Early depolarizing GABA controls critical-period plasticity in the rat visual cortex

Nature Neuroscience

Volumn 18, Issue 1, 2015, Pages 87-96

  Deidda, Gabriele ^a   Allegra, Manuela ^b,c   Cerri, Chiara ^c   Naskar, Shovan ^a   Bony, Guillaume ^a   Zunino, Giulia ^d   Bozzi, Yuri ^c,d   Caleo, Matteo ^c   Cancedda, Laura ^a  

^a ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

^b SCUOLA NORMALE SUPERIORE   (Italy)

^c CNR   (Italy)

^d UNIVERSITY OF TRENTO   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; BUMETANIDE; FUROSEMIDE; MANNITOL; 4 AMINOBUTYRIC ACID RECEPTOR BLOCKING AGENT; DIURETIC AGENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BRAIN CELL; BRAIN CORTEX; CELL COUNT; CELL DENSITY; CELL MATURATION; CONTROLLED STUDY; CRITICAL PERIOD PLASTICITY; DEPOLARIZATION; DOWN REGULATION; ELECTROPORATION; EVOKED VISUAL RESPONSE; EXTRACELLULAR MATRIX; EXTRACELLULAR SPACE; EYE DOMINANCE; FEMALE; GABAERGIC TRANSMISSION; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; INTERNEURON; LATERAL GENICULATE BODY; LEARNING; LONG TERM POTENTIATION; MALE; NERVE CELL PLASTICITY; NEWBORN; NONHUMAN; OSMOLARITY; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PYRAMIDAL NERVE CELL; RAT; SIGNAL TRANSDUCTION; STRIATE CORTEX; VISION; VISUAL ACUITY; VISUAL CORTEX; VISUAL DISCRIMINATION; ANIMAL; CONTRAST SENSITIVITY; DRUG EFFECTS; GROWTH, DEVELOPMENT AND AGING; LONG EVANS RAT; MAZE TEST; PHYSIOLOGY;

ANIMALS; ANIMALS, NEWBORN; BUMETANIDE; CONTRAST SENSITIVITY; CRITICAL PERIOD (PSYCHOLOGY); DIURETICS; EVOKED POTENTIALS, VISUAL; FEMALE; GABA ANTAGONISTS; GAMMA-AMINOBUTYRIC ACID; MALE; MAZE LEARNING; NEURONAL PLASTICITY; RATS; RATS, LONG-EVANS; VISUAL CORTEX;

EID: 84926137163     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.3890     Document Type: Article

References (57)

