Cholinergic modulation of spindle bursts in the neonatal rat visual cortex in vivo

Journal of Neuroscience

Volumn 27, Issue 21, 2007, Pages 5694-5705

  Hanganu, Ileana L ^a,c   Staiger, Jochen F ^b   Ben Ari, Yehezkel ^a   Khazipov, Rustem ^a  

^a INSERM   (France)

^b UNIVERSITY OF FREIBURG   (Germany)

^c JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

192 IgG saporin; Basal forebrain; Development; In vivo; Muscarinic; Oscillations

Indexed keywords

ACETYLCHOLINESTERASE; ATROPINE; MUSCARINIC RECEPTOR; PHYSOSTIGMINE; CHOLINERGIC RECEPTOR BLOCKING AGENT; CHOLINERGIC RECEPTOR STIMULATING AGENT;

ARTICLE; BRAIN DEPTH STIMULATION; CHOLINERGIC ACTIVITY; CONTROLLED STUDY; FOREBRAIN; IN VIVO STUDY; NONHUMAN; OSCILLATION; PRIORITY JOURNAL; RAT; VISUAL CORTEX; ANIMAL; CHOLINERGIC NERVE; COMPARATIVE STUDY; DRUG EFFECT; GROWTH, DEVELOPMENT AND AGING; MALE; NEWBORN; PHYSIOLOGY; SYNAPTIC TRANSMISSION; VISUAL SYSTEM;

ANIMALS; ANIMALS, NEWBORN; CHOLINERGIC AGENTS; CHOLINERGIC AGONISTS; CHOLINERGIC ANTAGONISTS; CHOLINERGIC FIBERS; MALE; RATS; RECEPTORS, MUSCARINIC; SYNAPTIC TRANSMISSION; VISUAL CORTEX; VISUAL PATHWAYS;

EID: 34250639819     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5233-06.2007     Document Type: Article

References (81)

