Nest building is impaired in the Ts65Dn mouse model of Down syndrome and rescued by blocking 5HT2a receptors

Neurobiology of Learning and Memory

Volumn 116, Issue , 2014, Pages 162-171

  Heller, H Craig ^a   Salehi, Ahmad ^a,b   Chuluun, Bayarsaikhan ^a   Das, Devsmita ^a,b   Lin, Bill ^b   Moghadam, Sarah ^b   Garner, Craig C ^a   Colas, Damien ^a  

^a STANFORD UNIVERSITY   (United States)

^b VA PALO ALTO HEALTH CARE SYSTEM   (United States)

Author keywords

Attention; Eplivanserin; Goal directed behavior; Pentylenetetrazole; Risperidone; SR 46349; Ts1Rhr; Ts65Dn

Indexed keywords

EPLIVANSERIN; RISPERIDONE; SEROTONIN 2A RECEPTOR; SEROTONIN 2 ANTAGONIST;

5HT2A RECEPTOR GENE; ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATTENTION DEFICIT DISORDER; CHROMOSOME 16; CONTROLLED STUDY; DOSE RESPONSE; DOWN SYNDROME; DRUG EFFECT; FEMALE; FRONTAL CORTEX; GENE EXPRESSION; HEREDITY; LIMBIC CORTEX; LOW DRUG DOSE; MALE; MOUSE; NESTING; NONHUMAN; PHENOTYPE; SIGNAL TRANSDUCTION; YOUNG ADULT; ANIMAL; COGNITIVE DEFECT; DISEASE MODEL; DRUG EFFECTS; GENETICS; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; COGNITION DISORDERS; DISEASE MODELS, ANIMAL; DOWN SYNDROME; GENE EXPRESSION; MICE; NESTING BEHAVIOR; PHENOTYPE; RECEPTOR, SEROTONIN, 5-HT2A; RISPERIDONE; SEROTONIN 5-HT2 RECEPTOR ANTAGONISTS;

EID: 84909993043     PISSN: 10747427     EISSN: 10959564     Source Type: Journal    
DOI: 10.1016/j.nlm.2014.10.002     Document Type: Article

References (81)

