Cholinergic Modulation of Spindle Bursts in the Neonatal Rat Visual Cortex In Vivo
Open accessAbstract
Acetylcholine (ACh) is known to shape the adult neocortical activity related to behavioral states and processing of sensory information. However, the impact of cholinergic input on the neonatal neuronal activity remains widely unknown. Early during development, the principal activity pattern in the primary visual (V1) cortex is the intermittent self-organized spindle burst oscillation that can be driven by the retinal waves. Here, we assessed the relationship between this early activity pattern and the cholinergic drive by either blocking or augmenting the cholinergic input and investigating the resultant effects on the activity of the rat visual cortex during the first postnatal week in vivo. Blockade of the muscarinic receptors by intracerebroventricular, intracortical, or supracortical atropine application decreased the occurrence of V1 spindle bursts by 50%, both the retina-independent and the optic nerve-mediated spindle bursts being affected. In contrast, blockade of acetylcholine esterase with physostigmine augmented the occurrence, amplitude, and duration of V1 spindle bursts. Whereas direct stimulation of the cholinergic basal forebrain nuclei increased the occurrence probability of V1 spindle bursts, their chronic immunotoxic lesion using 192 IgG-saporin decreased the occurrence of neonatal V1 oscillatory activity by 87%. Thus, the cholinergic input facilitates the neonatal V1 spindle bursts and may prime the developing cortex to operate specifically on relevant early (retinal waves) and later (visual input) stimuli.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Around birth, the numerous cholinergic projections arising from the basal forebrain nuclei innervate the primary cortical regions where they influence cortical ultrastructure.
“Around birth, the numerous cholinergic projections arising from the basal forebrain nuclei innervate the primary cortical regions where they influence cortical ultrastructure [210–213].”
From Development of prefrontal cortex (2022) · cites this paper as [213]
The Introduction describes abundant cholinergic afferents originating mainly in the basal forebrain and links cholinergic input to cortical development. The section on basal forebrain stimulation says these axons begin growing into cortical layers by birth. The paper discusses morphogenesis and circuit wiring, but does not establish an effect on cortical ultrastructure specifically. (LLM, conf=0.84)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
AChE-stained horizontal sections of the rat brain in stereotaxic coordinates
Paxinos, G., WATSON, C. R. R., & Emson, P. C. (1980) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(80)90021-7 · Cited by 4,497 · see citing works
Brain stem reticular formation and activation of the EEG
Moruzzi, G., & Magoun, H. W. (1949) · Electroencephalography and Clinical Neurophysiology · doi:10.1016/0013-4694(49)90219-9 · Cited by 4,307 · see citing works
Central cholinergic pathways in the rat: An overview based on an alternative nomenclature (Ch1–Ch6)
Mesulam, M. M., Mufson, E. J., Wainer, B. H., & Levey, A. I. (1983) · Neuroscience · doi:10.1016/0306-4522(83)90108-2 · Cited by 2,329 · see citing works
CENTRAL CHOLINERGIC SYSTEMS AND COGNITION
Everitt, B. J., & Robbins, T. W. (1997) · Annual Review of Psychology · doi:10.1146/annurev.psych.48.1.649 · Cited by 1,348 · see citing works
Hippocampal synaptic transmission enhanced by low concentrations of nicotine
Gray, R. G. F., Rajan, A. S., Radcliffe, K. A., Yakehiro, M., & Dani, J. A. (1996) · Nature · doi:10.1038/383713a0 · Cited by 947 · see citing works
Flores, C. M., Rogers, S. W., Pabreza, L. A., Wolfe, B. B., & Kellar, K. J. (1992) · Molecular Pharmacology · doi:10.1016/s0026-895x(25)08832-7 · Cited by 880 · see citing works
Zhou, Z., Hong, E. J., Cohen, S., Zhao, W.-N., Ho, H.-Y. H., Schmidt, L., Chen, W. G., Lin, Y., Savner, E., Griffith, E. C., et al. (2006) · Neuron · doi:10.1016/j.neuron.2006.09.037 · Cited by 877 · see citing works
Modulation of visual cortical plasticity by acetylcholine and noradrenaline
Bear, M. F., & Singer, W. (1986) · Nature · doi:10.1038/320172a0 · Cited by 858 · see citing works
Stuart, G. J., Dodt, H., & Sakmann, B. J. (1993) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/bf00374949 · Cited by 804 · see citing works
Hilmas, C., Pereira, E., Alkondon, M., Rassoulpour, A., Schwarcz, R., & Albuquerque, E. X. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-19-07463.2001 · Cited by 772 · see citing works
Nicotine activates and desensitizes midbrain dopamine neurons
Pidoplichko, V. I., DeBiasi, M., Williams, J. T., & Dani, J. A. (1997) · Nature · doi:10.1038/37120 · Cited by 769 · see citing works
Acetylcholine in mind: a neurotransmitter correlate of consciousness?
