTIVE FUNCTION; EXPLORATORY BEHAVIOR; FRONTOTEMPORAL DEMENTIA; HIPPOCAMPUS; IMPULSIVE BEHAVIOR; MICE; MUTATION; SOCIAL BEHAVIOR; TAU PROTEINS;

EID: 84956641751     PISSN: 10747427     EISSN: 10959564     Source Type: Journal    
DOI: 10.1016/j.nlm.2016.01.007     Document Type: Article

References (72)

1. Baeta-Corral R., Giménez-Llort L. Bizarre behaviors and risk assessment in 3xTg-AD mice at early stages of the disease. Behavioural Brain Research 2014, 258:97-105.
2. Ben Abdallah N.M.-B., Fuss J., Trusel M., Galsworthy M.J., Bobsin K., Colacicco G., Gass P. The puzzle box as a simple and efficient behavioral test for exploring impairments of general cognition and executive functions in mouse models of schizophrenia. Experimental Neurology 2011, 227:42-52.
3. Bigio E.H. Making the diagnosis of frontotemporal lobar degeneration. Archives of Pathology and Laboratory Medicine 2013, 137:314-325.
4. Callaerts-Vegh Z., Leo S., Vermaercke B., Meert T., D'Hooge R. LPA(5) receptor plays a role in pain sensitivity, emotional exploration and reversal learning. Genes, Brain, and Behavior 2012, 11:1009-1019.
5. Chao L.L., Knight R.T. Human prefrontal lesions increase distractibility to irrelevant sensory inputs. NeuroReport 1995, 6:1605-1610.
6. Cowan N. What are the differences between long-term, short-term, and working memory?. Progress in Brain Research 2008, 169:323-338.
7. Crawley J.N. Exploratory behavior models of anxiety in mice. Neuroscience and Biobehavioral Reviews 1985, 9:37-44.
8. Cruz M., Marinho V., Fontenelle L.F., Engelhardt E., Laks J. Topiramate may modulate alcohol abuse but not other compulsive behaviors in frontotemporal dementia: case report. Cognitive and Behavioral Neurology: Official Journal of the Society for Behavioral and Cognitive Neurology 2008, 21:104-106.
9. Devenney E., Vucic S., Hodges J.R., Kiernan M.C. Motor neuron disease-frontotemporal dementia: A clinical continuum. Expert Review of Neurotherapeutics 2015, 15:1-14.
10. Diehl-Schmid J., Schūlte-Overberg J., Hartmann J., Förstl H., Kurz A., Häussermann P. Extrapyramidal signs, primitive reflexes and incontinence in fronto-temporal dementia. European Journal of neurology: The Official Journal of the European Federation of Neurological Societies 2007, 14:860-864.
11. Dillon G.M., Qu X., Marcus J.N., Dodart J.-C. Excitotoxic lesions restricted to the dorsal CA1 field of the hippocampus impair spatial memory and extinction learning in C57BL/6 mice. Neurobiology of Learning and Memory 2008, 90:426-433.
12. Egashira N., Iwasaki K., Takashima A., Watanabe T., Kawabe H., Matsuda T., Fujiwara M. Altered depression-related behavior and neurochemical changes in serotonergic neurons in mutant R406W human tau transgenic mice. Brain Research 2005, 1059:7-12.
13. Eslinger P.J., Moore P., Anderson C., Grossman M. Social cognition, executive functioning, and neuroimaging correlates of empathic deficits in frontotemporal dementia. The Journal of Neuropsychiatry and Clinical Neurosciences 2011, 23:74-82.
14. Filiano A.J., Martens L.H., Young A.H., Warmus B.A., Zhou P., Diaz-Ramirez G., Roberson E.D. Dissociation of frontotemporal dementia-related deficits and neuroinflammation in progranulin haploinsufficient mice. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 2013, 33:5352-5361.
15. Galimberti D., Scarpini E. Genetics and biology of Alzheimer's disease and frontotemporal lobar degeneration. International Journal of Clinical and Experimental Medicine 2010, 3:129-143.
16. Galsworthy M.J., Paya-Cano J.L., Liu L., Monleón S., Gregoryan G., Fernandes C., Plomin R. Assessing reliability, heritability and general cognitive ability in a battery of cognitive tasks for laboratory mice. Behavior Genetics 2005, 35:675-692.
17. Gibbons Z.C., Richardson A., Neary D., Snowden J.S. Behaviour in amyotrophic lateral sclerosis. Amyotrophic Lateral Sclerosis: Official Publication of the World Federation of Neurology Research Group on Motor Neuron Diseases 2008, 9:67-74.