1. Alex K.D., Pehek E.A. Pharmacologic mechanisms of serotonergic regulation of dopamine neurotransmission. Pharmacology & Therapeutics 2007, 113:296-320.
2. Auclair A., Blanc G., Glowinski J., Tassin J.P. Role of serotonin 2A receptors in the D-amphetamine-induced release of dopamine: Comparison with previous data on alpha1b-adrenergic receptors. Journal of Neurochemistry 2004, 91:318-326.
3. Belichenko N.P., Belichenko P.V., Kleschevnikov A.M., Salehi A., Reeves R.H., Mobley W.C. The "Down syndrome critical region" is sufficient in the mouse model to confer behavioral, neurophysiological, and synaptic phenotypes characteristic of Down syndrome. Journal of Neuroscience 2009, 29:5938-5948.
4. Bianchi P., Ciani E., Guidi S., Trazzi S., Felice D., Grossi G., et al. Early pharmacotherapy restores neurogenesis and cognitive performance in the Ts65Dn mouse model for Down syndrome. Journal of Neuroscience 2010, 30:8769-8779.
5. Blank M., Fuerst P.G., Stevens B., Nouri N., Kirkby L., Warrier D., et al. The Down syndrome critical region regulates retinogeniculate refinement. Journal of Neuroscience 2011, 31:5764-5776.
6. Booij L., Van der Does A.J., Riedel W.J. Monoamine depletion in psychiatric and healthy populations: Review. Molecular Psychiatry 2003, 8:951-973.
7. Braudeau J., Dauphinot L., Duchon A., Loistron A., Dodd R.H., Herault Y., et al. Chronic treatment with a promnesiant GABA-A alpha5-selective inverse agonist increases immediate early genes expression during memory processing in mice and rectifies their expression levels in a Down syndrome mouse model. Advances in Pharmacological Sciences 2011, 2011:153218.
8. Capone G.T., Goyal P., Grados M., Smith B., Kammann H. Risperidone use in children with Down syndrome, severe intellectual disability, and comorbid autistic spectrum disorders: A naturalistic study. Journal of Developmental and Behavioral Pediatrics 2008, 29:106-116.
9. Carter O.L., Burr D.C., Pettigrew J.D., Wallis G.M., Hasler F., Vollenweider F.X. Using psilocybin to investigate the relationship between attention, working memory, and the serotonin 1A and 2A receptors. Journal of Cognitive Neuroscience 2005, 17:1497-1508.
10. Carter P.A., Swallow J.G., Davis S.J., Garland T. Nesting behavior of house mice (Mus domesticus) selected for increased wheel-running activity. Behavior Genetics 2000, 30:85-94.
11. Celada P., Puig M.V., Artigas F. Serotonin modulation of cortical neurons and networks. Frontiers in Integrative Neuroscience 2013, 7:25.
12. Clarke H.F., Dalley J.W., Crofts H.S., Robbins T.W., Roberts A.C. Cognitive inflexibility after prefrontal serotonin depletion. Science 2004, 304:878-880.
13. Colas D., Chuluun B., Warrier D., Blank M., Wetmore D.Z., Buckmaster P., et al. Short-term treatment with the GABAA receptor antagonist pentylenetetrazole produces a sustained pro-cognitive benefit in a mouse model of Down's syndrome. British Journal of Pharmacology 2013, 169:963-973.
14. Colas D., Valletta J.S., Takimoto-Kimura R., Nishino S., Fujiki N., Mobley W.C., et al. Sleep and EEG features in genetic models of Down syndrome. Neurobiology of Diseases 2008, 30:1-7.
15. Cools R., Roberts A.C., Robbins T.W. Serotoninergic regulation of emotional and behavioural control processes. Trends in Cognitive Sciences 2008, 12:31-40.
16. Costa A.C., Scott-McKean J.J., Stasko M.R. Acute injections of the NMDA receptor antagonist memantine rescue performance deficits of the Ts65Dn mouse model of Down syndrome on a fear conditioning test. Neuropsychopharmacology 2008, 33:1624-1632.
17. Creau N. Molecular and cellular alterations in Down syndrome: Toward the identification of targets for therapeutics. Neural Plasticity 2012, 2012:171639.
18. Dang V., Medina B., Das D., Moghadam S., Martin K.J., Lin B., et al. Formoterol, a long-acting beta2 adrenergic agonist, improves cognitive function and promotes dendritic complexity in a mouse model of Down syndrome. Biological Psychiatry 2013.
19. Deacon R.M. Assessing nest building in mice. Nature Protocols 2006, 1:1117-1119.
20. Deacon R. Assessing burrowing, nest construction, and hoarding in mice. Journal of Visualized Experiments 2012, e2607.