Perry, E. K., Walker, M. P., Grace, J., & Perry, R. H. (1999) · Trends in Neurosciences · doi:10.1016/s0166-2236(98)01361-7 · Cited by 764 · see citing works
Nicotinic Receptors in the Development and Modulation of CNS Synapses
Role, L. W., & Berg, D. K. (1996) · Neuron · doi:10.1016/s0896-6273(00)80134-8 · Cited by 762 · see citing works
Prenatal development of the visual system in rhesus monkey
RAKIC, P. T., Barlow, H. B., & Gaze, R. M. (1977) · Philosophical transactions of the Royal Society of London. Series B, Biological sciences · doi:10.1098/rstb.1977.0040 · Cited by 737 · see citing works
Neurotransmitter regulation of neuronal outgrowth, plasticity and survival
Lipton, S. A., & Kater, S. B. (1989) · Trends in Neurosciences · doi:10.1016/0166-2236(89)90026-x · Cited by 724 · see citing works
The mechanism of excitation by acetylcholine in the cerebral cortex
Krnjević, K., Pumain, R., & Renaud, L. P. (1971) · The Journal of Physiology · doi:10.1113/jphysiol.1971.sp009467 · Cited by 708 · see citing works
Fetal Nicotine or Cocaine Exposure: Which One is Worse?
Slotkin, T. A. (1998) · The Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(24)37495-6 · Cited by 676 · see citing works
Nicotinic acetylcholine involvement in cognitive function in animals
Levin, E. D., & Simon, B. B. (1998) · Psychopharmacology · doi:10.1007/s002130050667 · Cited by 675 · see citing works
Subplate Neurons Pioneer the First Axon Pathway from the Cerebral Cortex
McConnell, S. K., Ghosh, A., & Shatz, C. J. (1989) · Science · doi:10.1126/science.2475909 · Cited by 647 · see citing works
Early motor activity drives spindle bursts in the developing somatosensory cortex
Khazipov, R., Sirota, A., Leinekugel, X., Holmes, G. L., Ben‐Ari, Y., & Buzsáki, G. (2004) · Nature · doi:10.1038/nature03132 · Cited by 634 · see citing works
Self-citationBloom, J. S., & Hynd, G. W. (2005) · Neuropsychology Review · doi:10.1007/s11065-005-6252-y · Cited by 591 · see citing works
Tight-Seal Whole-Cell Recording
Marty, A., & Neher, E. (1983) · Springer eBooks · doi:10.1007/978-1-4615-7858-1_7 · Cited by 585 · see citing works
The maternal and fetal physiologic effects of nicotine
Lambers, D. S., & Clark, K. E. (1996) · Seminars in Perinatology · doi:10.1016/s0146-0005(96)80079-6 · Cited by 577 · see citing works
Metherate, R., Cox, C. L., & Ashe, J. H. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-12-04701.1992 · Cited by 575 · see citing works
Hamani, C., Aziz, T. Z., Bloem, B. R., Brown, P., Chabardès, S., Coyne, T. J., Foote, K. D., García‐Rill, E., Hirsch, É. C., Lozano, A. M., et al. (2016) · Stereotactic and Functional Neurosurgery · doi:10.1159/000449010 · Cited by 571 · see citing works
Alkondon, M., & Albuquerque, E. X. (1993) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)38283-2 · Cited by 554 · see citing works
Differential regulation of neocortical synapses by neuromodulators and activity
Gil, Z., Connors, B. W., & Amitai, Y. (1997) · Neuron · doi:10.1016/s0896-6273(00)80380-3 · Cited by 553 · see citing works
Romijn, H. J., Hofman, M. A., & Gramsbergen, A. (1991) · Early Human Development · doi:10.1016/0378-3782(91)90044-4 · Cited by 553 · see citing works
Lukas, R. J., Changeux, J., Novère, N. G. L., Albuquerque, E. X., Balfour, D. J. K., Berg, D. K., Bertrand, D., Chiappinelli, V. A., Clarke, P. B. S., Collins, A. C., et al. (1999) · Pharmacological Reviews · doi:10.1016/s0031-6997(24)01406-6 · Cited by 536 · see citing works
Neuromodulatory transmitter systems in the cortex and their role in cortical plasticity
Gu, Q. (2002) · Neuroscience · doi:10.1016/s0306-4522(02)00026-x · Cited by 518 · see citing works
Kostović, I., & RAKIC, P. T. (1980) · Journal of Neurocytology · doi:10.1007/bf01205159 · Cited by 499 · see citing works
Lidov, H. G. W., & Molliver, M. E. (1982) · Brain Research Bulletin · doi:10.1016/0361-9230(82)90077-6 · Cited by 483 · see citing works