1. Arters J, Hohmann CF, Mills J, Olaghere O, Berger-Sweeney J (1998) Sexually dimorphic responses to neonatal basal forebrain lesions in mice: I. Behavior and neurochemistry. J Neurobiol 37:582-594.
2. Avignone E, Cherubini E (1999) Muscarinic receptor modulation of GABA-mediated giant depolarizing potentials in the neonatal rat hippocampus. J Physiol (Lond) 518:97-107.
3. Bao S, Chang EF, Davis JD, Gobeske KT, Merzenich MM (2003) Progressive degradation and subsequent refinement of acoustic representations in the adult auditory cortex. J Neurosci 23:10765-10775.
4. Baskerville KA, Schweitzer JP, Herron P (1997) Effects of cholinergic depletion on experience-dependent plasticity in the cortex of the rat. Neuroscience 80:1159-1169.
5. Bear MF, Singer W (1986) Modulation of visual cortical plasticity by acetylcholine and noradrenaline. Nature 320:172-176.
6. Bloom JS, Hynd GW (2005) The role of the corpus callosum in interhemispheric transfer of information: excitation or inhibition? Neuropsychol Rev 15:59-71.
7. Book AA, Wiley RG, Schweitzer JB (1992) Specificity of 192 IgG-saporin for NGF receptor-positive cholinergic basal forebrain neurons in the rat. Brain Res 590:350-355.
8. Brimijoin S, Koenigsberger C (1999) Cholinesterases in neural development: new findings and toxicologic implications. Environ Health Perspect 107 [Suppl 1]:59-64.
9. Byers DM, Irwin LN, Moss DE, Sumaya IC, Hohmann CF (2005) Prenatal exposure to the acetylcholinesterase inhibitor methanesulfonyl fluoride alters forebrain morphology and gene expression. Dev Brain Res 158:13-22.
10. Calarco CA, Robertson RT (1995) Development of basal forebrain projections to visual cortex: DiI studies in rat. J Comp Neurol 354:608-626.
11. Cang J, Renteria RC, Kaneko M, Liu X, Copenhagen DR, Stryker MP (2005) Development of precise maps in visual cortex requires patterned spontaneous activity in the retina. Neuron 48:797-809.
12. Damasio AR, Graff-Radford NR, Eslinger PJ, Damasio H, Kassell N (1985) Amnesia following basal forebrain lesions. Arch Neurol 42:263-271.
13. del Rio T, Feller MB (2006) Early retinal activity and visual circuit development. Neuron 52:221-222.
14. Dupont E, Hanganu IL, Kilb W, Hirsch S, Luhmann HJ (2006) Rapid developmental switch in the mechanisms driving early cortical columnar networks. Nature 439:79-83.
15. Everitt BJ, Robbins TW (1997) Central cholinergic systems and cognition. Annu Rev Psychol 48:649-684.
16. Gaykema RP, Luiten PG, Nyakas C, Traber J (1990) Cortical projection patterns of the medial septum-diagonal band complex. J Comp Neurol 293:103-124.
17. Gregory E (1975) Comparison of postnatal CNS development between male and female rats. Brain Res 99:152-156.
18. Greuel JM, Luhmann HJ, Singer W (1988) Pharmacological induction of use-dependent receptive field modifications in the visual cortex. Science 242:74-77.
19. Grundfest H, Nachmansohn D, Kao CY, Chambers R (1952) Mode of blocking of axonal activity by curare and inhibitors of acetylcholinesterase. Nature 169:190.
20. Gu Q (2002) Neuromodulatory transmitter systems in the cortex and their role in cortical plasticity. Neuroscience 111:815-835.
21. Gu Q, Singer W (1993) Effects of intracortical infusion of anticholinergic drugs on neuronal plasticity in kitten striate cortex. Eur J Neurosci 5:475-485.
22. Gu QA, Bear MF, Singer W (1989) Blockade of NMDA-receptors prevents ocularity changes in kitten visual cortex after reversed monocular deprivation. Dev Brain Res 47:281-288.
23. Hanganu IL, Luhmann HJ (2004) Functional nicotinic acetylcholine receptors on subplate neurons in neonatal rat somatosensory cortex. J Neurophysiol 92:189-198.
24. Hanganu IL, Ben Ari Y, Khazipov R (2006) Retinal waves trigger spindle bursts in the neonatal rat visual cortex. J Neurosci 26:6728-6736.
25. Hohmann CF (2003) A morphogenetic role for acetylcholine in mouse cerebral neocortex. Neurosci Biobehav Rev 27:351-363.
26. Hohmann CF, Coyle JT (1988) Long-term effects of basal forebrain lesions on cholinergic, noradrenergic and serotonergic markers in mouse neocortex. Brain Res Bull 21:13-20.
27. Holschneider DP, Waite JJ, Leuchter AF, Walton NY, Scremin OU (1999) Changes in electrocortical power and coherence in response to the selective cholinergic immunotoxin 192 IgG-saporin. Exp Brain Res 126:270-280.
28. Huberman AD, Speer CM, Chapman B (2006) Spontaneous retinal activity mediates development of ocular dominance columns and binocular receptive fields in V1. Neuron 52:255-269.
29. Innocenti GM (1995) Exuberant development of connections, and its possible permissive role in cortical evolution. Trends Neurosci 18(9):397-402.