1. Berardi, N., Pizzorusso, T. & Maffei, L. Critical periods during sensory development. Curr. Opin. Neurobiol. 10, 138-145 (2000).
2. Espinosa, J.S. & Stryker, M.P. Development and plasticity of the primary visual cortex. Neuron 75, 230-249 (2012).
3. Cancedda, L. et al. Acceleration of visual system development by environmental enrichment. J. Neurosci. 24, 4840-4848 (2004).
4. Morishita, H. & Hensch, T.K. Critical period revisited: impact on vision. Curr. Opin. Neurobiol. 18, 101-107 (2008).
5. Huang, Z.J. et al. BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex. Cell 98, 739-755 (1999).
6. Fagiolini, M. & Hensch, T.K. Inhibitory threshold for critical-period activation in primary visual cortex. Nature 404, 183-186 (2000).
7. Harauzov, A. et al. Reducing intracortical inhibition in the adult visual cortex promotes ocular dominance plasticity. J. Neurosci. 30, 361-371 (2010).
8. Ben-Ari, Y. et al. Refuting the challenges of the developmental shift of polarity of GABA actions: GABA more exciting than ever! Front. Cell. Neurosci. 6, 35 (2012).
9. Sernagor, E., Chabrol, F., Bony, G. & Cancedda, L. GABAergic control of neurite outgrowth and remodeling during development and adult neurogenesis: general rules and differences in diverse systems. Front. Cell. Neurosci. 4, 11 (2010).
10. Wang, D.D. & Kriegstein, A.R. Blocking early GABA depolarization with bumetanide results in permanent alterations in cortical circuits and sensorimotor gating defcits. Cereb. Cortex 21, 574-587 (2011).
11. Cleary, R.T. et al. Bumetanide enhances phenobarbital effcacy in a rat model of hypoxic neonatal seizures. PLoS ONE 8, e57148 (2013); erratum doi:10.1371/annotation/48a011e6-e4d0-4706-9a28-857eba8cfb31 (13 August 2013).
12. Dzhala, V.I. et al. NKCC1 transporter facilitates seizures in the developing brain. Nat. Med. 11, 1205-1213 (2005).
13. Sipilä, S.T., Schuchmann, S., Voipio, J., Yamada, J. & Kaila, K. The cation-chloride cotransporter NKCC1 promotes sharp waves in the neonatal rat hippocampus. J. Physiol. (Lond.) 573, 765-773 (2006).
14. Levelt, C.N. & Hubener, M. Critical-period plasticity in the visual cortex. Annu. Rev. Neurosci. 35, 309-330 (2012).
15. Fagiolini, M., Pizzorusso, T., Berardi, N., Domenici, L. & Maffei, L. Functional postnatal development of the rat primary visual cortex and the role of visual experience: dark rearing and monocular deprivation. Vision Res. 34, 709-720 (1994).
16. Frenkel, M.Y. & Bear, M.F. How monocular deprivation shifts ocular dominance in visual cortex of young mice. Neuron 44, 917-923 (2004).
17. Cancedda, L., Fiumelli, H., Chen, K. & Poo, M.M. Excitatory GABA action is essential for morphological maturation of cortical neurons in vivo. J. Neurosci. 27, 5224-5235 (2007).
18. Menna, E., Cenni, M.C., Naska, S. & Maffei, L. The anterogradely transported BDNF promotes retinal axon remodeling during eye specifc segregation within the LGN. Mol. Cell. Neurosci. 24, 972-983 (2003).
19. Caleo, M. et al. Transient synaptic silencing of developing striate cortex has persistent effects on visual function and plasticity. J. Neurosci. 27, 4530-4540 (2007).
20. Maa, E.H., Kahle, K.T., Walcott, B.P., Spitz, M.C. & Staley, K.J. Diuretics and epilepsy: will the past and present meet? Epilepsia 52, 1559-1569 (2011).
21. Hochman, D.W. The extracellular space and epileptic activity in the adult brain: explaining the antiepileptic effects of furosemide and bumetanide. Epilepsia 53 (suppl. 1), 18-25 (2012).
22. Haglund, M.M. & Hochman, D.W. Furosemide and mannitol suppression of epileptic activity in the human brain. J. Neurophysiol. 94, 907-918 (2005).
23. Hensch, T.K. et al. Local GABA circuit control of experience-dependent plasticity in developing visual cortex. Science 282, 1504-1508 (1998).
24. Greifzu, F. et al. Environmental enrichment extends ocular dominance plasticity into adulthood and protects from stroke-induced impairments of plasticity. Proc. Natl. Acad. Sci. USA 111, 1150-1155 (2014).
25. Pizzorusso, T. et al. Reactivation of ocular dominance plasticity in the adult visual cortex. Science 298, 1248-1251 (2002).
26. A) receptor signaling and brain-derived neurotrophic factor (BDNF) release in developing neurons. J. Biol. Chem. 286, 21667-21677 (2011).
27. Mantelas, A., Stamatakis, A., Kazanis, I., Philippidis, H. & Stylianopoulou, F. Control of neuronal nitric oxide synthase and brain-derived neurotrophic factor levels by GABA-A receptors in the developing rat cortex. Brain Res. Dev. Brain Res. 145, 185-195 (2003).
28. Jang, S.W. et al. A selective TrkB agonist with potent neurotrophic activities by 7, 8-dihydroxyfavone. Proc. Natl. Acad. Sci. USA 107, 2687-2692 (2010).