Early patterns of electrical activity in the developing cerebral cortex of humans and rodents
Khazipov, R., & Luhmann, H. J. (2006) · Trends in Neurosciences · doi:10.1016/j.tins.2006.05.007 · Cited by 482 · see citing works
Self-citationAmnesia Following Basal Forebrain Lesions
Damásio, A. R., Graff‐Radford, N. R., Eslinger, P. J., Damasio, H., & Kassell, N. F. (1985) · Archives of Neurology · doi:10.1001/archneur.1985.04060030081013 · Cited by 475 · see citing works
Steriade, M., Dossi, R. C., Paré, D., & Oakson, G. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.10.4396 · Cited by 455 · see citing works
Nicotinic receptors in the brain: correlating physiology with function
Jones, S., Sudweeks, S. N., & Yakel, J. L. (1999) · Trends in Neurosciences · doi:10.1016/s0166-2236(99)01471-x · Cited by 447 · see citing works
Cholinergic Basal Forebrain Neurons Burst with Theta during Waking and Paradoxical Sleep
Lee, M., Hassani, O. K., Alonso, Á., & Jones, B. E. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.0178-05.2005 · Cited by 439 · see citing works
Immunolesioning: selective destruction of neurons using immunotoxin to rat NGF receptor
Wiley, R. G., Oeltmann, T. N., & Lappi, D. A. (1991) · Brain Research · doi:10.1016/0006-8993(91)91199-b · Cited by 417 · see citing works
Le Novère, N., Corringer, P., & Changeux, J. (2002) · Journal of Neurobiology · doi:10.1002/neu.10153 · Cited by 411 · see citing works
Functional contributions of α5 subunit to neuronal acetylcholine receptor channels
Ramírez-Latorre, J. A., Yu, C., Qu, X., Perin, F., Karlin, A., & Role, L. W. (1996) · Nature · doi:10.1038/380347a0 · Cited by 397 · see citing works
Cortical projection patterns of the medial septum‐diagonal band complex
Gaykema, R. P. A., Luiten, P. G. M., Nyakas, C. J., & Traber, J. (1990) · The Journal of Comparative Neurology · doi:10.1002/cne.902930109 · Cited by 387 · see citing works
Frazier, C. J., Rollins, Y. D., Breese, C. R., Leonard, S., Freedman, R., & Dunwiddie, T. V. (1998) · The Journal of Neuroscience · doi:10.1523/jneurosci.18-04-01187.1998 · Cited by 374 · see citing works
Higher levels of nicotine in arterial than in venous blood after cigarette smoking
Henningfield, J. E. (1993) · Drug and Alcohol Dependence · doi:10.1016/0376-8716(93)90030-t · Cited by 370 · see citing works
Correlated Bursts of Activity in the Neonatal Hippocampus in Vivo
Leinekugel, X., Khazipov, R., Cannon, R., Hirase, H., Ben-Ari, Y., & Buzsáki, G. (2002) · Science · doi:10.1126/science.1071111 · Cited by 362 · see citing works
Self-citationChronic Exposure to Nicotine Upregulates the Human α4β2 Nicotinic Acetylcholine Receptor Function
Buisson, B., & Bertrand, D. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-06-01819.2001 · Cited by 361 · see citing works
Atlas Of The Developing Rat Brain
Paxinos, G., & Fritchle, A. L. R. (1991) · Medical Entomology and Zoology · Cited by 345 · see citing works
Zoli, M., Novère, N. G. L., Hill, J. A., & Changeux, J. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-03-01912.1995 · Cited by 338 · see citing works
Alkondon, M., Pereira, E. F. R., Eisenberg, H. M., & Albuquerque, E. X. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-07-02693.1999 · Cited by 332 · see citing works
Rapid developmental switch in the mechanisms driving early cortical columnar networks
Dupont, E., Hanganu, I. L., Kilb, W., Hirsch, S., & Luhmann, H. J. (2006) · Nature · doi:10.1038/nature04264 · Cited by 324 · see citing works
Self-citationDevelopment of precise maps in visual cortex requires patterned spontaneous activity in the retina
Cang, J., Rentería, R. C., Kaneko, M., Liu, X., Copenhagen, D. R., & Stryker, M. P. (2005) · Neuron · doi:10.1016/j.neuron.2005.09.015 · Cited by 306 · see citing works
Two types of muscarinic response to acetylcholine in mammalian cortical neurons.
