Cognitive dysfunction in the dystrophin-deficient mouse model of Duchenne muscular dystrophy: A reappraisal from sensory to executive processes

Neurobiology of Learning and Memory

Volumn 124, Issue , 2015, Pages 111-122

  Chaussenot, Rémi ^a,b   Edeline, Jean Marc ^a,b   Le Bec, Benoit ^a,b,c   El Massioui, Nicole ^a,b   Laroche, Serge ^a,b   Vaillend, Cyrille ^a,b  

^a CNRS   (France)

^b UNIVERSITÉ PARIS SACLAY   (France)

^c Unite de Neurosciences Integratives et Computationnelles   (France)

Author keywords

Associative learning; Executive functions; Hearing; mdx mouse; Spatial learning; Working memory

Indexed keywords

DYSTROPHIN;

AMYGDALOID NUCLEUS; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUDITORY STIMULATION; BRAIN LEVEL; BRAIN TISSUE; COGNITIVE DEFECT; CONTROLLED STUDY; DUCHENNE MUSCULAR DYSTROPHY; EVOKED BRAIN STEM AUDITORY RESPONSE; EXECUTIVE FUNCTION; FEAR; FEMALE; MALE; MAZE TEST; MEMORY CONSOLIDATION; MOUSE; MOUSE MODEL; NERVE CELL NETWORK; NONHUMAN; PERCEPTION; PREPULSE INHIBITION; PROTEIN DEFICIENCY; RADIAL ARM MAZE TEST; SENSORY GATING; SPATIAL LEARNING; SPATIAL MEMORY; STARTLE REFLEX; STATE DEPENDENT LEARNING; WATER MAZE TEST; WORKING MEMORY; ANIMAL; AVOIDANCE BEHAVIOR; BRAIN; C57BL MOUSE; CONDITIONED REFLEX; DISEASE MODEL; GENETICS; HEARING; LONG TERM MEMORY; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; PSYCHOLOGY; SHORT TERM MEMORY; SPATIAL ORIENTATION; X CHROMOSOME LINKED MUSCULAR DYSTROPHIC MOUSE;

ACOUSTIC STIMULATION; ANIMALS; AUDITORY PERCEPTION; AVOIDANCE LEARNING; BEHAVIOR, ANIMAL; BRAIN; COGNITION DISORDERS; CONDITIONING, CLASSICAL; DISEASE MODELS, ANIMAL; DYSTROPHIN; EVOKED POTENTIALS, AUDITORY, BRAIN STEM; EXECUTIVE FUNCTION; FEAR; MAZE LEARNING; MEMORY, LONG-TERM; MEMORY, SHORT-TERM; MICE; MICE, INBRED C57BL; MICE, INBRED MDX; MUSCULAR DYSTROPHY, DUCHENNE; REFLEX, STARTLE; SENSORY GATING; SPATIAL MEMORY; SPATIAL NAVIGATION;

EID: 84941260163     PISSN: 10747427     EISSN: 10959564     Source Type: Journal    
DOI: 10.1016/j.nlm.2015.07.006     Document Type: Article

References (56)

