Deficits in tactile learning in a mouse model of fragile x syndrome

PLoS ONE

Volumn 9, Issue 10, 2014, Pages

  Arnett, Megan T ^a   Herman, David H ^a   McGee, Aaron W ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FRAGILE X MENTAL RETARDATION PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISEASE ASSOCIATION; EVOKED RESPONSE; FLUORESCENCE IMAGING; FMR1 GENE; FRAGILE X SYNDROME; GENE INACTIVATION; HYPERSENSITIVITY; INTRINSIC ACTIVITY; LEARNING; LEARNING DISORDER; MALE; MOUSE; MOUSE MODEL; NONHUMAN; SENSORY STIMULATION; SIGNAL TRANSDUCTION; SOMATOSENSORY CORTEX; TACTILE DISCRIMINATION; TACTILE LEARNING; TACTILE STIMULATION; VIBRISSA; ANIMAL; DISEASE MODEL; GENETICS; KNOCKOUT MOUSE; PATHOPHYSIOLOGY; PHYSIOLOGY; TOUCH;

ANIMALS; DISEASE MODELS, ANIMAL; FRAGILE X MENTAL RETARDATION PROTEIN; FRAGILE X SYNDROME; MALE; MICE; MICE, KNOCKOUT; TOUCH PERCEPTION;

EID: 84907854987     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0109116     Document Type: Article

References (47)