McCormick, D. A., & Prince, D. A. (1985) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.82.18.6344 · Cited by 302 · see citing works
Weihe, E., Tao-Cheng, J.-H., Schäfer, M., Erickson, J. D., & Eiden, L. E. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.8.3547 · Cited by 301 · see citing works
Visualizing unstained neurons in living brain slices by infrared DIC-videomicroscopy
Dodt, H., & Zieglgänsberger, W. (1990) · Brain Research · doi:10.1016/0006-8993(90)90380-t · Cited by 291 · see citing works
Brain stem reticular formation and activation of the EEG
Moruzzi, G. (1949) · Electroencephalography and Clinical Neurophysiology · doi:10.1016/0013-4694(49)90066-8 · Cited by 291 · see citing works
Role of Subplate Neurons in Functional Maturation of Visual Cortical Columns
Kanold, P. O., Kara, P., Reid, R. C., & Shatz, C. J. (2003) · Science · doi:10.1126/science.1084152 · Cited by 288 · see citing works
Retinal Waves Trigger Spindle Bursts in the Neonatal Rat Visual Cortex
Hanganu, I. L., Ben‐Ari, Y., & Khazipov, R. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.0752-06.2006 · Cited by 288 · see citing works
Self-citationFriauf, E., McConnell, S. K., & Shatz, C. J. (1990) · Journal of Neuroscience · doi:10.1523/jneurosci.10-08-02601.1990 · Cited by 278 · see citing works
Pharmacological Induction of Use-Dependent Receptive Field Modifications in the Visual Cortex
Greuel, J. M., Luhmann, H. J., & Singer, W. (1988) · Science · doi:10.1126/science.2902687 · Cited by 276 · see citing works
Nicotinic Stimulation Produces Multiple Forms of Increased Glutamatergic Synaptic Transmission
Radcliffe, K. A., & Dani, J. A. (1998) · The Journal of Neuroscience · doi:10.1523/jneurosci.18-18-07075.1998 · Cited by 271 · see citing works
Wenk, G. L., Stoehr, J. D., Quintana, G., Mobley, S., & Wiley, R. G. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-10-05986.1994 · Cited by 252 · see citing works
Involvement of Subplate Neurons in the Formation of Ocular Dominance Columns
Ghosh, A., & Shatz, C. J. (1992) · Science · doi:10.1126/science.1542795 · Cited by 249 · see citing works
Rodriguez, R., Kallenbach, U., Singer, W., & Munk, M. H. J. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.1839-04.2004 · Cited by 246 · see citing works
Pathfinding and target selection by developing geniculocortical axons
Ghosh, A., & Shatz, C. J. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-01-00039.1992 · Cited by 224 · see citing works
Thalamic Relay of Spontaneous Retinal Activity Prior to Vision
MOONEY, R. D., Penn, A. A., Gallego, R., & Shatz, C. J. (1996) · Neuron · doi:10.1016/s0896-6273(00)80218-4 · Cited by 218 · see citing works
Palma, E., Bertrand, S., Binzoni, T., & Bertrand, D. (1996) · The Journal of Physiology · doi:10.1113/jphysiol.1996.sp021203 · Cited by 218 · see citing works
Increased neurodegeneration during ageing in mice lacking high‐affinity nicotine receptors
Zoli, M., Picciotto, M. R., Ferrari, R., Cocchi, D., & Changeux, J. (1999) · The EMBO Journal · doi:10.1093/emboj/18.5.1235 · Cited by 206 · see citing works
Roerig, B., Nelson, D. A., & Katz, L. C. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-21-08353.1997 · Cited by 192 · see citing works
Mesulam, M. ‐., Hersh, L. B., Mash, D. C., & Geula, C. (1992) · Journal of Comparative Neurology · doi:10.1002/cne.903180308 · Cited by 188 · see citing works
Aramakis, V. B., & Metherate, R. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-20-08485.1998 · Cited by 182 · see citing works
Cholinergic depletion prevents expansion of topographic maps in somatosensory cortex.
