An abrupt developmental shift in callosal modulation of sleep-related spindle bursts coincides with the emergence of excitatory-inhibitory balance and a reduction of somatosensory cortical plasticity

Behavioral Neuroscience

Volumn 124, Issue 5, 2010, Pages 600-611

  Marcano Reik, Amy Jo ^a   Prasad, Tuhina ^a   Weiner, Joshua A ^a   Blumberg, Mark S ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

GABA; Glutamate; KCC2; Myoclonic twitching; Plasticity; REM sleep; Somatosensory cortex

Indexed keywords

BICUCULLINE; MUSCIMOL; POTASSIUM CHLORIDE COTRANSPORTER; POTASSIUM CHLORIDE COTRANSPORTER 2; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORPUS CALLOSUM; ELECTROMYOGRAPHY; FEMALE; FOREFOOT; GABAERGIC TRANSMISSION; GENE DISRUPTION; IMMUNOFLUORESCENCE TEST; MALE; MYOCLONUS; NERVE CELL PLASTICITY; NONHUMAN; PRESYNAPTIC NERVE; PROTEIN EXPRESSION; RAT; REM SLEEP; SLEEP SPINDLE; SOMATOSENSORY CORTEX; UPREGULATION; VISUAL CORTEX;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; BICUCULLINE; CORPUS CALLOSUM; ELECTROENCEPHALOGRAPHY; EVOKED POTENTIALS, SOMATOSENSORY; FEMALE; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; MALE; MUSCIMOL; NEURAL INHIBITION; NEURONAL PLASTICITY; PRESYNAPTIC TERMINALS; RATS; RECOVERY OF FUNCTION; SLEEP; SOMATOSENSORY CORTEX; SYMPORTERS;

EID: 77958142235     PISSN: 07357044     EISSN: 19390084     Source Type: Journal    
DOI: 10.1037/a0020774     Document Type: Article

References (67)