30. Juliano SL, Ma W, Eslin D (1991) Cholinergic depletion prevents expansion of topographic maps in somatosensory cortex. Proc Natl Acad Sci USA 88:780-784.
31. Khazipov R, Sirota A, Leinekugel X, Holmes GL, Ben-Ari Y, Buzsáki G (2004) Early motor activity drives spindle bursts in the developing somatosensory cortex. Nature 432:758-761.
32. Kilb W, Luhmann HJ (2003) Carbachol-induced network oscillations in the intact cerebral cortex of the newborn rat. Cereb Cortex 13:409-421.
33. Kiss J, Patel AJ (1992) Development of the cholinergic fibres innervating the cerebral cortex of the rat. Int J Dev Neurosci 10:153-170.
34. Koh S, Loy R (1989) Localization and development of nerve growth factor-sensitive rat basal forebrain neurons and their afferent projections to hippocampus and neocortex. J Neurosci 9:2999-3018.
35. Koh S, Santos TC, Cole AJ (2005) Susceptibility to seizure-induced injury and acquired microencephaly following intraventricular injection of saporin-conjugated 192 IgG in developing rat brain. Exp Neurol 194:457-466.
36. Krnjevic K, Pumain R, Renaud L (1971) The mechanism of excitation by acetylcholine in the cerebral cortex. J Physiol (Lond) 215:247-268.
37. Kuczewski N, Aztiria E, Leanza G, Domenici L (2005) Selective cholinergic immunolesioning affects synaptic plasticity in developing visual cortex. Eur J Neurosci 21:1807-1814.
38. Latsari M, Dori I, Antonopoulos J, Chiotelli M, Dinopoulos A (2002) Noradrenergic innervation of the developing and mature visual and motor cortex of the rat brain: a light and electron microscopic immunocytochemical analysis. J Comp Neurol 445:145-158.
39. Leanza G, Nilsson OG, Nikkhah G, Wiley RG, Bjorklund A (1996) Effects of neonatal lesions of the basal forebrain cholinergic system by 192 immunoglobulin G-saporin: biochemical, behavioural and morphological characterization. Neuroscience 74:119-141.
40. Lee MG, Hassani OK, Alonso A, Jones BE (2005) Cholinergic basal forebrain neurons burst with theta during waking and paradoxical sleep. J Neurosci 25:4365-4369.
41. Leinekugel X, Khazipov R, Cannon R, Hirase H, Ben-Ari Y, Buzsaki G (2002) Correlated bursts of activity in the neonatal hippocampus in vivo. Science 296:2049-2052.
42. Lidov HG, Molliver ME (1982) An immunohistochemical study of serotonin neuron development in the rat: ascending pathways and terminal fields. Brain Res Bull 8:389-430.
43. Lipton SA, Kater SB (1989) Neurotransmitter regulation of neuronal outgrowth, plasticity and survival. Trends Neurosci 12:265-270.
44. Luhmann HJ, Khazipov R (2006) Early patterns of electrical activity in the developing cerebral cortex of humans and rodents. Trends Neurosci 29:414-418.
45. Ma X, Suga N (2005) Long-term cortical plasticity evoked by electric stimulation and acetylcholine applied to the auditory cortex. Proc Natl Acad Sci USA 102:9335-9340.
46. Maggi L, Le Magueresse C, Changeux JP, Cherubini E (2003) Nicotine activates immature "silent" connections in the developing hippocampus. Proc Natl Acad Sci USA 100:2059-2064.
47. McCormick DA, Prince DA (1985) Two types of muscarinic response to acetylcholine in mammalian cortical neurons. Proc Natl Acad Sci USA 82:6344-6348.
48. McGaughy J, Koene RA, Eichenbaum H, Hasselmo ME (2005) Cholinergic deafferentation of the entorhinal cortex in rats impairs encoding of novel but not familiar stimuli in a delayed nonmatch-to-sample task. J Neurosci 25:10273-10281.
49. Meinecke DL, Rakic P (1993) Low-affinity p75 nerve growth factor receptor expression in the embryonic monkey telencephalon: timing and localization in diverse cellular elements. Neuroscience 54:105-116.
50. Mesulam MM, Mufson EJ, Wainer BH, Levey AI (1983) Central cholinergic pathways in the rat: an overview based on an alternative nomenclature (Ch1-Ch6). Neuroscience 10:1185-1201.
51. Mesulam MM, Hersh LB, Mash DC, Geula C (1992) Differential cholinergic innervation within functional subdivisions of the human cerebral cortex: a choline acetyltransferase study. J Comp Neurol 318:316-328.
52. Metherate R, Ashe JH (1991) Basal forebrain stimulation modifies auditory cortex responsiveness by an action at muscarinic receptors. Brain Res 559:163-167.
53. Metherate R, Cox CL, Ashe JH (1992) Cellular bases of neocortical activation: modulation of neural oscillations by the nucleus basalis and endogenous acetylcholine. J Neurosci 12:4701-4711.
54. Mooney R, Penn AA, Gallego R, Shatz CJ (1996) Thalamic relay of spontaneous retinal activity prior to vision. Neuron 17:863-874.
55. Moruzzi G, Magoun W (1949) Brain stem reticular formation and activation of the EEG. Electroencephalogr Clin Neurophysiol 1:455-473.