18. Grochmal-Bach B., Bidzan L., Pachalska M., Bidzan M., Łukaszewska B., Pufal A. Aggressive and impulsive behaviors in frontotemporal dementia and Alzheimer's disease. Medical Science Monitor: International Medical Journal of Experimental and Clinical Research 2009, 15:248-254.
19. Grunwald T., Boutros N.N., Pezer N., von Oertzen J., Fernández G., Schaller C., Elger C.E. Neuronal substrates of sensory gating within the human brain. Biological Psychiatry 2003, 53:511-519.
20. Harciarek M., Cosentino S. Language, executive function and social cognition in the diagnosis of frontotemporal dementia syndromes. International Review of Psychiatry (Abingdon, England) 2013, 25:178-196.
21. Hodges J.R. Alzheimer's disease and the frontotemporal dementias: Contributions to clinico-pathological studies, diagnosis, and cognitive neuroscience. Journal of Alzheimer's Disease: JAD 2013, 33(Suppl 1):S211-S217.
22. Hodges J.R., Davies R.R., Xuereb J.H., Casey B., Broe M., Bak T.H., Halliday G.M. Clinicopathological correlates in frontotemporal dementia. Annals of Neurology 2004, 56:399-406.
23. Huey E.D., Goveia E.N., Paviol S., Pardini M., Krueger F., Zamboni G., Grafman J. Executive dysfunction in frontotemporal dementia and corticobasal syndrome. Neurology 2009, 72:453-459.
24. Hughes R.N. The value of spontaneous alternation behavior (SAB) as a test of retention in pharmacological investigations of memory. Neuroscience and Biobehavioral Reviews 2004, 28:497-505.
25. Ittner L.M., Halliday G.M., Kril J.J., Götz J., Hodges J.R., Kiernan M.C. FTD and ALS-translating mouse studies into clinical trials. Nature Reviews Neurology 2015, 11:360-366.
26. Ittner L.M., Ke Y.D., Delerue F., Bi M., Gladbach A., van Eersel J., Götz J. Dendritic function of tau mediates amyloid-beta toxicity in Alzheimer's disease mouse models. Cell 2010, 142:387-397.
27. Johns E.K., Phillips N.A., Belleville S., Goupil D., Babins L., Kelner N., Chertkow H. Executive functions in frontotemporal dementia and Lewy body dementia. Neuropsychology 2009, 23:765-777.
28. Ke Y.D., Delerue F., Gladbach A., Götz J., Ittner L.M. Experimental diabetes mellitus exacerbates tau pathology in a transgenic mouse model of Alzheimer's disease. PLoS ONE 2009, 4:e7917.
29. Knight R.T., Staines W.R., Swick D., Chao L.L. Prefrontal cortex regulates inhibition and excitation in distributed neural networks. Acta Psychologica 1999, 101:159-178.
30. Knutson K.M., Dal Monte O., Schintu S., Wassermann E.M., Raymont V., Grafman J., Krueger F. Areas of brain damage underlying increased reports of behavioral disinhibition. The Journal of Neuropsychiatry and Clinical Neurosciences 2015, 10.1176/appi.neuropsych.14060126.
31. Koppel J., Jimenez H., Azose M., D'Abramo C., Acker C., Buthorn J., Davies P. Pathogenic tau species drive a psychosis-like phenotype in a mouse model of Alzheimer's disease. Behavioural Brain Research 2014, 275:27-33.
32. Lalonde R. The neurobiological basis of spontaneous alternation. Neuroscience and Biobehavioral Reviews 2002, 26:91-104.
33. Landqvist Waldö M., Santillo A.F., Gustafson L., Englund E., Passant U. Somatic complaints in frontotemporal dementia. American Journal of Neurodegenerative Disease 2014, 3:84-92.
34. Lindau M., Almkvist O., Kushi J., Boone K., Johansson S.E., Wahlund L.O., Miller B.L. First symptoms-frontotemporal dementia versus Alzheimer's disease. Dementia and Geriatric Cognitive Disorders 2000, 11:286-293.
35. Manes F.F., Torralva T., Roca M., Gleichgerrcht E., Bekinschtein T.A., Hodges J.R. Frontotemporal dementia presenting as pathological gambling. Nature Reviews Neurology 2010, 6:347-352.
36. Meeker H.C., Chadman K.K., Heaney A.T., Carp R.I. Assessment of social interaction and anxiety-like behavior in senescence-accelerated-prone and -resistant mice. Physiology & Behavior 2013, 118:97-102.
