Comparison of brain maturation among species: An example in translational research suggesting the possible use of bumetanide in newborn

Frontiers in Neurology

Volumn 4 APR, Issue , 2013, Pages 1-

  Pressler, Ronit ^a,b   Auvin, Stéphane ^c,d  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b GREAT ORMOND STREET HOSPITAL   (United Kingdom)

^c INSERM   (France)

^d HÔPITAL ROBERT DEBRÉ   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANTICONVULSIVE AGENT; BUMETANIDE; ETIRACETAM; KAINIC ACID; LOOP DIURETIC AGENT; PHENOBARBITAL; PHENYTOIN; SODIUM POTASSIUM CHLORIDE COTRANSPORTER;

ANTICONVULSANT ACTIVITY; APOPTOSIS; ARTICLE; ASTROCYTE; BRAIN CORTEX; BRAIN DEVELOPMENT; BRAIN GROWTH; BRAIN HYPOXIA; BRAIN MATURATION; BRAIN NERVE CELL; BRAIN REGION; BRAIN SLICE; CELL MIGRATION; DRUG EFFICACY; DRUG MECHANISM; EXPERIMENTAL MODEL; FERTILIZATION; FOOT; GESTATIONAL AGE; HAND FUNCTION; HIPPOCAMPUS; HUMAN; HUMAN EMBRYO; HYPOXIC ISCHEMIC ENCEPHALOPATHY; IN VIVO STUDY; INFANTILE SPASM; LOCOMOTION; METABOLIC DISORDER; NERVE EXCITABILITY; NERVE STIMULATION; NERVOUS SYSTEM DEVELOPMENT; NEUROTRANSMISSION; NEWBORN PERIOD; NONHUMAN; PERINATAL PERIOD; RISK BENEFIT ANALYSIS; SEIZURE; SEIZURE SUSCEPTIBILITY; SENSORY GATING; SPECIES COMPARISON; SYNAPTIC INHIBITION; SYNAPTOGENESIS; TRANSLATIONAL RESEARCH; TREATMENT RESPONSE;

EID: 84878782432     PISSN: None     EISSN: 16642295     Source Type: Journal    
DOI: 10.3389/fneur.2013.00036     Document Type: Article

References (55)