1. Akerman C.J., Cline H.T. Refining the roles of GABAergic signaling during neural circuit formation. Trends in Neurosciences 2007, 30:382-389.
2. Allen T.A., Narayanan N.S., Kholodar-Smith D.B., Zhao Y., Laubach M., Brown T.H. Imaging the spread of reversible brain inactivations using fluorescent muscimol. Journal of Neuroscience Methods 2008, 171:30-38.
3. Aton S.J., Seibt J., Dumoulin M., Jha S.K., Steinmetz N., Coleman T., Naidoo N., Frank M.G. Mechanisms of sleep-dependent consolidation of cortical plasticity. Neuron 2009, 61:454-466.
4. Ben-Ari Y. Excitatory actions of GABA during development: The nature of the nurture. Nature Reviews Neuroscience 2002, 3:728-739.
5. Blaesse P., Guillemin I., Schindler J., Schweizer M., Delpire E., Khiroug L., Friauf E., Nothwang H.G. Oligomerization of KCC2 correlates with development of inhibitory neurotransmission. Journal of Neuroscience 2006, 26:10407-10419.
6. Blakemore S.J., Wolpert D., Frith C. Why can't you tickle yourself?. Neuroreport 2000, 11:R11-16.
7. Bloom J.S., Hynd G.W. The role of the corpus callosum in interhemispheric transfer of information: Excitation or inhibition?. Neuropsychology Review 2005, 15:59-71.
8. Blumberg M.S., Lucas D.E. A developmental and component analysis of active sleep. Developmental Psychobiology 1996, 29:1-22.
9. Blumberg M.S., Seelke A.M. The form and function of infant sleep: From muscle to neocortex. The Oxford Handbook of Developmental Behavioral Neuroscience 2010, 391-423. Oxford University Press, New York. M.S. Blumberg, J.H. Freeman, S.R. Robinson (Eds.).
10. Campolattaro M.M., Freeman J.H. Eyeblink conditioning in 12-day-old rats using pontine stimulation as the conditioned stimulus. Proceedings of the National Academy of Sciences, USA of the United States of America 2008, 105:8120-8123.
11. Cobas A., Alvarez-Bolado G., Fairen A. Transient GABA-like immunoreactive axons in the corpus callosum of perinatal rats. Neuroscience Letters 1988, 93:7-12.
12. Corner M.A., Mirmiran M., Bour H.L., Boer G.J., van de Poll N.E., van Oyen H.G., Uylings H.B. Does rapid-eye-movement sleep play a role in brain development?. Progress in Brain Research 1980, 53:347-356.
13. Crair M.C. Neuronal activity during development: Permissive or instructive?. Current Opinion in Neurobiology 1999, 9:88-93.
14. Cullen K.E. Sensory signals during active versus passive movement. Current Opinion in Neurobiology 2004, 14:698-706.
15. Fabri M., Manzoni T. Glutamic acid decarboxylase immunoreactivity in callosal projecting neurons of cat and rat somatic sensory areas. Neuroscience 2004, 123:557-566.
16. Feldman D.E. Synaptic mechanisms for plasticity in neocortex. Annual Review of Neuroscience 2009, 32:33-55.
17. Feller M.B., Scanziani M. A precritical period for plasticity in visual cortex. Current Opinion in Neurobiology 2005, 15:94-100.
18. Gall A.J., Todd W.D., Ray B., Coleman C.M., Blumberg M.S. The development of day-night differences in sleep and wakefulness in Norway rats and the effect of bilateral enucleation. Journal of Biological Rhythms 2008, 23:232-241.
19. Ganguly K., Schinder A.F., Wong S.T., Poo M. GABA itself promotes the developmental switch of neuronal GABAergic responses from excitation to inhibition. Cell 2001, 105:521-532.
20. Gramsbergen A., Schwartze P., Prechtl H.F.R. The postnatal development of behavioral states in the rat. Developmental Psychobiology 1970, 3:267-280.
21. Hanganu I.L., Staiger J.F., Ben-Ari Y., Khazipov R. Cholinergic modulation of spindle bursts in the neonatal rat visual cortex in vivo. Journal of Neuroscience 2007, 27:5694-5705.
22. Hensch T.K. Critical period plasticity in local cortical circuits. Nature Reviews Neuroscience 2005, 6:877-888.
23. Innocenti G.M., Price D.J. Exuberance in the development of cortical networks. Nature Reviews Neuroscience 2005, 6:955-965.
24. Ivy G.O., Killackey H.P. The ontogeny of the distribution of callosal projection neurons in the rat parietal cortex. Journal of Comparative Neurology 1981, 195:367-389.