37. Mendez M.F. The accuracy of clinical criteria for the diagnosis of frontotemporal dementia. International Journal of Psychiatry in Medicine 2004, 34:125-130.
38. Mendez M.F. The unique predisposition to criminal violations in frontotemporal dementia. The Journal of the American Academy of Psychiatry and the Law 2010, 38:318-323.
39. Mendez M.F. Pathological stealing in dementia: Poor response to SSRI medications. The Journal of Clinical Psychiatry 2011, 72:418-419.
40. Mendez M.F., Perryman K.M. Neuropsychiatric features of frontotemporal dementia: Evaluation of consensus criteria and review. The Journal of Neuropsychiatry and Clinical Neurosciences 2002, 14:424-429.
41. Merrilees J., Klapper J., Murphy J., Lomen-Hoerth C., Miller B.L. Cognitive and behavioral challenges in caring for patients with frontotemporal dementia and amyotrophic lateral sclerosis. Amyotrophic Lateral Sclerosis: Official Publication of the World Federation of Neurology Research Group on Motor Neuron Diseases 2010, 11:298-302.
42. Moy S.S., Nadler J.J., Perez A., Barbaro R.P., Johns J.M., Magnuson T.R., Crawley J.N. Sociability and preference for social novelty in five inbred strains: An approach to assess autistic-like behavior in mice. Genes, Brain, and Behavior 2004, 3:287-302.
43. Naert A., Gantois I., Laeremans A., Vreysen S., Van den Bergh G., Arckens L., D'Hooge R. Behavioural alterations relevant to developmental brain disorders in mice with neonatally induced ventral hippocampal lesions. Brain Research Bulletin 2013, 94:71-81.
44. Neary D., Snowden J., Mann D. Frontotemporal dementia. The Lancet Neurology 2005, 4:771-780.
45. Njung'e K., Handley S.L. Evaluation of marble-burying behavior as a model of anxiety. Pharmacology, Biochemistry and Behavior 1991, 38:63-67.
46. Passant U., Elfgren C., Englund E., Gustafson L. Psychiatric symptoms and their psychosocial consequences in frontotemporal dementia. Alzheimer Disease and Associated Disorders 2005, 19(Suppl 1):S15-S18.
47. Perriol M.-P., Dujardin K., Derambure P., Marcq A., Bourriez J.-L., Laureau E., Destée A. Disturbance of sensory filtering in dementia with Lewy bodies: Comparison with Parkinson's disease dementia and Alzheimer's disease. Journal of Neurology, Neurosurgery and Psychiatry 2005, 76:106-108.
48. Peters F., Perani D., Herholz K., Holthoff V., Beuthien-Baumann B., Sorbi S., Salmon E. Orbitofrontal dysfunction related to both apathy and disinhibition in frontotemporal dementia. Dementia and Geriatric Cognitive Disorders 2006, 21:373-379.
49. Pompanin S., Jelcic N., Cecchin D., Cagnin A. Impulse control disorders in frontotemporal dementia: Spectrum of symptoms and response to treatment. General Hospital Psychiatry 2014, 36(760):e5-e7.
50. Pressman P.S., Miller B.L. Diagnosis and management of behavioral variant frontotemporal dementia. Biological Psychiatry 2014, 75:574-581.
51. Rademakers R., Neumann M., Mackenzie I.R. Advances in understanding the molecular basis of frontotemporal dementia. Nature Reviews Neurology 2012, 8:423-434.
52. Rafael J.A., Nitta Y., Peters J., Davies K.E. Testing of SHIRPA, a mouse phenotypic assessment protocol, on Dmd(mdx) and Dmd(mdx3cv) dystrophin-deficient mice. Mammalian Genome: Official Journal of the International Mammalian Genome Society 2000, 11:725-728.
53. Rankin K.P., Kramer J.H., Miller B.L. Patterns of cognitive and emotional empathy in frontotemporal lobar degeneration. Cognitive and Behavioral Neurology: Official Journal of the Society for Behavioral and Cognitive Neurology 2005, 18:28-36.
54. Reisel D., Bannerman D.M., Schmitt W.B., Deacon R.M.J., Flint J., Borchardt T., Rawlins J.N.P. Spatial memory dissociations in mice lacking GluR1. Nature Neuroscience 2002, 5:868-873.
55. Rogers D.C., Fisher E.M., Brown S.D., Peters J., Hunter A.J., Martin J.E. Behavioral and functional analysis of mouse phenotype: SHIRPA, a proposed protocol for comprehensive phenotype assessment. Mammalian Genome: Official Journal of the International Mammalian Genome Society 1997, 8:711-713.