56. Moruzzi G, Magoun HW (1995) Brain stem reticular formation and activation of the EEG. 1949. J Neuropsychiatry Clin Neurosci 7:251-267.
57. Munoz-Cueto JA, Garcia-Segura LM, Ruiz-Marcos A (1991) Regional sex differences in spine density along the apical shaft of visual cortex pyramids during postnatal development. Brain Res 540:41-47.
58. Myers CP, Lewcock JW, Hanson MG, Gosgnach S, Aimone JB, Gage FH, Lee KF, Landmesser LT, Pfaff SL (2005) Cholinergic input is required during embryonic development to mediate proper assembly of spinal locomotor circuits. Neuron 46:37-49.
59. Pappas BA, Sherren N (2003) Neonatal 192 IgG-saporin lesion of forebrain cholinergic neurons: focus on the life span? Neurosci Biobehav Rev 27:365-376.
60. Pappas BA, Davidson CM, Fortin T, Nallathamby S, Park GA, Mohr E, Wiley RG (1996) 192 IgG-saporin lesion of basal forebrain cholinergic neurons in neonatal rats. Brain Res Dev Brain Res 96:52-61.
61. Pappas BA, Payne KB, Fortin T, Sherren N (2005) Neonatal lesion of forebrain cholinergic neurons: further characterization of behavioral effects and permanency. Neuroscience 133:485-492.
62. Paxinos G, Watson CR, Emson PC (1980) AChE-stained horizontal sections of the rat brain in stereotaxic coordinates. J Neurosci Methods 3:129-149.
63. Paxinos G, Törk I, Tecott LH, Valentino KL (1991) Atlas of the developing rat brain. San Diego: Academic.
64. Peinado A (2000) Traveling slow waves of neural activity: a novel form of network activity in developing neocortex. J Neurosci 20:RC54.
65. Pugh PC, Margiotta JF (2000) Nicotinic acetylcholine receptor agonists promote survival and reduce apoptosis of chick ciliary ganglion neurons. Mol Cell Neurosci 15:113-122.
66. Rasmusson DD, Clow K, Szerb JC (1994) Modification of neocortical acetylcholine release and electroencephalogram desynchronization due to brainstem stimulation by drugs applied to the basal forebrain. Neuroscience 60:665-677.
67. Robertson RT, Gallardo KA, Claytor KJ, Ha DH, Ku KH, Yu BP, Lauterborn JC, Wiley RG, Yu J, Gall CM, Leslie FM (1998) Neonatal treatment with 192 IgG-saporin produces long-term forebrain cholinergic deficits and reduces dendritic branching and spine density of neocortical pyramidal neurons. Cereb Cortex 8:142-155.
68. Rodriguez R, Kallenbach U, Singer W, Munk MH (2004) Short- and long-term effects of cholinergic modulation on gamma oscillations and response synchronization in the visual cortex. J Neurosci 24:10369-10378.
69. 3 receptors in developing visual cortex. J Neurosci 17:8353-8362.
70. Role LW, Berg DK (1996) Nicotinic receptors in the development and modulation of CNS synapses. Neuron 16:1077-1085.
71. Schafer MK, Weihe E, Erickson JD, Eiden LE (1995) Human and monkey cholinergic neurons visualized in paraffin-embedded tissues by immunoreactivity for VAChT, the vesicular acetylcholine transporter. J Mol Neurosci 6:225-235.
72. Semba K, Fibiger HC (1989) Organization of central cholinergic systems. Prog Brain Res 79:37-63.
73. Siciliano R, Fontanesi G, Casamenti F, Berardi N, Bagnoli P, Domenici L (1997) Postnatal development of functional properties of visual cortical cells in rats with excitotoxic lesions of basal forebrain cholinergic neurons. Vis Neurosci 14:111-123.
74. Singer W (1986) The brain as a self-organizing system. Eur Arch Psychiatry Neurol Sci 236:4-9.
75. Staiger JF, Masanneck C, Schleicher A, Zuschratter W (2004) Calbindin-containing interneurons are a target for VIP-immunoreactive synapses in rat primary somatosensory cortex. J Comp Neurol 468:179-189.
76. Steriade M, Dossi RC, Paré D, Oakson G (1991) Fast oscillations (20-40 Hz) in thalamocortical systems and their potentiation by mesopontine cholinergic nuclei in the cat. Proc Natl Acad Sci USA 88:4396-4400.
77. Weihe E, Tao-Cheng JH, Schafer MK, Erickson JD, Eiden LE (1996) Visualization of the vesicular acetylcholine transporter in cholinergic nerve terminals and its targeting to a specific population of small synaptic vesicles. Proc Natl Acad Sci USA 93:3547-3552.
78. Wenk GL, Stoehr JD, Quintana G, Mobley S, Wiley RG (1994) Behavioral, biochemical, histological, and electrophysiological effects of 192 IgG-saporin injections into the basal forebrain of rats. J Neurosci 14:5986-5995.
79. Wiley RG, Oeltmann TN, Lappi DA (1991) Immunolesioning: selective destruction of neurons using immunotoxin to rat NGF receptor. Brain Res 562:149-153.
80. Zhang Y, Dyck RH, Hamilton SE, Nathanson NM, Yan J (2005) Disrupted tonotopy of the auditory cortex in mice lacking M1 muscarinic acetylcholine receptor. Hear Res 201:145-155.
81. Zhu XO, Waite PM (1998) Cholinergic depletion reduces plasticity of barrel field cortex. Cereb Cortex 8:63-72.