21. Deacon R.M., Croucher A., Rawlins J.N. Hippocampal cytotoxic lesion effects on species-typical behaviours in mice. Behavioural Brain Research 2002, 132:203-213.
22. Deacon R.M., Penny C., Rawlins J.N. Effects of medial prefrontal cortex cytotoxic lesions in mice. Behavioural Brain Research 2003, 139:139-155.
23. Deco G., Rolls E.T. Attention, short-term memory, and action selection: A unifying theory. Progress in Neurobiology 2005, 76:236-256.
24. DeLorey T.M., Sahbaie P., Hashemi E., Homanics G.E., Clark J.D. Gabrb3 gene deficient mice exhibit impaired social and exploratory behaviors, deficits in non-selective attention and hypoplasia of cerebellar vermal lobules: A potential model of autism spectrum disorder. Behavioural Brain Research 2008, 187:207-220.
25. Dentel C., Palamiuc L., Henriques A., Lannes B., Spreux-Varoquaux O., Gutknecht L., et al. Degeneration of serotonergic neurons in amyotrophic lateral sclerosis: A link to spasticity. Brain 2013, 136:483-493.
26. Dierssen M. Down syndrome: The brain in trisomic mode. Nature Reviews Neuroscience 2012, 13:844-858.
27. Driscoll L.L., Carroll J.C., Moon J., Crnic L.S., Levitsky D.A., Strupp B.J. Impaired sustained attention and error-induced stereotypy in the aged Ts65Dn mouse: A mouse model of Down syndrome and Alzheimer's disease. Behavioral Neuroscience 2004, 118:1196-1205.
28. Edgin J.O., Mason G.M., Spano G., Fernandez A., Nadel L. Human and mouse model cognitive phenotypes in Down syndrome: Implications for assessment. Progress in Brain Research 2012, 197:123-151.
29. Ekstein S., Glick B., Weill M., Kay B., Berger I. Down syndrome and attention-deficit/hyperactivity disorder (ADHD). Journal of Child Neurology 2011, 26:1290-1295.
30. Enge S., Fleischhauer M., Lesch K.P., Reif A., Strobel A. Variation in key genes of serotonin and norepinephrine function predicts gamma-band activity during goal-directed attention. Cerebral Cortex 2012, 10.1093/cercor/bhs398.
31. Escorihuela R.M., Fernandez-Teruel A., Vallina I.F., Baamonde C., Lumbreras M.A., Dierssen M., et al. A behavioral assessment of Ts65Dn mice. a putative Down syndrome model. Neuroscience Letters 1995, 199:143-146.
32. Fernandez F., Morishita W., Zuniga E., Nguyen J., Blank M., Malenka R.C., et al. Pharmacotherapy for cognitive impairment in a mouse model of Down syndrome. Nature Neuroscience 2007, 10:411-413.
33. Filali M., Lalonde R. Age-related cognitive decline and nesting behavior in an APPswe/PS1 biogenic model of Alzheimer's disease. Brain Research 2009, 1292:93-99.
34. Filip M., Bubar M.J., Cunningham K.A. Contribution of serotonin (5-hydroxytryptamine 5-HT) 5-HT2 receptor subtypes to the hyper locomotor effects of cocaine: Acute and chronic pharmacological analyses. Journal of Pharmacology and Experimental Therapeutics 2004, 310:1246-1254.
35. Gardiner K., Herault Y., Lott I.T., Antonarakis S.E., Reeves R.H., Dierssen M. Down syndrome: From understanding the neurobiology to therapy. Journal of Neuroscience 2010, 30:14943-14945.
36. González-Maeso J., Weisstaub N.V., Zhou M., Chan P., Ivic L., Ang R., et al. Hallucinogens recruit specific cortical 5-HT(2A) receptor-mediated signaling pathways to affect behavior. Neuron 2007, 53(3):439-452.
37. Heinen M., Hettich M.M., Ryan D.P., Schnell S., Paesler K., Ehninger D. Adult-onset fluoxetine treatment does not improve behavioral impairments and may have adverse effects on the Ts65Dn mouse model of Down syndrome. Neural Plasticity 2012, 2012:467251.
38. Herault Y., Duchon A., Velot E., Marechal D., Brault V. The in vivo Down syndrome genomic library in mouse. Progress in Brain Research 2012, 197:169-197.
39. Hunter C.L., Bimonte H.A., Granholm A.C. Behavioral comparison of 4 and 6 month-old Ts65Dn mice: Age-related impairments in working and reference memory. Behavioural Brain Research 2003, 138:121-131.
40. Ji N.Y., Capone G.T., Kaufmann W.E. Autism spectrum disorder in Down syndrome: Cluster analysis of Aberrant Behaviour Checklist data supports diagnosis. Journal of Intellectual Disability Research 2011, 55:1064-1077.
