Neurofibromin regulates corticostriatal inhibitory networks during working memory performance

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 29, 2010, Pages 13141-13146

  Shilyansky, Carrie ^a   Karlsgodt, Katherine H ^b   Cummings, Damian M ^a   Sidiropoulou, Kyriaki ^c   Hardt, Molly ^b   James, Alex S ^b   Ehninger, Dan ^a   Bearden, Carrie E ^a,b   Poirazi, Panayiota ^c   Jentsch, J David ^a,b   Cannon, Tyrone D ^a,b   Levine, Michael S ^a,b   Silva, Alcino J ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c INSTITUTE OF MOLECULAR BIOLOGY AND BIOTECHNOLOGY   (Greece)

Author keywords

GABA; Learning disability; Neurofibromatosis type I; Prefrontal cortex; Ras

Indexed keywords

4 AMINOBUTYRIC ACID; NEUROFIBROMIN;

AMNESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CORPUS STRIATUM; ELECTROPHYSIOLOGY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; MOUSE; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; WORKING MEMORY;

ANIMALS; BEHAVIOR, ANIMAL; COMPUTER SIMULATION; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; GAMMA-AMINOBUTYRIC ACID; HUMANS; INHIBITORY POSTSYNAPTIC POTENTIALS; MALE; MEMORY, SHORT-TERM; MICE; MODELS, BIOLOGICAL; NEOSTRIATUM; NEURAL INHIBITION; NEUROFIBROMATOSIS 1; NEUROFIBROMIN 1; PREFRONTAL CORTEX; RAS PROTEINS; SIGNAL TRANSDUCTION; YOUNG ADULT;

MUS;

EID: 77955610837     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1004829107     Document Type: Article

References (52)

