Impaired inhibitory control of cortical synchronization in fragile X syndrome

Journal of Neurophysiology

Volumn 106, Issue 5, 2011, Pages 2264-2272

  Paluszkiewicz, Scott M ^a,b   Olmos Serrano, Jose Luis ^a   Corbin, Joshua G ^a   Huntsman, Molly M ^a  

^a CHILDREN'S NATIONAL MEDICAL CENTER   (United States)

^b GEORGETOWN UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

aminobutyric acid; Barrel cortex; Developmental disorder; Interneuron

Indexed keywords

3,5 DIHYDROXYPHENYLGLYCINE; FRAGILE X MENTAL RETARDATION PROTEIN; SOMATOSTATIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CELL; CELL ACTIVATION; CONTROLLED STUDY; CORTICAL SYNCHRONIZATION; FRAGILE X SYNDROME; MALE; MOUSE; NERVE CELL MEMBRANE STEADY POTENTIAL; NERVE CELL NETWORK; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SOMATOSENSORY CORTEX; SYNAPTIC INHIBITION;

ACTION POTENTIALS; ANIMALS; CORTICAL SYNCHRONIZATION; FRAGILE X MENTAL RETARDATION PROTEIN; FRAGILE X SYNDROME; GAMMA-AMINOBUTYRIC ACID; INTERNEURONS; MALE; METHOXYHYDROXYPHENYLGLYCOL; MICE; MICE, INBRED STRAINS; MICE, KNOCKOUT; NEURAL INHIBITION; ORGAN CULTURE TECHNIQUES; PHENOTYPE; PYRAMIDAL CELLS; RECEPTORS, METABOTROPIC GLUTAMATE; SOMATOSENSORY CORTEX; SOMATOSTATIN; SYNAPTIC TRANSMISSION;

EID: 80755188026     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00421.2011     Document Type: Article

References (52)