1. Al-Ghoul, W. M., and Miller, M. W. (1989). Transient expression of Alz-50 immunoreactivity in developing rat neocortex: a marker for naturally occurring neuronal death? Brain Res. 481, 361-367.
2. Bar, I., de, R. C., and Goffinet, A. M. (2000). The evolution of cortical development. An hypothesis based on the role of the Reelin signaling pathway. Trends Neurosci. 23, 633-638.
3. Bayer, S. A., Altman, J., Russo, R. J., and Zhang, X. (1993). Timetables of neurogenesis in the human brain based on experimentally determined patterns in the rat. Neurotoxicology 14, 83-144.
4. Ben-Ari, Y., and Holmes, G. L. (2006). Effects of seizures on developmental processes in the immature brain. Lancet Neurol. 5, 1055-1063.
5. Bittigau, P., Sifringer, M., Genz, K., Reith, E., Pospischil, D., Govindarajalu, S., et al. (2002). Antiepileptic drugs and apoptotic neurodegeneration in the developing brain. Proc. Natl. Acad. Sci. U.S.A. 99, 15089-15094.
6. Blume, H. K., Garrison, M. M., and Christakis, D. A. (2009). Neonatal seizures: treatment and treatment variability in 31 United States pediatric hospitals. J. Child Neurol. 24, 148-154.
7. Booth, D., and Evans, D. J. (2004). Anticonvulsants for neonates with seizures. Cochrane Database Syst. Rev. 18, CD004218.
8. Boylan, G. B., Rennie, J. M., Chorley, G., Pressler, R. M., Fox, G. F., Farrer, K., et al. (2004). Second-line anticonvulsant treatment of neonatal seizures: a video-EEG monitoring study. Neurology 62, 486-488.
9. Catalano, S. M., Robertson, R. T., and Killackey, H. P. (1991). Early ingrowth of thalamocortical afferents to the neocortex of the prenatal rat. Proc. Natl. Acad. Sci. U.S.A. 88, 2999-3003.
10. Chiron, C., Dulac, O., and Pons, G. (2008). Antiepileptic drug development in children: considerations for a revisited strategy. Drugs 68, 17-25.
11. Cleary, R. T., Sun, H., Huynh, T., Manning, S. M., Li, Y., Rotenberg, A., et al. (2013). Bumetanide enhances phenobarbital efficacy in a rat model of hypoxic neonatal seizures. PLoS ONE 8:e57148. doi: 10.1371/journal.pone.0057148
12. Del Rio, J. A., Martinez, A., Auladell, C., and Soriano, E. (2000). Developmental history of the subplate and developing white matter in the murine neocortex. Neuronal organization and relationship with the main afferent systems at embryonic and perinatal stages. Cereb. Cortex 10, 784-801.
13. Deng, J., and Elberger, A. J. (2003). Corticothalamic and thalamocortical pathfinding in the mouse: dependence on intermediate targets and guidance axis. Anat. Embryol. 207, 177-192.
14. Dzhala, V. I., Talos, D. M., Sdrulla, D. A., Brumback, A. C., Mathews, G. C., Benke, T. A., et al. (2005). NKCC1 transporter facilitates seizures in the developing brain. Nat. Med. 11, 1205-1213.
15. Ferrer, I., Bernet, E., Soriano, E., del, R. T., and Fonseca, M. (1990). Naturally occurring cell death in the cerebral cortex of the rat and removal of dead cells by transitory phagocytes. Neuroscience 39, 451-458.
16. Forcelli, P. A., Janssen, M. J., Vicini, S., and Gale, K. (2012a). Neonatal exposure to antiepileptic drugs disrupts striatal synaptic development. Ann. Neurol. 72, 363-372.
17. Forcelli, P. A., Kozlowski, R., Snyder, C., Kondratyev, A., and Gale, K. (2012b). Effects of neonatal antiepileptic drug exposure on cognitive, emotional, and motor function in adult rats. J. Pharmacol. Exp. Ther. 340, 558-566.
18. Gottlieb, A., Keydar, I., and Epstein, H. T. (1977). Rodent brain growth stages: an analytical review. Biol. Neonate 32, 166-176.
19. Gupta, R. K., Hasan, K. M., Trivedi, R., Pradhan, M., Das, V., Parikh, N. A., et al. (2005). Diffusion tensor imaging of the developing human cerebrum. J. Neurosci. Res. 81, 172-178.
20. Herschkowitz, N., Kagan, J., and Zilles, K. (1997). Neurobiological bases of behavioral development in the first year. Neuropediatrics 28, 296-306.
21. Hevner, R. F. (2000). Development of connections in the human visual system during fetal mid-gestation: a DiI-tracing study. J. Neuropathol. Exp. Neurol. 59, 385-392.
22. Holmes, G. L. (2005). Effects of seizures on brain development: lessons from the laboratory. Pediatr. Neurol. 33, 1-11.
23. Huttenlocher, P. R., and Dabholkar, A. S. (1997). Regional differences in synaptogenesis in human cerebral cortex. J. Comp. Neurol. 387, 167-178.
24. Jensen, F. E. (2009). Developmental factors in the pathogenesis of neonatal seizures. J. Pediatr. Neurol. 7, 5-12.
25. Kahle, K. T., Barnett, S. M., Sassower, K. C., and Staley, K. J. (2009). Decreased seizure activity in a human neonate treated with bumetanide, an inhibitor of the Na(+)-K(+)-2Cl(-) cotransporter NKCC1. J. Child Neurol. 24, 572-576.
26. Khazipov, R., Esclapez, M., Caillard, O., Bernard, C., Khalilov, I., Tyzio, R., et al. (2001). Early development of neuronal activity in the primate hippocampus in utero. J. Neurosci. 21, 9770-9781.
27. Kilb, W., Sinning, A., and Luhmann, H. J. (2007). Model-specific effects of bumetanide on epileptiform activity in the in-vitro intact hippocampus of the newborn mouse. Neuropharmacology 53, 524-533.