1. Anderson J.L., Morley J.W., Head S.I. Enhanced homosynaptic LTD in cerebellar Purkinje cells of the dystrophic MDX mouse. Muscle and Nerve 2010, 41(3):329-334.
2. Björklund M., Siverina I., Heikkinen T., Tanila H., Sallinen J., Scheinin M., et al. Spatial working memory improvement by an alpha2-adrenoceptor agonist dexmedetomidine is not mediated through alpha2C-adrenoceptor. Progress in Neuro-Psychopharmacology and Biological Psychiatry 2001, 25:1539-1554.
3. Carretta D., Santarelli M., Sbriccoli A., Pinto F., Catini C., Minciacchi D. Spatial analysis reveals alterations of parvalbumin- and calbindin-positive local circuit neurons in the cerebral cortex of mutant mdx mice. Brain Research 2004, 1016(1):1-11.
4. Chabout J., Cressant A., Hu X., Edeline J.M., Granon S. Making choice between competing rewards in uncertain vs. safe social environment: Role of neuronal nicotinic receptors of acetylcholine. Frontiers in Human Neuroscience 2013, 7:468.
5. Cyrulnik S.E., Hinton V.J. Duchenne muscular dystrophy: A cerebellar disorder?. Neuroscience and Biobehavioral Reviews 2008, 32:486-496.
6. Dallérac G., Perronnet C., Chagneau C., Leblanc-Veyrac P., Samson-Desvignes N., Peltekian E., et al. Rescue of a dystrophin-like protein by exon skipping normalizes synaptic plasticity in the hippocampus of the mdx mouse. Neurobiology of Disease 2011, 43:635-641.
7. D'Angelo M.G., Lorusso M.L., Civati F., Comi G.P., Magri F., Del Bo R., et al. Neurocognitive profiles in Duchenne muscular dystrophy and gene mutation site. Pediatric Neurology 2011, 45:292-299.
8. Desguerre I., Christov C., Mayer M., Zeller R., Becane H.M., Bastuji-Garin S., et al. Clinical heterogeneity of duchenne muscular dystrophy (DMD): Definition of sub-phenotypes and predictive criteria by long-term follow-up. PLoS ONE 2009, 4:e4347.
9. Dodson H.C., Piper T.A., Clarke J.D., Quinlivan R.M., Dickson G. Dystrophin expression in the hair cells of the cochlea. Journal of Neurocytology 1995, 24:625-632.
10. Donders J., Taneja C. Neurobehavioral characteristics of children with Duchenne muscular dystrophy. Child Neuropsychology 2009, 15:295-304.
11. Esclassan F., Coutureau E., Di Scala G., Marchand A.R. Differential contribution of dorsal and ventral hippocampus to trace and delay fear conditioning. Hippocampus 2009, 19(1):33-44.
12. Esclassan F., Coutureau E., Di Scala G., Marchand A.R. A cholinergic-dependent role for the entorhinal cortex in trace fear conditioning. Journal of Neuroscience 2009, 29(25):8087-8093.
13. Gourévitch B., Doisy T., Avillac M., Edeline J.M. Follow-up of latency and threshold shifts of auditory brainstem responses after single and interrupted acoustic trauma in guinea pig. Brain Research 2009, 1304:66-79.
14. Goyenvalle A., Griffith G., Babbs A., El Andaloussi S., Ezzat K., Avril A., et al. Functional correction in mouse models of muscular dystrophy using exon-skipping tricyclo-DNA oligomers. Nature Medicine 2015, 21(3):270-275.
15. Grady R.M., Wozniak D.F., Ohlemiller K.K., Sanes J.R. Cerebellar synaptic defects and abnormal motor behavior in mice lacking alpha- and beta-dystrobrevin. The Journal of Neuroscience 2006, 26:2841-2851.
16. Hashimoto T., Nguyen Q.L., Rotaru D., Keenan T., Arion D., Beneyto M., et al. Protracted developmental trajectories of GABAA receptor alpha1 and alpha2 subunit expression in primate prefrontal cortex. Biological Psychiatry 2009, 65:1015-1023.
17. Herry C., Johansen J.P. Encoding of fear learning and memory in distributed neuronal circuits. Nature Neuroscience 2014, 17(12):1644-1654.
18. Hinton V.J., De Vivo D.C., Nereo N.E., Goldstein E., Stern Y. Poor verbal working memory across intellectual level in boys with Duchenne dystrophy. Neurology 2000, 54:2127-2132.