1. Agmon A, Connors BW. Thalamocortical responses of mouse somatosensory (barrel) cortex in vitro. Neuroscience 41: 365-379, 1991.
2. Bassell GJ, Warren ST. Fragile X syndrome: loss of local mRNA regulation alters synaptic development and function. Neuron 60: 201-214, 2008.
3. Beierlein M, Gibson JR, Connors BW. A network of electrically coupled interneurons drives synchronized inhibition in neocortex. Nat Neurosci 3: 904-910, 2000.
4. Beierlein M, Gibson JR, Connors BW. Two dynamically distinct inhibitory networks in layer 4 of the neocortex. J Neurophysiol 90: 2987-3000, 2003.
5. Berry-Kravis E. Epilepsy in fragile X syndrome. Dev Med Child Neurol 44: 724-728, 2002.
6. Berry-Kravis E, Raspa M, Loggin-Hester L, Bishop E, Holiday D, Bailey DB. Seizures in fragile X syndrome: characteristics and comorbid diagnoses. Am J Intellect Dev Disabil 115: 461-472, 2010.
7. Bianchi R, Chuang SC, Zhao W, Young SR, Wong RK. Cellular plasticity for group I mGluR-mediated epileptogenesis. J Neurosci 29: 3497-3507, 2009.
8. Blatow M, Rozov A, Katona I, Hormuzdi SG, Meyer AH, Whittington MA, Caputi A, Monyer H. A novel network of multipolar bursting interneurons generates theta frequency oscillations in neocortex. Neuron 38: 805-817, 2003.
9. Buckmaster PS, Jongen-Rêlo AL. Highly specific neuron loss preserves lateral inhibitory circuits in the dentate gyrus of kainate-induced epileptic rats. J Neurosci 19: 9519-9529, 1999.
10. Cardin JA, Carlén M, Meletis K, Knoblich U, Zhang F, Deisseroth K, Tsai LH, Moore CI. Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature 459: 663-667, 2009.
11. Chu Z, Hablitz JJ. Activation of group I mGluRs increases spontaneous IPSC frequency in rat frontal cortex. J Neurophysiol 80: 621-627, 1998.
12. Chuang SC, Zhao W, Bauchwitz R, Yan Q, Bianchi R, Wong RK. Prolonged epileptiform discharges induced by altered group I metabotropic glutamate receptor-mediated synaptic responses in hippocampal slices of a fragile X mouse model. J Neurosci 25: 8048-8055, 2005.
13. Cossart R, Dinocourt C, Hirsch JC, Merchan-Perez A, De Felipe J, Ben-Ari Y, Esclapez M, Bernard C. Dendritic but not somatic GABAergic inhibition is decreased in experimental epilepsy. Nat Neurosci 4: 52-62, 2001.
14. Deans MR, Gibson JR, Sellitto C, Connors BW, Paul DL. Synchronous activity of inhibitory networks in neocortex requires electrical synapses containing connexin36. Neuron 31: 477-485, 2001.
15. Dolen G, Bear MF. Role for metabotropic glutamate receptor 5 (mGluR5) in the pathogenesis of fragile X syndrome. J Physiol 586: 1502-1508, 2008.
16. Fanselow EE, Connors BW. The roles of somatostatin-expressing (GIN) and fast-spiking inhibitory interneurons in UP-DOWN states of mouse neocortex. J Neurophysiol 104: 596-606, 2010.
17. Fanselow EE, Richardson KA, Connors BW. Selective, state-dependent activation of somatostatin-expressing inhibitory interneurons in mouse neocortex. J Neurophysiol 100: 2640-2652, 2008.
18. Gibson JR, Bartley AF, Hays SA, Huber KM. 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, 2008.
19. Gibson JR, Beierlein M, Connors BW. Two networks of electrically coupled inhibitory neurons in neocortex. Nature 402: 75-79, 1999.
20. Gogolla N, Leblanc JJ, Quast KB, Südhof T, Fagiolini M, Hensch TK. Common circuit defect of excitatory-inhibitory balance in mouse models of autism. J Neurodev Disord 1: 172-181, 2009.
21. Hagerman RJ, Berry-Kravis E, Kaufmann WE, Ono MY, Tartaglia N, Lachiewicz A, Kronk R, Delahunty C, Hessl D, Visootsak J, Picker J, Gane L, Tranfaglia M. Advances in the treatment of fragile X syndrome. Pediatrics 123: 378-390, 2009.
22. Huber KM, Gallagher SM, Warren ST, Bear MF. Altered synaptic plasticity in a mouse model of fragile X mental retardation. Proc Natl Acad Sci USA 99: 7746-7750, 2002.
23. Kahana MJ, Seelig D, Madsen JR. Theta returns. Curr Opin Neurobiol 11: 739-744, 2001.
24. Kapfer C, Glickfield LL, Atallah BV, Scaniziani M. Supralinear increase of recurrent inhibition during sparse activity in the somatosensory cortex. Nat Neurosci 10: 743-753, 2007.
25. Kawaguchi Y. Groupings of nonpyramidal and pyramidal cells with specific physiological and morphological characteristics in rat frontal cortex. J Neurophysiol 69: 416-431, 1993.
26. Kawaguchi Y, Kubota Y. GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb Cortex 7: 476-486, 1997.
27. Kerner JA, Standaert DG, Penney JBJ, Young AB, Landwehrmeyer GB. Expression of group one metabotropic glutamate receptor subunit mRNAs in neurochemically identified neurons in the rat neostriatum, neocortex, and hippocampus. Mol Brain Res 48: 259-269, 1997.
28. Landisman CE, Connors BW. Long-term modulation of electrical synapses in the mammalian thalamus. Science 310: 1809-1813, 2005.