25. Jones M.S., Barth D.S. Effects of bicuculline methiodide on fast (>200 Hz) electrical oscillations in rat somatosensory cortex. Journal of Neurophysiology 2002, 88:1016-1025.
26. Juliano S.L., Ma W., Eslin D. Cholinergic depletion prevents expansion of topographic maps in somatosensory cortex. Proceedings of the National Academy of Sciences, USA of the United States of America 1991, 88:780-784.
27. Kanold P.O. Subplate neurons: Crucial regulators of cortical development and plasticity. Frontiers in Neuroanatomy 2009, 3:1-9.
28. Karlsson K.Æ., Blumberg M.S. The union of the state: Myoclonic twitching is coupled with nuchal muscle atonia in infant rats. Behavioral Neuroscience 2002, 116:912-917.
29. Karlsson K.Æ., Gall A.J., Mohns E.J., Seelke A.M.H., Blumberg M.S. The neural substrates of infant sleep in rats. PLoS Biology 2005, 3:891-901.
30. Karlsson K.Æ., Kreider J.C., Blumberg M.S. Hypothalamic contribution to sleep-wake cycle development. Neuroscience 2004, 123:575-582.
31. Katz L.C., Shatz C.J. Synaptic activity and the construction of cortical circuits. Science 1996, 274:1133-1138.
32. Khazipov R. GABA and early patterns in vivo, INMED Satellite Conference of SFN 2009, Chicago.
33. Khazipov R., Sirota A., Leinekugel X., Holmes G.L., Ben-Ari Y., Buzsaki G. Early motor activity drives spindle-bursts in the developing somatosensory cortex. Nature 2004, 432:758-761.
34. Kilgard M.P., Merzenich M.M. Cortical map reorganization enabled by nucleus basalis activity. Science 1998, 279:1714-1718.
35. Kimura F., Baughman R.W. GABAergic transcallosal neurons in developing rat neocortex. European Journal of Neuroscience 1997, 9:1137-1143.
36. Kolb B., Halliwell C., Gibb R. Factors influencing neocortical development in the normal and injured brain. The Oxford Handbook of Developmental Behavioral Neuroscience 2010, 375-388. Oxford University Press, New York. M.S. Blumberg, J.H. Freeman, S.R. Robinson (Eds.).
37. Kreider J.C., Blumberg M.S. Mesopontine contribution to the expression of active 'twitch' sleep in decerebrate week-old rats. Brain Research 2000, 872:149-159.
38. Lamsa K., Palva J.M., Ruusuvuori E., Kaila K., Taira T. Synaptic GABA(A) activation inhibits AMPA-kainate receptor-mediated bursting in the newborn (P0-P2) rat hippocampus. Journal of Neurophysiology 2000, 83:359-366.
39. Ludwig A., Li H., Saarma M., Kaila K., Rivera C. Developmental up-regulation of KCC2 in the absence of GABAergic and glutamatergic transmission. European Journal of Neuroscience 2003, 18:3199-3206.
40. Ma W., Hohmann C.F., Coyle J.T., Juliano S.L. Lesions of the basal forebrain alter stimulus-evoked metabolic activity in mouse somatosensory cortex. Journal of Comparative Neurology 1989, 288:414-427.
41. Makarov V.A., Schmidt K.E., Castellanos N.P., Lopez-Aguado L., Innocenti G.M. Stimulus-dependent interaction between the visual areas 17 and 18 of the 2 hemispheres of the ferret (Mustela putorius). Cerebral Cortex 2008, 18:1951-1960.
42. Marcano-Reik A.J., Blumberg M.S. The corpus callosum modulates spindle-burst activity within homotopic regions of somatosensory cortex in newborn rats. European Journal of Neuroscience 2008, 28:1457-1466.
43. Marmigere F., Rage F., Tapia-Arancibia L. GABA-glutamate interaction in the control of BDNF expression in hypothalamic neurons. Neurochemistry International 2003, 42:353-358.
44. Marty S., Berzaghi Mda P., Berninger B. Neurotrophins and activity-dependent plasticity of cortical interneurons. Trends in Neurosciences 1997, 20:198-202.
45. Minlebaev M., Ben-Ari Y., Khazipov R. Network mechanisms of spindle-burst oscillations in the neonatal rat barrel cortex in vivo. Journal of Neurophysiology 2007, 97:692-700.
46. Mizuno H., Hirano T., Tagawa Y. Evidence for activity-dependent cortical wiring: Formation of interhemispheric connections in neonatal mouse visual cortex requires projection neuron activity. Journal of Neuroscience 2007, 27:6760-6770.