28. Kim, J. S., Kondratyev, A., Tomita, Y., and Gale, K. (2007). Neurodevelopmental impact of antiepileptic drugs and seizures in the immature brain. Epilepsia 48(Suppl.5), 19-26.
29. Kostovic, I., and Jovanov-Milosevic, N. (2006). The development of cerebral connections during the first 20-45 weeks' gestation. Semin. Fetal Neonatal Med. 11, 415-422.
30. Kostovic, I., and Judas, M. (2002). Correlation between the sequential ingrowth of afferents and transient patterns of cortical lamination in preterm infants. Anat. Rec. 267, 1-6.
31. Kostovic, I., and Rakic, P. (1990). Developmental history of the transient subplate zone in the visual and somatosensory cortex of the macaque monkey and human brain. J. Comp. Neurol. 297, 441-470.
32. Kretschmann, H. J., Kammradt, G., Krauthausen, I., Sauer, B., and Wingert, F. (1986). Growth of the hippocampal formation in man. Bibl. Anat. 28, 27-52.
33. Letinic, K., and Kostovic, I. (1997). Transient fetal structure, the gangliothalamic body, connects telencephalic germinal zone with all thalamic regions in the developing human brain. J. Comp. Neurol. 384, 373-395.
34. Letinic, K., and Rakic, P. (2001). Telencephalic origin of human thalamic GABAergic neurons. Nat. Neurosci. 4, 931-936.
35. Levitt, P. (2003). Structural and functional maturation of the developing primate brain. J. Pediatr. 143, S35-S45.
36. Mares, P. (2009). Age- and dose-specific anticonvulsant action of bumetanide in immature rats. Physiol. Res. 58, 927-930.
37. Mazarati, A., Shin, D., and Sankar, R. (2009). Bumetanide inhibits rapid kindling in neonatal rats. Epilepsia 50, 2117-2122.
38. Miller, S. P., Weiss, J., Barnwell, A., Ferriero, D. M., Latal-Hajnal, B., Ferrer-Rogers, A., et al. (2002). Seizure-associated brain injury in term newborns with perinatal asphyxia. Neurology 58, 542-548.
39. Molliver, M. E., Kostovic, I., and van der, L. H. (1973). The development of synapses in cerebral cortex of the human fetus. Brain Res. 50, 403-407.
40. Painter, M. J., Scher, M. S., Stein, A. D., Armatti, S., Wang, Z., Gardiner, J. C., et al. (1999). Phenobarbital compared with phenytoin for the treatment of neonatal seizures. N. Engl. J. Med. 341, 485-489.
41. Pangratz-Fuehrer, S., and Hestrin, S. (2011). Synaptogenesis of electrical and GABAergic synapses of fast-spiking inhibitory neurons in the neocortex. J. Neurosci. 31, 10767-10775.
42. Price, D. J., Aslam, S., Tasker, L., and Gillies, K. (1997). Fates of the earliest generated cells in the developing murine neocortex. J. Comp. Neurol. 377, 414-422.
43. Raedler, E., Raedler, A., and Feldhaus, S. (1980). Dynamical aspects of neocortical histogenesis in the rat. Anat. Embryol. 158, 253-269.
44. Romijn, H. J., Hofman, M. A., and Gramsbergen, A. (1991). At what age is the developing cerebral cortex of the rat comparable to that of the full-term newborn human baby? Early Hum. Dev. 26, 61-67.
45. Ronen, G. M., Buckley, D., Penney, S., and Streiner, D. L. (2007). Long-term prognosis in children with neonatal seizures: a population-based study. Neurology 69, 1816-1822.
46. Schlumpf, M., Shoemaker, W. J., and Bloom, F. E. (1980). Innervation of embryonic rat cerebral cortex by catecholamine-containing fibers. J. Comp. Neurol. 192, 361-376.
47. Silverstein, F. S., Jensen, F. E., Inder, T., Hellstrom-Westas, L., Hirtz, D., and Ferriero, D. M. (2008). Improving the treatment of neonatal seizures: national Institute of Neurological Disorders and Stroke workshop report. J. Pediatr. 153, 12-15.
48. Vento, M., de Vries, L. S., Alberola, A., Blennow, M., Steggerda, S., Greisen, G., et al. (2010). Approach to seizures in the neonatal period: a European perspective. Acta Paediatr. 99, 497-501.
49. Wang, D. D., and Kriegstein, A. R. (2011). Blocking Early GABA Depolarization with Bumetanide Results in Permanent Alterations in Cortical Circuits and Sensorimotor Gating Deficits. Cereb. Cortex 21, 574-587.
50. Wood, J. G., Martin, S., and Price, D. J. (1992). Evidence that the earliest generated cells of the murine cerebral cortex form a transient population in the subplate and marginal zone. Brain Res. Dev. Brain Res. 66, 137-140.
51. Wood, S. L., Beyer, B. K., and Cappon, G. D. (2003). Species comparison of postnatal CNS development: functional measures. Birth Defects Res. B Dev. Reprod. Toxicol. 68, 391-407.
52. Zagon, I. S., and McLaughlin, P. J. (1977). Effect of chronic maternal methadone exposure on perinatal development. Biol. Neonate 31, 271-282.
53. Zecevic, N. (1998). Synaptogenesis in layer I of the human cerebral cortex in the first half of gestation. Cereb. Cortex 8, 245-252.
54. Zecevic, N., Bourgeois, J. P., and Rakic, P. (1989). Changes in synaptic density in motor cortex of rhesus monkey during fetal and postnatal life. Brain Res. Dev. Brain Res. 50, 11-32.
55. Zeng, S. J., Lin, Y. T., Tian, C. P., Song, K. J., Zhang, X. W., and Zuo, M. X. (2009). Evolutionary significance of delayed neurogenesis in the core versus shell auditory areas of Mus musculus. J. Comp. Neurol. 515, 600-613.