29. Lee H, Simpson GV, Logothetis NK, Rainer G. Phase locking of single neuron activity to theta oscillations during working memory in monkey extrastriate visual cortex. Neuron 45: 147-156, 2005.
30. Liao L, Park SK, Xu T, Vanderklish P, Yates JR. Quantitative proteomic analysis of primary neurons reveals diverse changes in synaptic protein content in fmr1 knockout mice. Proc Natl Acad Sci USA 105: 15281-15286, 2008.
31. Long MA, Cruickshank SJ, Jutras MJ, Connors BW. Abrupt maturation of a spike-synchronizing mechanism in neocortex. J Neurosci 25: 7309-7316, 2005.
32. Maccarrone M, Rossi S, Bari M, De Chiara V, Rapino C, Bernardi G, Bagni C, Centonze D. Abnormal mGlu5 receptor/endocannabinoid coupling in mice lacking FMRP and BC1 RNA. Neuropsychopharmacology 35: 1500-1509, 2010.
33. Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, Wu C. Interneurons of the neocortical inhibitory system. Nat Rev Neurosci 5: 793-807, 2004.
34. Miller LJ, McIntosh DN, McGrath J, Shyu V, Lampe M, Taylor AK, Tassone F, Neitzel K, Stackhouse T, Hagerman RJ. Electrodermal responses to sensory stimuli in individuals with fragile X syndrome: a preliminary report. Am J Med Genet 83: 268-279, 1999.
35. Moore CI, Carlen M, Knoblich U, Cardin JA. Neocortical interneurons: from diversity, strength. Cell 142: 189-193, 2010.
36. Musumeci SA, Bosco P, Calabrese G, Bakker C, De Sarro GB, Elia M, Ferri R, Oostra BA. Audiogenic seizure susceptibility in transgenic mice with fragile X syndrome. Epilepsia 41: 19-23, 2000.
37. Nyhus E, Curran T. Functional role of gamma and theta oscillations in episodic memory. Neurosci Biobehav Rev 34: 1023-1035, 2010.
38. Olmos-Serrano JL, Paluszkiewicz SM, Martin BS, Kaufmann WE, Corbin JG, Huntsman MM. Defective GABAergic neurotransmission and pharmacological rescue of neuronal hyperexcitability in the amygdala in a mouse model of fragile X syndrome. J Neurosci 30: 9929-9938, 2010.
39. Perez Velazquez JL, Barcelo F, Hung Y, Leschenko Y, Nenadovic V, Belkas J, Raghavan V, Brian J, Garcia Dominguez L. Decreased brain coordinated activity in autism spectrum disorders during executive tasks: reduced long-range synchronization in the fronto-parietal networks. Int J Psychophysiol 73: 341-349, 2009.
40. Porter JT, Johnson CK, Agmon A. Diverse types of interneurons generate thalamus-evoked feedforward inhibition in the mouse barrel cortex. J Neurosci 21: 2699-2710, 2001.
41. Raghavachari S, Lisman JE, Tully M, Madsen JR, Bromfield EB, Kahana MJ. Theta oscillations in human cortex during a working-memory task: evidence for local generators. J Neurophysiol 95: 1630-1638, 2006.
42. Sederberg PB, Kahana MJ, Howard MW, Donner EJ, Madsen JR. Theta and gamma oscillations during encoding predict subsequent recall. J Neurosci 23: 10809-10814, 2003.
43. Silberberg G, Markram H. Disynaptic inhibition between neocortical pyramidal cells mediated by Martinotti cells. Neuron 53: 735-746, 2007.
44. Sohal VS, Zhang F, Yizhar O, Deisseroth K. Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature 459: 698-702, 2009.
45. Stinehelfer S, Vruwink M, Burette A. Immunolocalization of mGluR1alpha in specific populations of local circuit neurons in the cerebral cortex. Brain Res 861: 37-44, 2000.
46. Szabadics J, Lorincz A, Tamas G. Beta and gamma frequency synchronization by dendritic GABAergic synapses and gap junctions in a network of cortical interneurons. J Neurosci 21: 5824-5831, 2001.
47. Uhlhaas PJ, Roux F, Rodriguez E, Rotarska-Jagiela A, Singer W. Neural synchrony and the development of cortical networks. Trends Cogn Sci 14: 72-80, 2010.
48. Uhlhaas PJ, Singer W. Neural synchrony in brain disorders: relevance for cognitive dysfunctions and pathophysiology. Neuron 52: 155-168, 2006.
49. Verkerk A, Pieretti M, Sutcliffe JS, Fu YH, Kuhl DP, Pizzuti A, Reiner O, Richards S, Victoria MF, Zhang FP, Eussen BE, van Ommen GB, Blonden LAJ, Riggins GJ, Chastain JL, Kunst CB, Galjaard H, Caskey CT, Nelson DL, Oostra BA, Warren ST. Identification of a gene (FMR-1) containing a CGG repeat coincident with a breakpoint cluster region exhibiting length variation in fragile X syndrome. Cell 65: 905-914, 1991.
50. Wang Y, Toledo-Rodriguez M, Gupta A, Wu C, Silberberg G, Luo J, Markram H. Anatomical, physiological and molecular properties of Martinotti cells in the somatosensory cortex of the juvenile rat. J Physiol 561: 65-90, 2004.
51. Xu X, Roby KD, Callaway EM. Mouse cortical inhibitory neuron type that coexpresses somatostatin and calretinin. J Comp Neurol 499: 144-160, 2006.
52. Zhang L, Alger BE. Enhanced endocannabinoid signaling elevates neuronal excitability in fragile X syndrome. J Neurosci 30: 5724-5729, 2010.