1. Turner G, Webb T, Wake S, Robinson H (1996) Prevalence of fragile X syndrome. Am J Med Genet 64: 196-197. doi:10.1002/(SICI)1096-8628(19960712)64:1, 196::AID-AJMG35.3.0.CO;2-G.
2. O'Donnell WT, Warren ST (2002) A Decade of Molecular Studies of Fragile X Syndrome. Annu Rev Neurosci 25: 315-338. doi:10.1146/annurev.-neuro.25.112701.142909.
3. Garber K, Smith KT, Reines D, Warren ST (2006) Transcription, translation and fragile X syndrome. Current Opinion in Genetics & Development 16: 270- 275. doi:10.1016/j.gde.2006.04.010.
4. Pfeiffer BE, Huber KM (2009) The State of Synapses in Fragile X Syndrome. The Neuroscientist: A review journal bringing neurobiology, neurology and psychiatry 15: 549-567. doi:10.1177/1073858409333075.
5. Miller LJ, McIntosh DN, McGrath J, Shyu V, Lampe M, et al. (1999) Electrodermal responses to sensory stimuli in individuals with fragile X syndrome: A preliminary report. Am J Med Genet 83: 268-279.
6. Hagerman RJ, Amiri K, Cronister A (1991) Fragile X checklist. Am J Med Genet 38: 283-287.
7. The Dutch-Belgian Fragile X Consortium (1994) Fmr1 knockout mice: A model to study fragile X mental retardation. The Dutch-Belgian Fragile X Consortium. Cell 78: 23-33.
8. Paradee W, Melikian HE, Rasmussen DL, Kenneson A, Conn PJ, et al. (1999) Fragile X mouse: strain effects of knockout phenotype and evidence suggesting deficient amygdala function. Neuroscience 94: 185-192.
9. Spencer CM, Alekseyenko O, Serysheva E, Yuva-Paylor LA, Paylor R (2005) Altered anxiety-related and social behaviors in the Fmr1 knockout mouse model of fragile X syndrome. Genes Brain Behav 4: 420-430. doi:10.1111/j.1601- 183X.2005.00123.x.
10. Brennan FX, Albeck DS, Paylor R (2006) Fmr1 knockout mice are impaired in a leverpress escape/avoidance task. Genes Brain Behav 5: 467-471. doi:10.1111/j.1601-183X.2005.00183.x.
11. Padmashri R, Reiner BC, Suresh A, Spartz E, Dunaevsky A (2013) Altered Structural and Functional Synaptic Plasticity with Motor Skill Learning in a Mouse Model of Fragile X Syndrome. Journal of Neuroscience 33: 19715- 19723. doi:10.1523/JNEUROSCI.2514-13.2013.
12. Frankland PW, Wang Y, Rosner B, Shimizu T, Balleine BW, et al. (2004) Sensorimotor gating abnormalities in young males with fragile X syndrome and Fmr1-knockout mice. Mol Psychiatry 9: 417-425. doi:10.1038/sj.mp.4001432.
13. Curia G, Papouin T, Seguela P, Avoli M (2009) Downregulation of Tonic GABAergic Inhibition in a Mouse Model of Fragile X Syndrome. Cerebral Cortex 19: 1515-1520. doi:10.1093/cercor/bhn159.
14. Olmos-Serrano JL, Paluszkiewicz SM, Martin BS, Kaufmann WE, Corbin JG, et al. (2010) Defective GABAergic Neurotransmission and Pharmacological Rescue of Neuronal Hyperexcitability in the Amygdala in a Mouse Model of Fragile X Syndrome. Journal of Neuroscience 30: 9929-9938. doi:10.1523/JNEUROSCI.1714-10.2010.
15. Harris JA, Petersen RS, Diamond ME (1999) Distribution of tactile learning and its neural basis. Proc Natl Acad Sci USA 96: 7587-7591.
16. Celikel T, Sakmann B (2007) Sensory integration across space and in time for decision making in the somatosensory system of rodents. Proc Natl Acad Sci USA 104: 1395-1400. doi:10.1073/pnas.0610267104.
17. Voigts J, Sakmann B, Celikel T (2008) Unsupervised Whisker Tracking in Unrestrained Behaving Animals. J Neurophysiol 100: 504-515. doi:10.1152/jn.00012.2008.
18. Hutson KA, Masterton RB (1986) The sensory contribution of a single vibrissa's cortical barrel. J Neurophysiol 56: 1196-1223.
19. Kalatsky VA, Stryker MP (2003) New paradigm for optical imaging: Temporally encoded maps of intrinsic signal. Neuron 38: 529-545.
20. Cang J, Kalatsky VA, Löwel S, Stryker MP (2005) Optical imaging of the intrinsic signal as a measure of cortical plasticity in the mouse. Vis Neurosci 22: 685-691. doi:10.1017/S0952523805225178.
21. Grinvald A, Lieke E, Frostig RD, Gilbert CD, Wiesel TN (1986) Functional architecture of cortex revealed by optical imaging of intrinsic signals. Nature 324: 361-364. doi:10.1038/324361a0.
22. Frostig RD, Lieke EE, Ts'o DY, Grinvald A (1990) Cortical functional architecture and local coupling between neuronal activity and the microcirculation revealed by in vivo high-resolution optical imaging of intrinsic signals. Proc Natl Acad Sci USA 87: 6082-6086.
23. Chen-Bee CH, Agoncillo T, Xiong Y, Frostig RD (2007) The Triphasic Intrinsic Signal: Implications for Functional Imaging. Journal of Neuroscience 27: 4572- 4586. doi:10.1523/JNEUROSCI.0326-07.2007.
24. Lefort S, Tomm C, Sarria JCF, Petersen CCH (2009) The Excitatory Neuronal Networkof the C2 Barrel Columnin Mouse Primary Somatosensory Cortex. Neuron 61: 301-316. doi:10.1016/j.neuron.2008.12.020.