Juliano, S. L., Ma, W., & Eslin, D. E. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.3.780 · Cited by 171 · see citing works
Exuberant development of connections, and its possible permissive role in cortical evolution
Innocenti, G. M. (1995) · Trends in Neurosciences · doi:10.1016/0166-2236(95)93936-r · Cited by 168 · see citing works
Cholinergic regulation of cortical development and plasticity. New twists to an old story.
Cf, H., & Berger-Sweeney, J. E. (1998) · PubMed · Cited by 165 · see citing works
Chapter 4 Organization of central cholinergic systems
Semba, K., & Fibiger, H. C. (1989) · Progress in brain research · doi:10.1016/s0079-6123(08)62464-4 · Cited by 160 · see citing works
Myers, C. P., Lewcock, J. W., Hanson, M. G., Gosgnach, S., Aimone, J. B., Gage, F. H., Lee, K., Landmesser, L. T., & Pfaff, S. L. (2005) · Neuron · doi:10.1016/j.neuron.2005.02.022 · Cited by 160 · see citing works
Functional Synaptic Projections onto Subplate Neurons in Neonatal Rat Somatosensory Cortex
Hanganu, I. L., Kilb, W., & Luhmann, H. J. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-16-07165.2002 · Cited by 159 · see citing works
Self-citationBertrand, D., Ballivet, M., & Rungger, D. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.5.1993 · Cited by 158 · see citing works
Rasmusson, D. D., Clow, K. A., & Szerb, J. C. (1994) · Neuroscience · doi:10.1016/0306-4522(94)90495-2 · Cited by 156 · see citing works
Kostović, I. (1986) · Neuroscience · doi:10.1016/0306-4522(86)90077-1 · Cited by 153 · see citing works
Cholinergic modulation of excitatory synaptic transmission in the CA3 area of the hippocampus
Vogt, K. E., & Regehr, W. G. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-01-00075.2001 · Cited by 149 · see citing works
Koh, S., & Loy, R. (1989) · Journal of Neuroscience · doi:10.1523/jneurosci.09-09-02999.1989 · Cited by 147 · see citing works
Book, A. A., Wiley, R. G., & Schweitzer, J. B. (1992) · Brain Research · doi:10.1016/0006-8993(92)91121-t · Cited by 145 · see citing works
Metherate, R., & Ashe, J. H. (1991) · Brain Research · doi:10.1016/0006-8993(91)90301-b · Cited by 145 · see citing works
Gu, Q., Bear, M. F., & Singer, W. (1989) · Developmental Brain Research · doi:10.1016/0165-3806(89)90183-1 · Cited by 144 · see citing works
Cholinergic mechanisms in the rat somatosensory cerebral cortex
Stone, T. W. (1972) · The Journal of Physiology · doi:10.1113/jphysiol.1972.sp009951 · Cited by 139 · see citing works
Gu, Q., & Singer, W. (1993) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1993.tb00514.x · Cited by 137 · see citing works
Margiotta, J. F., Berg, D. K., & Dionne, V. E. (1987) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.84.22.8155 · Cited by 130 · see citing works
Broide, R. S., O’Connor, L. T., Smith, M. A., Smith, J. A., & Leslie, F. M. (1995) · Neuroscience · doi:10.1016/0306-4522(94)00623-d · Cited by 129 · see citing works
Huberman, A. D., Speer, C. M., & Chapman, B. (2006) · Neuron · doi:10.1016/j.neuron.2006.07.028 · Cited by 125 · see citing works
Broide, R. S., Robertson, R. T., & Leslie, F. M. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-09-02956.1996 · Cited by 123 · see citing works
A critical period for nicotine-induced disruption of synaptic development in rat auditory cortex
Aramakis, V. B., Hsieh, C. Y., Leslie, F. M., & Metherate, R. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-16-06106.2000 · Cited by 120 · see citing works
Effects of cholinergic depletion on experience-dependent plasticity in the cortex of the rat
Baskerville, K. A., Schweitzer, J. B., & Herron, P. (1997) · Neuroscience · doi:10.1016/s0306-4522(97)00064-x · Cited by 120 · see citing works