19. Hinton V.J., De Vivo D.C., Nereo N.E., Goldstein E., Stern Y. Selective deficits in verbal working memory associated with a known genetic etiology: The neuropsychological profile of duchenne muscular dystrophy. Journal of the International Neuropsychological 2001, 7:45-54.
20. Knuesel I., Mastrocola M., Zuellig R.A., Bornhauser B., Schaub M.C., Fritschy J.M. Short communication: Altered synaptic clustering of GABAA receptors in mice lacking dystrophin (mdx mice). European Journal of Neuroscience 1999, 11:4457-4462.
21. Koch M. The neurobiology of startle. Progress in Neurobiology 1999, 59(2):107-128.
22. Kohl S., Heekeren K., Klosterkötter J., Kuhn J. Prepulse inhibition in psychiatric disorders-apart from schizophrenia. Journal of Psychiatric Research 2013, 47:445-452.
23. LeDoux J.E. Emotion circuits in the brain. Annual Review of Neuroscience 2000, 23:155-184.
24. Leppä E., Linden A.M., Vekovischeva O.Y., Swinny J.D., Rantanen V., Toppila E., et al. Removal of GABA(A) receptor γ2 subunits from parvalbumin neurons causes wide-ranging behavioral alterations. PLoS ONE 2011, 6:e24159.
25. Lidov H.G., Byers T.J., Kunkel L.M. The distribution of dystrophin in the murine central nervous system: An immunocytochemical study. Neuroscience 1993, 54:167-187.
26. Lorusso M.L., Civati F., Molteni M., Turconi A.C., Bresolin N., D'Angelo M.G. Specific profiles of neurocognitive and reading functions in a sample of 42 Italian boys with Duchenne Muscular Dystrophy. Child Neuropsychology 2013, 19:350-369.
27. Makkar S.R., Zhang S.Q., Cranney J. Behavioral and neural analysis of GABA in the acquisition, consolidation, reconsolidation, and extinction of fear memory. Neuropsychopharmacology 2010, 35:1625-1652.
28. Mento G., Tarantino V., Bisiacchi P.S. The neuropsychological profile of infantile Duchenne muscular dystrophy. The Clinical Neuropsychologist 2011, 25:1359-1377.
29. Miranda R., Sébrié C., Degrouard J., Gillet B., Jaillard D., Laroche S., et al. Reorganization of inhibitory synapses and increased PSD length of perforated excitatory synapses in hippocampal area CA1 of dystrophin-deficient mdx mice. Cerebral Cortex 2009, 19:876-888.
30. Pastoret C., Sebille A. Mdx mice show progressive weakness and muscle deterioration with age. Journal of Neurological Science 1995, 129(2):97-105.
31. Paxinos, G., Franklin, K. B. J. (2001). The mouse brain in stereotaxic coordinates, 2nd ed. Academic Press, San Diego (CA).
32. Perronnet C., Chagneau C., Le Blanc P., Samson-Desvignes N., Mornet D., Laroche S., et al. Upregulation of brain utrophin does not rescue behavioral alterations in dystrophin-deficient mice. Human Molecular Genetics 2012, 21:2263-2276.
33. Perronnet C., Vaillend C. Dystrophins, utrophins, and associated scaffolding complexes: Role in mammalian brain and implications for therapeutic strategies. Journal of Biomedicine and Biotechnology 2010, 2010:849426.
34. Piccini G., Gazzellini S., D'Amico A., Pane M., Castelli E., Vicari S., et al. Developmental lag of visuospatial attention in Duchenne muscular dystrophy. Research in Developmental Disabilities 2014, 36C:55-61.
35. Pillers D.A., Duncan N.M., Dwinnell S.J., Rash S.M., Kempton J.B., Trune D.R. Normal cochlear function in mdx and mdx(Cv3) Duchenne muscular dystrophy mouse models. The Laryngoscope 1999, 109:1310-1312.
36. Pillers D.A., Weleber R.G., Green D.G., Rash S.M., Dally G.Y., Howard P.L., et al. Effects of dystrophin isoforms on signal transduction through neural retina: Genotype-phenotype analysis of duchenne muscular dystrophy mouse mutants. Molecular Genetics and Metabolism 1999, 66:100-110.
37. Powell S.B., Zhou X., Geyer M.A. Prepulse inhibition and genetic mouse models of schizophrenia. Behavioural Brain Research 2009, 204:282-294.