56. Savage S.A., Lillo P., Kumfor F., Kiernan M.C., Piguet O., Hodges J.R. Emotion processing deficits distinguish pure amyotrophic lateral sclerosis from frontotemporal dementia. Amyotrophic Lateral Sclerosis & Frontotemporal Degeneration 2014, 15:39-46.
57. Seltman R.E., Matthews B.R. Frontotemporal lobar degeneration: Epidemiology, pathology, diagnosis and management. CNS Drugs 2012, 26:841-870.
58. Shea Y.F., Ha J., Chu L.-W. Comparisons of clinical symptoms in biomarker-confirmed Alzheimer's disease, dementia with Lewy bodies, and frontotemporal dementia patients in a local memory clinic. Psychogeriatrics: The Official Journal of the Japanese Psychogeriatric Society 2014.
59. Sieben A., Van Langenhove T., Engelborghs S., Martin J.-J., Boon P., Cras P., Cruts M. The genetics and neuropathology of frontotemporal lobar degeneration. Acta Neuropathologica 2012, 124:353-372.
60. Snowden J.S., Bathgate D., Varma A., Blackshaw A., Gibbons Z.C., Neary D. Distinct behavioural profiles in frontotemporal dementia and semantic dementia. Journal of Neurology, Neurosurgery and Psychiatry 2001, 70:323-332.
61. Snowden J.S., Gibbons Z.C., Blackshaw A., Doubleday E., Thompson J., Craufurd D., Neary D. Social cognition in frontotemporal dementia and Huntington's disease. Neuropsychologia 2003, 41:688-701.
62. Starkstein S.E., Robinson R.G. Mechanism of disinhibition after brain lesions. The Journal of Nervous and Mental Disease 1997, 185:108-114.
63. Sterniczuk R., Antle M.C., Laferla F.M., Dyck R.H. Characterization of the 3xTg-AD mouse model of Alzheimer's disease: Part 2. Behavioral and cognitive changes. Brain Research 2010, 1348:149-155.
64. Stopford C.L., Thompson J.C., Neary D., Richardson A.M.T., Snowden J.S. Working memory, attention, and executive function in Alzheimer's disease and frontotemporal dementia. Cortex: A Journal Devoted to the Study of the Nervous System and Behavior 2012, 48:429-446.
65. Takeuchi H., Iba M., Inoue H., Higuchi M., Takao K., Tsukita K., Takahashi R. P301S mutant human tau transgenic mice manifest early symptoms of human tauopathies with dementia and altered sensorimotor gating. PLoS ONE 2011, 6:e21050.
66. Tasan R.O., Lin S., Hetzenauer A., Singewald N., Herzog H., Sperk G. Increased novelty-induced motor activity and reduced depression-like behavior in neuropeptide Y (NPY)-Y4 receptor knockout mice. Neuroscience 2009, 158:1717-1730.
67. Van der Jeugd A., Blum D., Raison S., Eddarkaoui S., Buée L., D'Hooge R. Observations in THY-Tau22 mice that resemble behavioral and psychological signs and symptoms of dementia. Behavioural Brain Research 2013, 242:34-39.
68. Van Der Jeugd A., Vermaercke B., Lo A.C., Hamdane M., Blum D., Buée L., D'Hooge R. Progressive age-related cognitive decline in tau mice. Journal of Alzheimer's Disease 2013, 37:777-788.
69. Van Eersel J., Stevens C.H., Przybyla M., Gladbach A., Stefanoska K., Chan C.K.-X., Ittner L.M. Early-onset axonal pathology in a novel P301S-Tau transgenic mouse model of frontotemporal lobar degeneration. Neuropathology and Applied Neurobiology 2015.
70. Varty G.B., Morgan C.A., Cohen-Williams M.E., Coffin V.L., Carey G.J. The gerbil elevated plus-maze I: Behavioral characterization and pharmacological validation. Neuropsychopharmacology: Official Publication of the American College of Neuropsychopharmacology 2002, 27:357-370.
71. Xia D., Li C., Götz J. Pseudophosphorylation of Tau at distinct epitopes or the presence of the P301L mutation targets the microtubule-associated protein Tau to dendritic spines. Biochimica et Biophysica Acta 2015, 1852:913-924.
72. Yin F., Dumont M., Banerjee R., Ma Y., Li H., Lin M.T., Ding A. Behavioral deficits and progressive neuropathology in progranulin-deficient mice: A mouse model of frontotemporal dementia. FASEB Journal: Official Publication of the Federation of American Societies for Experimental Biology 2010, 24:4639-4647.