47. Mohns E.J., Blumberg M.S. Synchronous bursts of neuronal activity in the developing hippocampus: Modulation by active sleep and association with emerging gamma and theta rhythms. Journal of Neuroscience 2008, 28:10134-10144.
48. Mohns E.J., Blumberg M.S. Neocortical activation of the hippocampus during sleep in newborn rats. Journal of Neuroscience 2010, 30:3438-3449.
49. Owens D.F., Boyce L.H., Davis M.B., Kriegstein A.R. Excitatory GABA responses in embryonic and neonatal cortical slices demonstrated by gramicidin perforated-patch recordings and calcium imaging. Journal of Neuroscience 1996, 16:6414-6423.
50. Owens D.F., Kriegstein A.R. Is there more to GABA than synaptic inhibition?. Nature Reviews Neuroscience 2002, 3:715-727.
51. Paul L.K., Brown W.S., Adolphs R., Tyszka J.M., Richards L.J., Mukherjee P., Sherr E.H. Agenesis of the corpus callosum: Genetic, developmental and functional aspects of connectivity. Nature Reviews Neuroscience 2007, 8:287-299.
52. Petersson P., Waldenström A., Fåhraeus C., Schouenborg J. Spontaneous muscle twitches during sleep guide spinal self-organization. Nature 2003, 424:72-75.
53. Rasmusson D.D., Dykes R.W. Long-term enhancement of evoked potentials in cat somatosensory cortex produced by co-activation of the basal forebrain and cutaneous receptors. Experimental Brain Research 1988, 70:276-286.
54. - cotransporter KCC2 and carbonic anhydrase CAVII. Journal of Physiology 2005, 562:27-36.
55. Roffwarg H.P., Muzio J.N., Dement W.C. Ontogenetic development of the human sleep-dream cycle. Science 1966, 152:604-619.
56. Seelke A.M., Blumberg M.S. Developmental appearance and disappearance of cortical events and oscillations in infant rats. Brain Research 2010, 1324:34-42.
57. Seelke A.M.H., Blumberg M.S. Thermal and nutritional modulation of sleep in infant rats. Behavioral Neuroscience 2005, 19:603-611.
58. Seelke A.M.H., Karlsson K.Æ., Gall A.J., Blumberg M.S. Extraocular muscle activity, rapid eye movements, and the development of active and quiet sleep. European Journal of Neuroscience 2005, 22:911-920.
59. Sipilä S.T., Blaesse P., Kaila K. Development of GABAergic signaling: From molecules to emerging networks. The Oxford Handbook of Developmental Behavioral Neuroscience 2010, 108-139. Oxford University Press, New York. M.S. Blumberg, J.H. Freeman, S.R. Robinson (Eds.).
60. Tremblay N., Warren R.A., Dykes R.W. Electrophysiological studies of acetylcholine and the role of the basal forebrain in the somatosensory cortex of the cat. II. Cortical neurons excited by somatic stimuli. Journal of Neurophysiology 1990, 64:1212-1222.
61. Turrigiano G.G. Homeostatic plasticity in neuronal networks: The more things change, the more they stay the same. Trends in Neurosciences 1999, 22:221-227.
62. Wang C., Shimizu-Okabe C., Watanabe K., Okabe A., Matsuzaki H., Ogawa T., Mori N., Fukuda A., Sato K. Developmental changes in KCC1, KCC2, and NKCC1 mRNA expressions in the rat brain. Developmental Brain Research 2002, 139:59-66.
63. Wang C.L., Zhang L., Zhou Y., Zhou J., Yang X.J., Duan S.M., Xiong Z.Q., Ding Y.Q. Activity-dependent development of callosal projections in the somatosensory cortex. Journal of Neuroscience 2007, 27:11334-11342.
64. Wise S.P., Jones E.G. The organization and postnatal development of the commissural projection of the rat somatic sensory cortex. Journal of Comparative Neurology 1976, 168:313-343.
65. Wong M., Yamada K.A. Developmental characteristics of epileptiform activity in immature rat neocortex: A comparison of four in vitro seizure models. Developmental Brain Research 2001, 128:113-120.
66. Wong R.O. Retinal waves and visual system development. Annual Review of Neuroscience 1999, 22:29-47.
67. Xiong H., Futamura T., Jourdi H., Zhou H., Takei N., Diverse-Pierluissi M., Plevy S., Nawa H. Neurotrophins induce BDNF expression through the glutamate receptor pathway in neocortical neurons. Neuropharmacology 2002, 42:903-912.