Mathie, A. A., Colquhoun, D. M., & Cull-Candy, S. G. (1990) · The Journal of Physiology · doi:10.1113/jphysiol.1990.sp018191 · Cited by 119 · see citing works
Brain stem reticular formation and activation of the EEG. 1949 [classical article]
Moruzzi, G., & Magoun, H. W. (1995) · Journal of Neuropsychiatry · doi:10.1176/jnp.7.2.251 · Cited by 117 · see citing works
A transmembrane motif governs the surface trafficking of nicotinic acetylcholine receptors
Wang, J.-M., Zhang, L., Yao, Y., Viroonchatapan, N., Rothe, E. E., & Wang, Z.-Z. (2002) · Nature Neuroscience · doi:10.1038/nn918 · Cited by 116 · see citing works
Naeff, B., Schlumpf, M., & LICHTENSTEIGER, W. (1992) · Developmental Brain Research · doi:10.1016/0165-3806(92)90058-5 · Cited by 115 · see citing works
Atluri, P., Fleck, M. W., Shen, Q., Mah, S. J., Stadfelt, D., Barnes, W., Goderie, S. K., Temple, S., & Schneider, A. S. (2001) · Developmental Biology · doi:10.1006/dbio.2001.0453 · Cited by 110 · see citing works
Conroy, W. G., & Berg, D. K. (1998) · Molecular Pharmacology · doi:10.1124/mol.53.3.392 · Cited by 110 · see citing works
Nicotine activates immature “silent” connections in the developing hippocampus
Maggi, L., Magueresse, C. L., Changeux, J., & Cherubini, E. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0437947100 · Cited by 109 · see citing works
Surface and intracellular distribution of a putative neuronal nicotinic acetylcholine receptor.
Jacob, M. H., Lindstrom, J., & Berg, D. K. (1986) · The Journal of Cell Biology · doi:10.1083/jcb.103.1.205 · Cited by 106 · see citing works
Dual Fate of Subplate Neurons in a Rodent
Woo, T., Beale, J. M., & Finlay, B. L. (1991) · Cerebral Cortex · doi:10.1093/cercor/1.5.433 · Cited by 105 · see citing works
The role of nAChR‐mediated spontaneous retinal activity in visual system development
Feller, M. B. (2002) · Journal of Neurobiology · doi:10.1002/neu.10140 · Cited by 104 · see citing works
McGaughy, J. A., Koene, R. A., Eichenbaum, H., & Hasselmo, M. E. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.2386-05.2005 · Cited by 103 · see citing works
Laudenbach, V., Medja, F., Zoli, M., Rossi, F., Evrard, P., Changeux, J., & Gressèns, P. (2002) · The FASEB Journal · doi:10.1096/fj.01-0532fje · Cited by 103 · see citing works
Cholinesterases in neural development: new findings and toxicologic implications.
Brimijoin, S., & Koenigsberger, C. (1999) · Environmental Health Perspectives · doi:10.1289/ehp.99107s159 · Cited by 99 · see citing works
Benowitz, N. L., Porchet, H. C., & Jacob, P. (1989) · Progress in brain research · doi:10.1016/s0079-6123(08)62487-5 · Cited by 98 · see citing works
Bao, S., Chang, E. F., Davis, J. D., Gobeske, K. T., & Merzenich, M. M. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-34-10765.2003 · Cited by 96 · see citing works
Kostović, I., Lukinović, N., Judáš, M., Bogdanović, N., Mrzljak, L., Zečević, N., & Kubat, M. (1989) · Metabolic Brain Disease · doi:10.1007/bf00999489 · Cited by 95 · see citing works
The brain as a self-organizing system
Singer, W. (1986) · European Archives of Psychiatry and Clinical Neuroscience · doi:10.1007/bf00641050 · Cited by 92 · see citing works
Mechawar, N., & Descarries, L. (2001) · Neuroscience · doi:10.1016/s0306-4522(01)00389-x · Cited by 91 · see citing works
Mienville, J., & Pesold, C. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-05-01636.1999 · Cited by 87 · see citing works
Spontaneous Synaptic Activity of Subplate Neurons in Neonatal Rat Somatosensory Cortex
Hanganu, I. L. (2001) · Cerebral Cortex · doi:10.1093/cercor/11.5.400 · Cited by 84 · see citing works
Self-citationRobertson, R. (1998) · Cerebral Cortex · doi:10.1093/cercor/8.2.142 · Cited by 81 · see citing works
A morphogenetic role for acetylcholine in mouse cerebral neocortex