29. Gianfranceschi, L. et al. Visual cortex is rescued from the effects of dark rearing by overexpression of BDNF. Proc. Natl. Acad. Sci. USA 100, 12486-12491 (2003).
30. Ciucci, F. et al. Insulin-like growth factor 1 (IGF-1) mediates the effects of enriched environment (EE) on visual cortical development. PLoS ONE 2, e475 (2007).
31. Fagiolini, M. et al. Separable features of visual cortical plasticity revealed by N-methyl-d-aspartate receptor 2A signaling. Proc. Natl. Acad. Sci. USA 100, 2854-2859 (2003).
32. Stephany, C.É. et al. Plasticity of binocularity and visual acuity are differentially limited by nogo receptor. J. Neurosci. 34, 11631-11640 (2014).
33. Tyzio, R. et al. Maternal oxytocin triggers a transient inhibitory switch in GABA signaling in the fetal brain during delivery. Science 314, 1788-1792 (2006).
34. Tyzio, R. et al. Oxytocin-mediated GABA inhibition during delivery attenuates autism pathogenesis in rodent offspring. Science 343, 675-679 (2014).
35. Sale, A. et al. Environmental enrichment in adulthood promotes amblyopia recovery through a reduction of intracortical inhibition. Nat. Neurosci. 10, 679-681 (2007).
36. Gao, M. et al. Rebound potentiation of inhibition in juvenile visual cortex requires vision-induced BDNF expression. J. Neurosci. 34, 10770-10779 (2014).
37. Abidin, I., Eysel, U.T., Lessmann, V. & Mittmann, T. Impaired GABAergic inhibition in the visual cortex of brain-derived neurotrophic factor heterozygous knockout mice. J. Physiol. (Lond.) 586, 1885-1901 (2008).
38. Jang, H.J. et al. Layer-specifc serotonergic facilitation of IPSC in layer 2/3 pyramidal neurons of the visual cortex. J. Neurophysiol. 107, 407-416 (2012).
39. Maffei, A., Lambo, M.E. & Turrigiano, G.G. Critical period for inhibitory plasticity in rodent binocular V1. J. Neurosci. 30, 3304-3309 (2010).
40. Beurdeley, M. et al. Otx2 binding to perineuronal nets persistently regulates plasticity in the mature visual cortex. J. Neurosci. 32, 9429-9437 (2012).
41. Chattopadhyaya, B. et al. GAD67-mediated GABA synthesis and signaling regulate inhibitory synaptic innervation in the visual cortex. Neuron 54, 889-903 (2007).
42. Huberman, A.D., Feller, M.B. & Chapman, B. Mechanisms underlying development of visual maps and receptive felds. Annu. Rev. Neurosci. 31, 479-509 (2008).
43. Mellios, N. et al. miR-132, an experience-dependent microRNA, is essential for visual cortex plasticity. Nat. Neurosci. 14, 1240-1242 (2011).
44. Tognini, P., Putignano, E., Coatti, A. & Pizzorusso, T. Experience-dependent expression of miR-132 regulates ocular dominance plasticity. Nat. Neurosci. 14, 1237-1239 (2011).
45. Weaver, I.C. et al. Epigenetic programming by maternal behavior. Nat. Neurosci. 7, 847-854 (2004).
46. Deidda, G., Bozarth, I.F. & Cancedda, L. Modulation of GABAergic transmission in development and neurodevelopmental disorders: investigating physiology and pathology to gain therapeutic perspectives. Front. Cell. Neurosci. doi:10.3389/fncel.2014.00119 (22 May 2014).
47. Lemonnier, E. et al. A randomised controlled trial of bumetanide in the treatment of autism in children. Transl. Psychiatry 2, e202 (2012).
48. -cotransporter NKCC1. J. Child Neurol. 24, 572-576 (2009).
49. Vanhatalo, S., Hellstrom-Westas, L. & De Vries, L.S. Bumetanide for neonatal seizures: based on evidence or enthusiasm? Epilepsia 50, 1292-1293 (2009).
50. Chabwine, J.N. & Vanden Eijnden, S. A claim for caution in the use of promising bumetanide to treat neonatal seizures. J. Child Neurol. 26, 657-658, author reply 658-659 (2011).
51. Allegra, M. et al. Altered GABAergic markers, increased binocularity and reduced plasticity in the visual cortex of Engrailed-2 knockout mice. Front. Cell. Neurosci. 8, 163 (2014).
52. dal Maschio, M. et al. High-performance and site-directed in utero electroporation by a triple-electrode probe. Nat. Commun. 3, 960 (2012).
53. Antonucci, F. et al. Cracking down on inhibition: selective removal of GABAergic interneurons from hippocampal networks. J. Neurosci. 32, 1989-2001 (2012).
54. Sgadò, P. et al. Loss of GABAergic neurons in the hippocampus and cerebral cortex of Engrailed-2 null mutant mice: implications for autism spectrum disorders. Exp. Neurol. 247, 496-505 (2013).
55. Chattopadhyaya, B. et al. Experience and activity-dependent maturation of perisomatic GABAergic innervation in primary visual cortex during a postnatal critical period. J. Neurosci. 24, 9598-9611 (2004).
56. Ge, S. et al. GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature 439, 589-593 (2006).
57. Jovanovic, J.N., Czernik, A.J., Fienberg, A.A., Greengard, P. & Sihra, T.S. Synapsins as mediators of BDNF-enhanced neurotransmitter release. Nat. Neurosci. 3, 323-329 (2000).