41. Kekesi K.A., Juhasz G., Simor A., Gulyassy P., Szego E.M., Hunyadi-Gulyas E., et al. Altered functional protein networks in the prefrontal cortex and amygdala of victims of suicide. PLoS ONE 2012, 7:e50532.
42. Kinder E. A study of the nest-building activity in the albino rat. The Journal of Experimental Zoology 1927, 47:117-161.
43. Kleschevnikov A.M., Belichenko P.V., Villar A.J., Epstein C.J., Malenka R.C., Mobley W.C. Hippocampal long-term potentiation suppressed by increased inhibition in the Ts65Dn mouse, a genetic model of Down syndrome. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 2004, 24:8153-8160.
44. Knudsen E.I. Fundamental components of attention. Annual Review of Neuroscience 2007, 30:57-78.
45. Kolb B. Functions of the frontal cortex of the rat: A comparative review. Brain Research 1984, 320:65-98.
46. Korzan W.J., Summers C.H. Serotonergic response to social stress and artificial social sign stimuli during paired interactions between male Anolis carolinensis. Neuroscience 2004, 123(4):835-845.
47. Leysen J.E., Janssen P.M., Megens A.A., Schotte A. Risperidone: A novel antipsychotic with balanced serotonin-dopamine antagonism, receptor occupancy profile, and pharmacologic activity. Journal of Clinical Psychiatry 1994, 55(Suppl.):5-12.
48. Li X., Morrow D., Witkin J.M. Decreases in Nestlet shredding of mice by serotonin uptake inhibitors: Comparison with marble burying. Life Sciences 2006, 78:1933-1939.
49. Liu C., Belichenko P.V., Zhang L., Fu D., Kleschevnikov A.M., Baldini A., et al. Mouse models for Down syndrome-associated developmental cognitive disabilities. Developmental Neuroscience 2011, 33:404-413.
50. Marek G.J., Carpenter L.L., McDougle C.J., Price L.H. Synergistic action of 5-HT2A antagonists and selective serotonin reuptake inhibitors in neuropsychiatric disorders. Neuropsychopharmacology 2003, 28:402-412.
51. Martinez-Cue C., Baamonde C., Lumbreras M., Paz J., Davisson M.T., Schmidt C., et al. Differential effects of environmental enrichment on behavior and learning of male and female Ts65Dn mice, a model for Down syndrome. Behavioural Brain Research 2002, 134:185-200.
52. Martinez-Cue C., Rueda N., Garcia E., Davisson M.T., Schmidt C., Florez J. Behavioral, cognitive and biochemical responses to different environmental conditions in male Ts65Dn mice, a model of Down syndrome. Behavioural Brain Research 2005, 163:174-185.
53. McLean T.H., Parrish J.C., Braden M.R., Marona-Lewicka D., Gallardo-Godoy A., Nichols D.E. 1-Aminomethylbenzocycloalkanes: Conformationally restricted hallucinogenic phenethylamine analogues as functionally selective 5-HT2A receptor agonists. Journal of Medicinal Chemistry 2006, 49:5794-5803.
54. Megias M., Verduga R., Dierssen M., Florez J., Insausti R., Crespo D. Cholinergic, serotonergic and catecholaminergic neurons are not affected in Ts65Dn mice. NeuroReport 1997, 8:3475-3478.
55. Moon J., Chen M., Gandhy S.U., Strawderman M., Levitsky D.A., Maclean K.N., et al. Perinatal choline supplementation improves cognitive functioning and emotion regulation in the Ts65Dn mouse model of Down syndrome. Behavioral Neuroscience 2010, 124:346-361.
56. Morris J.K., Alberman E. Trends in Down's syndrome live births and antenatal diagnoses in England and Wales from 1989 to 2008: Analysis of data from the National Down Syndrome Cytogenetic Register. BMJ 2009, 339:b3794.
57. Moss J., Richards C., Nelson L., Oliver C. Prevalence of autism spectrum disorder symptomatology and related behavioural characteristics in individuals with Down syndrome. Autism 2013, 17:390-404.
58. Nadel L. Down's syndrome: A genetic disorder in biobehavioral perspective. Genes, Brain, and Behavior 2003, 2:156-166.
59. Prandini P., Deutsch S., Lyle R., Gagnebin M., Delucinge Vivier C., Delorenzi M., et al. Natural gene-expression variation in Down syndrome modulates the outcome of gene-dosage imbalance. American Journal of Human Genetics 2007, 81:252-263.
60. Puig M.V., Gulledge A.T. Serotonin and prefrontal cortex function: Neurons, networks, and circuits. Molecular Neurobiology 2011, 44:449-464.
61. Rachidi M., Lopes C. Mental retardation in Down syndrome: From gene dosage imbalance to molecular and cellular mechanisms. Neuroscience Research 2007, 59:349-369.