Höhmann, C. F. (2003) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(03)00066-6 · Cited by 80 · see citing works
Schäfer, M. K.-H., Weihe, E., Erickson, J. D., & Eiden, L. E. (1995) · Journal of Molecular Neuroscience · doi:10.1007/bf02736782 · Cited by 79 · see citing works
Cholinergic depletion reduces plasticity of barrel field cortex
Zhu, X. (1998) · Cerebral Cortex · doi:10.1093/cercor/8.1.63 · Cited by 77 · see citing works
Pugh, P. C., & Margiotta, J. F. (2000) · Molecular and Cellular Neuroscience · doi:10.1006/mcne.1999.0810 · Cited by 73 · see citing works
Leanza, G., Nilsson, O., Nikkhah, G., et al. (1996) · Neuroscience · doi:10.1016/0306-4522(96)00095-4 · Cited by 72 · see citing works
Ma, X., & Suga, N. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0503851102 · Cited by 72 · see citing works
t Traveling Slow Waves of Neural Activity: A Novel Form of Network Activity in Developing Neocortex
Peinado, T. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-02-j0002.2000 · Cited by 68 · see citing works
Ego‐Stengel, V., Shulz, D. E., Haidarliu, S., Sosnik, R., & Ahissar, E. (2001) · Journal of Neurophysiology · doi:10.1152/jn.2001.86.1.422 · Cited by 65 · see citing works
Papke, R. L., Webster, J. C., Lippiello, P. M., Bencherif, M., & Francis, M. M. (2000) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2000.0750204.x · Cited by 63 · see citing works
Kilb, W., & Luhmann, H. J. (2000) · Journal of Neurophysiology · doi:10.1152/jn.2000.84.3.1681 · Cited by 62 · see citing works
Bina, K. G., Guzmán, P., Broide, R. S., Leslie, F. M., Smith, M. A., & O’Dowd, D. K. (1995) · The Journal of Comparative Neurology · doi:10.1002/cne.903630212 · Cited by 62 · see citing works
Holschneider, D. P., Waite, J. J., Leuchter, A. F., Walton, N. Y., & Scremin, O. U. (1999) · Experimental Brain Research · doi:10.1007/s002210050736 · Cited by 60 · see citing works
A direct nicotinic receptor-mediated inhibition recorded intracellularly in vitro
Wong, L. A., & Gallagher, J. P. (1989) · Nature · doi:10.1038/341439a0 · Cited by 58 · see citing works
Latsari, M., Dori, I., Antonopoulos, J., Chiotelli, M., & Dinopoulos, A. (2002) · The Journal of Comparative Neurology · doi:10.1002/cne.10156 · Cited by 53 · see citing works
Staiger, J. F., Masanneck, C., Schleicher, A., & Zuschratter, W. (2004) · Journal of Comparative Neurology · doi:10.1002/cne.10953 · Cited by 53 · see citing works
Self-citation192 IgG-saporin lesion of basal forebrain cholinergic neurons in neonatal rats
Pappas, B. A., Davidson, C. M., Fortin, T., et al. (1996) · Developmental Brain Research · doi:10.1016/0165-3806(96)00095-8 · Cited by 48 · see citing works
Disrupted tonotopy of the auditory cortex in mice lacking M1 muscarinic acetylcholine receptor
Zhang, Y. F., Dyck, R. H., Hamilton, S. E., Nathanson, N. M., & Yan, J. (2004) · Hearing Research · doi:10.1016/j.heares.2004.10.003 · Cited by 47 · see citing works
Shacka, J. J., & Robinson, S. E. (1998) · Neuroscience · doi:10.1016/s0306-4522(97)00564-2 · Cited by 46 · see citing works
Candy, J., Perry, E. K., Perry, R. H., Bloxham, C. A., Thompson, J., Johnson, M. H., Oakley, A. E., & Edwardson, J. A. (1985) · Neuroscience Letters · doi:10.1016/0304-3940(85)90406-9 · Cited by 46 · see citing works
Schröder, R., & Luhmann, H. J. (1997) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1997.tb01364.x · Cited by 44 · see citing works
Development of the cholinergic fibres innervating the cerebral cortex of the rat
Kiss, J. Z., & Patel, A. J. (1992) · International Journal of Developmental Neuroscience · doi:10.1016/0736-5748(92)90043-y · Cited by 43 · see citing works
Carbachol-induced Network Oscillations in the Intact Cerebral Cortex of the Newborn Rat
Kilb, W. (2003) · Cerebral Cortex · doi:10.1093/cercor/13.4.409 · Cited by 43 · see citing works