25. Till SM, Wijetunge LS, Seidel VG, Harlow E, Wright AK, et al. (2012) Altered maturation of the primary somatosensory cortex in a mouse model of fragile X syndrome. Human Molecular Genetics 21: 2143-2156. doi:10.1093/hmg/dds030.
26. Rogers SJ, Hepburn S, Wehner E (2003) Parent reports of sensory symptoms in toddlers with autism and those with other developmental disorders. J Autism Dev Disord 33: 631-642.
27. Kaufmann WE, Cortell R, Kau ASM, Bukelis I, Tierney E, et al. (2004) Autism spectrum disorder in fragile X syndrome: Communication, social interaction, and specific behaviors. Am J Med Genet 129A: 225-234. doi:10.1002/ajmg.a.30229.
28. Moy SS, Nadler JJ (2007) Advances in behavioral genetics: mouse models of autism. Mol Psychiatry 13: 4-26. doi:10.1038/sj.mp.4002082.
29. Bassell GJ, Warren ST (2008) Fragile X Syndrome: Loss of Local mRNA Regulation Alters Synaptic Development and Function. Neuron 60: 201-214. doi:10.1016/j.neuron.2008.10.004.
30. Darnell JC, Jensen KB, Jin P, Brown V, Warren ST, et al. (2001) Fragile X mental retardation protein targets G quartet mRNAs important for neuronal function. Cell 107: 489-499.
31. Bear MF, Huber KM, Warren ST (2004) The mGluR theory of fragile X mental retardation. Trends Neurosci 27: 370-377. doi:10.1016/j.tins.2004.04.009.
32. Sidorov MS, Auerbach BD, Bear MF (2013) Fragile X mental retardation protein and synaptic plasticity. Molecular Brain 6: 1-1. doi:10.1186/1756-6606- 6-15.
33. Darnell JC, Klann E (2013) The translation of translational control by FMRP: Therapeutic targets for FXS. Nature Publishing Group 16: 1530-1536. doi:10.1038/nn.3379.
34. Irwin SA, Galvez R, Greenough WT (2000) Dendritic spine structural anomalies in fragile-X mental retardation syndrome. Cereb Cortex 10: 1038-1044.
35. Huber KM, Gallagher SM, Warren ST, Bear MF (2002) Altered synaptic plasticity in a mouse model of fragile X mental retardation. Proc Natl Acad Sci USA 99: 7746-7750. doi:10.1073/pnas.122205699.
36. Galvez R, Greenough WT (2005) Sequence of abnormal dendritic spine development in primary somatosensory cortex of a mouse model of the fragile X mental retardation syndrome. Am J Med Genet 135A: 155-160. doi:10.1002/ajmg.a.30709.
37. Selby L, Zhang C, Sun Q-Q (2007) Major defects in neocortical GABAergic inhibitory circuits in mice lacking the fragile X mental retardation protein. Neurosci Lett 412: 227-232. doi:10.1016/j.neulet.2006.11.062.
38. Gibson JR, Bartley AF, Hays SA, Huber KM (2008) Imbalance of Neocortical Excitation and Inhibition and Altered UP States Reflect Network Hyperexcitability in the Mouse Model of Fragile X Syndrome. J Neurophysiol 100: 2615- 2626. doi:10.1152/jn.90752.2008.
39. Paluszkiewicz SM, Olmos-Serrano JL, Corbin JG, Huntsman MM (2011) Impaired inhibitory control of cortical synchronization in fragile X syndrome. J Neurophysiol 106: 2264-2272. doi:10.1152/jn.00421.2011.
40. Hays SA, Huber KM, Gibson JR (2011) Altered Neocortical Rhythmic Activity States in Fmr1 KO Mice Are Due to Enhanced mGluR5 Signaling and Involve Changes in Excitatory Circuitry. Journal of Neuroscience 31: 14223-14234. doi:10.1523/JNEUROSCI.3157-11.2011.
41. Gonçalves JT, Anstey JE, Golshani P, Portera-Cailliau C (2013) Circuit level defects in the developing neocortex of Fragile X mice. Nature Neuroscience 16: 903-909. doi:10.1038/nn.3415.
42. Patel AB, Loerwald KW, Huber KM, Gibson JR (2014) Postsynaptic FMRP Promotes the Pruning of Cell-to-Cell Connections among Pyramidal Neurons in the L5A Neocortical Network. Journal of Neuroscience 34: 3413-3418. doi:10.1523/JNEUROSCI.2921-13.2014.
43. O'Connor DH, Clack NG, Huber D, Komiyama T, Myers EW, et al. (2010) Vibrissa-Based Object Localization in Head-Fixed Mice. Journal of Neuroscience 30: 1947-1967. doi:10.1523/JNEUROSCI.3762-09.2010.
44. Huber D, Gutnisky DA, Peron S, O'Connor DH, Wiegert JS, et al. (2013) Multiple dynamic representations in themotor cortex during sensorimotor learning. Nature 484: 473-478. doi:10.1038/nature11039.
45. Moy SS, Nadler JJ, Young NB, Nonneman RJ, Grossman AW, et al. (2009) Social approach in genetically engineered mouse lines relevant to autism. Genes Brain Behav 8: 129-142. doi:10.1111/j.1601-183X.2008.00452.x.
46. deVrij FMS, Levenga J, van der Linde HC, Koekkoek SK, De Zeeuw CI, et al. (2008) Rescue of behavioral phenotype and neuronal protrusion morphology in Fmr1 KO mice. Neurobiology of Disease 31: 127-132. doi:10.1016/j.nbd.2008.04.002.
47. Henderson C, Wijetunge L, Kinoshita MN, Shumway M, Hammond RS, et al. (2012) Reversal of Disease-Related Pathologies in the Fragile X Mouse Model by Selective Activation of GABAB Receptors with Arbaclofen. Science Translational Medicine 4: 152ra128-152ra128. doi:10.1126/scitranslmed.3004218.