62. Reeves R.H., Irving N.G., Moran T.H., Wohn A., Kitt C., Sisodia S.S., et al. A mouse model for Down syndrome exhibits learning and behaviour deficits. Nature Genetics 1995, 11:177-184.
63. Ribases M., Ramos-Quiroga J.A., Hervas A., Bosch R., Bielsa A., Gastaminza X., et al. Exploration of 19 serotoninergic candidate genes in adults and children with attention-deficit/hyperactivity disorder identifies association for 5HT2A, DDC and MAOB. Molecular Psychiatry 2009, 14:71-85.
64. Rinaldi-Carmona M., Congy C., Santucci V., Simiand J., Gautret B., Neliat G., et al. Biochemical and pharmacological properties of SR 46349B, a new potent and selective 5-hydroxytryptamine2 receptor antagonist. Journal of Pharmacology and Experimental Therapeutics 1992, 262:759-768.
65. Rueda N., Florez J., Martinez-Cue C. Mouse models of Down syndrome as a tool to unravel the causes of mental disabilities. Neural Plasticity 2012, 2012:584071.
66. Ruparelia A., Pearn M.L., Mobley W.C. Cognitive and pharmacological insights from the Ts65Dn mouse model of Down syndrome. Current Opinion in Neurobiology 2012, 22:880-886.
67. Salehi A., Delcroix J.-D., Belichenko P.V., Zhan K., Wu C., Valletta J.S., et al. Increased App expression in a mouse model of Down's syndrome disrupts NGF transport and causes cholinergic neuron degeneration. Neuron 2006, 51:29-42.
68. Salehi A., Faizi M., Belichenko P.V., Mobley W.C. Using mouse models to explore genotype-phenotype relationship in Down syndrome. Mental Retardation and Developmental Disabilities Research Reviews 2007, 13:207-214.
69. Salehi A., Faizi M., Colas D., Valletta J., Laguna J., Takimoto-Kimura R., et al. Restoration of norepinephrine-modulated contextual memory in a mouse model of Down syndrome. Science Translational Medicine 2009, 1:7ra17.
70. Schmitt J.A., Wingen M., Ramaekers J.G., Evers E.A., Riedel W.J. Serotonin and human cognitive performance. Current Pharmaceutical Design 2006, 12:2473-2486.
71. Seregaza Z., Roubertoux P.L., Jamon M., Soumireu-Mourat B. Mouse models of cognitive disorders in trisomy 21: A review. Behavior Genetics 2006, 36:387-404.
72. Sharma A., Shaw S.R. Efficacy of risperidone in managing maladaptive behaviors for children with autistic spectrum disorder: A meta-analysis. Journal of Pediatric Health Care 2012, 26:291-299.
73. Stagni F., Magistretti J., Guidi S., Ciani E., Mangano C., Calza L., et al. Pharmacotherapy with fluoxetine restores functional connectivity from the dentate gyrus to field CA3 in the Ts65Dn mouse model of Down syndrome. PLoS ONE 2013, 8:e61689.
74. Stasko M.R., Costa A.C. Experimental parameters affecting the Morris water maze performance of a mouse model of Down syndrome. Behavioural Brain Research 2004, 154:1-17.
75. Su Y.A., Si T.M., Zhou D.F., Guo C.M., Wang X.D., Yang Y., et al. Risperidone attenuates MK-801-induced hyperlocomotion in mice via the blockade of serotonin 5-HT 2A/2C receptors. European Journal of Pharmacology 2007, 564:123-130.
76. Teegarden B.R., Al Shamma H., Xiong Y. 5-HT(2A) inverse-agonists for the treatment of insomnia. Current Topics in Medicinal Chemistry 2008, 8:969-976.
77. Turner C.A., Presti M.F., Newman H.A., Bugenhagen P., Crnic L., Lewis M.H. Spontaneous stereotypy in an animal model of Down syndrome: Ts65Dn mice. Behavior Genetics 2001, 31:393-400.
78. Van de Weerd H.A., Van Loo P.L., Van Zutphen L.F., Koolhaas J.M., Baumans V. Preferences for nesting material as environmental enrichment for laboratory mice. Laboratory Animals 1997, 31:133-143.
79. Vyas N.S., Lee Y., Ahn K., Ternouth A., Stahl D.R., Al-Chalabi A., et al. Association of a serotonin receptor 2A gene polymorphism with visual sustained attention in early-onset schizophrenia patients and their non-psychotic siblings. Aging & Disease 2012, 3:291-300.
80. Wenger G.R., Schmidt C., Davisson M.T. Operant conditioning in the Ts65Dn mouse: Learning. Behavior Genetics 2004, 34:105-119.
81. Zheng H., Jiang M., Trumbauer M.E., Hopkins R., Sirinathsinghji D.J., Stevens K.A., et al. Mice deficient for the amyloid precursor protein gene. Annals of the New York Academy of Sciences 1996, 777:421-426.