1. Krab LC, et al. (2008) Impact of neurofibromatosis type 1 on school performance. J Child Neurol 23:1002-1010.
2. Viskochil D, et al. (1990) Deletions and a translocation interrupt a cloned gene at the neurofibromatosis type 1 locus. Cell 62:187-192.
3. Wallace MR, et al. (1990) Type 1 neurofibromatosis gene: Identification of a large transcript disrupted in three NF1 patients. Science 249:181-186.
4. Hyman SL, Shores A, North KN (2005) The nature and frequency of cognitive deficits in children with neurofibromatosis type 1. Neurology 65:1037-1044. (Pubitemid 41429628)
5. Rowbotham I, Pit-ten Cate IM, Sonuga-Barke EJ, Huijbregts SC (2009) Cognitive control in adolescents with neurofibromatosis type 1. Neuropsychology 23:50-60.
6. Costa RM, et al. (2002) Mechanism for the learning deficits in a mouse model of neurofibromatosis type 1. Nature 415:526-530.
7. Cui Y, et al. (2008) Neurofibromin regulation of ERK signaling modulates GABA release and learning. Cell 135:549-560.
8. Bajenaru ML, et al. (2003) Optic nerve glioma in mice requires astrocyte Nf1 gene inactivation and Nf1 brain heterozygosity. Cancer Res 63:8573-8577.
9. Tisch S, Silberstein P, Limousin-Dowsey P, Jahanshahi M (2004) The basal ganglia: Anatomy, physiology, and pharmacology. Psychiatr Clin North Am 27:757-799.
10. Powell KB, Voeller KK (2004) Prefrontal executive function syndromes in children. J Child Neurol 19:785-797.
11. Godefroy O (2003) Frontal syndrome and disorders of executive functions. J Neurol 250:1-6.
12. Fuster JM, Alexander GE (1971) Neuron activity related to short-term memory. Science 173:652-654.
13. Brown VJ, Bowman EM (2002) Rodent models of prefrontal cortical function. Trends Neurosci 25:340-343.
14. Uylings HB, Groenewegen HJ, Kolb B (2003) Do rats have a prefrontal cortex? Behav Brain Res 146:3-17.
15. Taylor CL, Latimer MP, Winn P (2003) Impaired delayed spatial win-shift behaviour on the eight arm radial maze following excitotoxic lesions of the medial prefrontal cortex in the rat. Behav Brain Res 147:107-114.
16. Stühmer T, Puelles L, Ekker M, Rubenstein JL (2002) Expression from a Dlx gene enhancer marks adult mouse cortical GABAergic neurons. Cereb Cortex 12:75-85. (Pubitemid 33152019)
17. Ballester R, et al. (1990) The NF1 locus encodes a protein functionally related to mammalian GAP and yeast IRA proteins. Cell 63:851-859.
18. Xu GF, et al. (1990) The catalytic domain of the neurofibromatosis type 1 gene product stimulates ras GTPase and complements ira mutants of S. cerevisiae. Cell 63:835-841.
19. Li W, et al. (2005) The HMG-CoA reductase inhibitor lovastatin reverses the learning and attention deficits in a mouse model of neurofibromatosis type 1. Curr Biol 15:1961-1967.
20. Rao SG, Williams GV, Goldman-Rakic PS (2000) Destruction and creation of spatial tuning by disinhibition: GABA(A) blockade of prefrontal cortical neurons engaged by working memory. J Neurosci 20:485-494.
21. Constantinidis C, Williams GV, Goldman-Rakic PS (2002) A role for inhibition in shaping the temporal flow of information in prefrontal cortex. Nat Neurosci 5:175-180.
22. Sawaguchi T, Matsumura M, Kubota K (1989) Delayed response deficits produced by local injection of bicuculline into the dorsolateral prefrontal cortex in Japanese macaque monkeys. Exp Brain Res 75:457-469.
23. Funahashi S, Bruce CJ, Goldman-Rakic PS (1993) Dorsolateral prefrontal lesions and oculomotor delayed-response performance: Evidence for mnemonic "scotomas". J Neurosci 13:1479-1497.
24. Funahashi S, Bruce CJ, Goldman-Rakic PS (1989) Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex. J Neurophysiol 61:331-349.
25. Chudasama Y, Robbins TW (2006) Functions of frontostriatal systems in cognition: Comparative neuropsychopharmacological studies in rats, monkeys and humans. Biol Psychol 73:19-38.
26. Floresco SB, Braaksma DN, Phillips AG (1999) Thalamic-cortical-striatal circuitry subserves working memory during delayed responding on a radial arm maze. J Neurosci 19:11061-11071.
27. Floresco SB, Seamans JK, Phillips AG (1997) Selective roles for hippocampal, prefrontal cortical, and ventral striatal circuits in radial-arm maze tasks with or without a delay. J Neurosci 17:1880-1890.
28. Seamans JK, Floresco SB, Phillips AG (1995) Functional differences between the prelimbic and anterior cingulate regions of the rat prefrontal cortex. Behav Neurosci 109:1063-1073.
29. Aarde SM, Jentsch JD (2006) Haploinsufficiency of the arginine-vasopressin gene is associated with poor spatial working memory performance in rats. Horm Behav 49:501-508.
30. Chudasama Y, Robbins TW (2004) Dopaminergic modulation of visual attention and working memory in the rodent prefrontal cortex. Neuropsychopharmacology 29:1628-1636.
31. Jentsch JD, et al. (2009) Dysbindin modulates prefrontal cortical glutamatergic circuits and working memory function in mice. Neuropsychopharmacology 34:2601-2608.
32. Glahn DC, et al. (2002) Maintenance and manipulation in spatial working memory: Dissociations in the prefrontal cortex. Neuroimage 17:201-213.
33. Cannon TD, et al. (2005) Dorsolateral prefrontal cortex activity during maintenance and manipulation of information in working memory in patients with schizophrenia. Arch Gen Psychiatry 62:1071-1080.
34. Moghaddam B, Homayoun H (2008) Divergent plasticity of prefrontal cortex networks. Neuropsychopharmacology 33:42-55.
35. Rawley JB, Constantinidis C (2009) Neural correlates of learning and working memory in the primate posterior parietal cortex. Neurobiol Learn Mem 91:129-138.
36. Menzies L, et al. (2007) Effects of gamma-aminobutyric acid-modulating drugs on working memory and brain function in patients with schizophrenia. Arch Gen Psychiatry 64:156-167. (Pubitemid 46220773)
37. Lanfranchi S, Carretti B, Spanò G, Cornoldi C (2009) A specific deficit in visuospatial simultaneous working memory in Down syndrome. J Intellect Disabil Res 53:474-483.
38. Lanfranchi S, Jerman O, Vianello R (2009) Working memory and cognitive skills in individuals with down syndrome. Child Neuropsychol 15:397-416.
39. Kwon H, et al. (2001) Functional neuroanatomy of visuospatial working memory in fragile X syndrome: Relation to behavioral and molecular measures. Am J Psychiatry 158:1040-1051. (Pubitemid 32623107)
40. Haberecht MF, et al. (2001) Functional neuroanatomy of visuo-spatial working memory in Turner syndrome. Hum Brain Mapp 14:96-107.
41. Dani VS, et al. (2005) Reduced cortical activity due to a shift in the balance between excitation and inhibition in a mouse model of Rett syndrome. Proc Natl Acad Sci USA 102:12560-12565.
42. Fernandez F, et al. (2007) Pharmacotherapy for cognitive impairment in a mouse model of Down syndrome. Nat Neurosci 10:411-413. (Pubitemid 46494581)
43. 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.
44. Centonze D, et al. (2008) Abnormal striatal GABA transmission in the mouse model for the fragile X syndrome. Biol Psychiatry 63:963-973. (Pubitemid 351602272)
45. Bear MF, Dölen G, Osterweil E, Nagarajan N (2008) Fragile X: Translation in action. Neuropsychopharmacology 33:84-87.
46. Zhu Y, et al. (2001) Ablation of NF1 function in neurons induces abnormal development of cerebral cortex and reactive gliosis in the brain. Genes Dev 15:859-876. (Pubitemid 32295067)
47. Cummings DM, et al. (2009) Alterations in cortical excitation and inhibition in genetic mouse models of Huntington's disease. J Neurosci 29:10371-10386.
48. Hines ML, Carnevale NT (1997) The NEURON simulation environment. Neural Comput 9:1179-1209.
49. Smith SM, et al. (2004) Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23 (Suppl 1):S208-S219.
50. Jenkinson M, Smith S (2001) A global optimisation method for robust affine registration of brain images. Med Image Anal 5:143-156. (Pubitemid 35282800)
51. Jenkinson M, Bannister P, Brady M, Smith S (2002) Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage 17:825-841. (Pubitemid 35317016)
52. Behrens TE, et al. (2003) Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging. Nat Neurosci 6:750-757.