38. Poysky J. Behavior patterns in Duchenne muscular dystrophy: Report on the Parent Project Muscular Dystrophy behavior workshop 8-9 of December 2006, Philadelphia, USA. Neuromuscular Disorders 2007, 17:986-994. Behavior in DMD Study Group.
39. Raynor E.M., Mulroy M.J. Sensorineural hearing loss in the mdx mouse: A model of Duchenne muscular dystrophy. The Laryngoscope 1997, 107:1053-1056.
40. Rondi-Reig L., Burguière E. Is the cerebellum ready for navigation?. Progress in Brain Research 2005, 148:199-212.
41. Sbriccoli A., Santarelli M., Carretta D., Pinto F., Granato A., Minciacchi D. Architectural changes of the cortico-spinal system in the dystrophin defective mdx mouse. Neuroscience Letters 1995, 200(1):53-56.
42. Sekiguchi M., Zushida K., Yoshida M., Maekawa M., Kamichi S., Yoshida M., et al. A deficit of brain dystrophin impairs specific amygdala GABAergic transmission and enhances defensive behaviour in mice. Brain 2009, 132:124-135.
43. Sesay A.K., Errington M.L., Levita L., Bliss T.V. Spatial learning and hippocampal long-term potentiation are not impaired in mdx mice. Neuroscience Letters 1996, 211:207-210.
44. Snow W.M., Anderson J.E., Jakobson L.S. Neuropsychological and neurobehavioral functioning in Duchenne muscular dystrophy: A review. Neuroscience and Biobehavioral Reviews 2013, 37:743-752.
45. Vaillend C., Billard J.M., Claudepierre T., Rendon A., Dutar P., Ungerer A. Spatial discrimination learning and CA1 hippocampal synaptic plasticity in mdx and mdx3cv mice lacking dystrophin gene products. Neuroscience 1998, 86:53-66.
46. Vaillend C., Billard J.M., Laroche S. Impaired long-term spatial and recognition memory and enhanced CA1 hippocampal LTP in the dystrophin-deficient Dmd(mdx) mouse. Neurobiology of Disease 2004, 17:10-20.
47. Vaillend C., Perronnet C., Ros C., Gruszczynski C., Goyenvalle A., Laroche S., et al. Rescue of a dystrophin-like protein by exon skipping in vivo restores GABAA-receptor clustering in the hippocampus of the mdx mouse. Molecular Therapy 2010, 18:1683-1688.
48. Vaillend C., Rendon A., Misslin R., Ungerer A. Influence of dystrophin-gene mutation on mdx mouse behavior. I. Retention deficits at long delays in spontaneous alternation and bar-pressing tasks. Behavior Genetics 1995, 25:569-579.
49. Vaillend C., Ungerer A. Behavioral characterization of mdx3cv mice deficient in C-terminal dystrophins. Neuromuscular Disorders 1999, 9(5):296-304.
50. Vojinovic D., Adams H.H., van der Lee S.J., Ibrahim-Verbaas C.A., Brouwer R., van den Hout M.C., et al. The dystrophin gene and cognitive function in the general population. European Journal of Human Genetics 2014.
51. Volk D.W., Pierri J.N., Fritschy J.M., Auh S., Sampson A.R., Lewis D.A. Reciprocal alterations in pre- and postsynaptic inhibitory markers at chandelier cell inputs to pyramidal neurons in schizophrenia. Cerebral Cortex 2002, 12:1063-1070.
52. Waite A., Tinsley C.L., Locke M., Blake D.J. The neurobiology of the dystrophin-associated glycoprotein complex. Annals of Medicine 2009, 41:344-359.
53. Wersinger E., Bordais A., Schwab Y., Sene A., Bénard R., Alunni V., et al. Reevaluation of dystrophin localization in the mouse retina. Investigative Ophthalmology and Visual Science 2011, 52:7901-7908.
54. Wicksell R.K., Kihlgren M., Melin L., Eeg-Olofsson O. Specific cognitive deficits are common in children with Duchenne muscular dystrophy. Developmental Medicine and Child Neurology 2004, 46:154-159.
55. Willott, J. F. (2006). Measurement of the auditory brainstem response (ABR) to study auditory sensitivity in mice. Current Protocols in Neuroscience, Unit 8.21B (Chapter 8).
56. Yeomans J.S., Bosch D., Alves N., Daros A., Ure R.J., Schmid S. GABA receptors and prepulse inhibition of acoustic startle in mice and rats. The European Journal of Neuroscience 2010, 31:2053-2061.