Muñoz‐Cueto, J. A., García‐Segura, L. M., & Ruiz‐Marcos, A. (1991) · Brain Research · doi:10.1016/0006-8993(91)90490-m · Cited by 42 · see citing works
Development of basal forebrain projections to visual cortex: Dil studies in rat
Calarco, C. A., & Robertson, R. T. (1995) · The Journal of Comparative Neurology · doi:10.1002/cne.903540409 · Cited by 41 · see citing works
Comparison of postnatal CNS development between male and female rats
Gregory, E. H. (1975) · Brain Research · doi:10.1016/0006-8993(75)90618-6 · Cited by 40 · see citing works
Amino Acid Determinants of α7 Nicotinic Acetylcholine Receptor Surface Expression
Dineley, K. T., & Patrick, J. W. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.275.18.13974 · Cited by 33 · see citing works
Csillik, A. E. (2002) · Cerebral Cortex · doi:10.1093/cercor/12.11.1193 · Cited by 32 · see citing works
Selective cholinergic immunolesioning affects synaptic plasticity in developing visual cortex
Kuczewski, N., Aztiria, E., Leanza, G., & Domenici, L. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.04014.x · Cited by 32 · see citing works
Hanganu, I. L., & Luhmann, H. J. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00010.2004 · Cited by 32 · see citing works
Self-citationMeinecke, D. L., & RAKIC, P. T. (1993) · Neuroscience · doi:10.1016/0306-4522(93)90386-t · Cited by 26 · see citing works
Mode of Blocking of Axonal Activity by Curare and Inhibitors of Acetyl-cholinesterase
Grundfest, H., Nachmansohn, D. A., Kao, C. Y., et al. (1952) · Nature · doi:10.1038/169190a0 · Cited by 24 · see citing works
Ostermann, C.-H., Grünwald, J., Wevers, A., Lorke, D. E., Reinhardt, S., Maelicke, A., & Schröder, H. C. (1995) · Neuroscience Letters · doi:10.1016/0304-3940(95)11598-q · Cited by 23 · see citing works
Pappas, B. A., Payne, K. B., Fortin, T., et al. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.02.040 · Cited by 22 · see citing works
Early retinal activity and visual circuit development
del Rio, T., & Feller, M. B. (2006) · Neuron · doi:10.1016/j.neuron.2006.10.001 · Cited by 21 · see citing works
Höhmann, C. F., & Coyle, J. T. (1988) · Brain Research Bulletin · doi:10.1016/0361-9230(88)90113-x · Cited by 20 · see citing works
Chessell, I. P., & Humphrey, P. P. A. (1995) · Neuropharmacology · doi:10.1016/0028-3908(95)00096-o · Cited by 20 · see citing works
Avignone, E., & Cherubini, E. (1999) · The Journal of Physiology · doi:10.1111/j.1469-7793.1999.0097r.x · Cited by 20 · see citing works
Siciliano, R., Fontanesi, G., Casamenti, F., Berardi, N., Bagnoli, P., & Domenici, L. (1997) · Visual Neuroscience · doi:10.1017/s0952523800008816 · Cited by 20 · see citing works
Cellular Morphology and Physiology of the Perinatal Rat Cerebral Cortex
Luhmann, H. J., Schubert, D., Kötter, R., & Staiger, J. F. (1999) · Developmental Neuroscience · doi:10.1159/000017379 · Cited by 16 · see citing works
Self-citationByers, D. M., Irwin, L. N., Moss, D. E., et al. (2005) · Developmental Brain Research · doi:10.1016/j.devbrainres.2005.05.003 · Cited by 15 · see citing works
Akimoto, H. (1961) · Brain and nerve · Cited by 13 · see citing works
Neonatal 192 IgG-saporin lesion of forebrain cholinergic neurons: focus on the life span?
Pappas, B. A., & Sherren, N. (2003) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(03)00067-8 · Cited by 13 · see citing works
Koh, S., Santos, T. C., & Cole, A. J. (2005) · Experimental Neurology · doi:10.1016/j.expneurol.2005.03.002 · Cited by 11 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Development of prefrontal cortex
Kolk, S. M., & Rakic, P. (2022) · Neuropsychopharmacology · doi:10.1038/s41386-021-01137-9 · Cited by 378 · see citing works
Yang, J.-W., Hanganu-Opatz, I. L., Sun, J.-J., & Luhmann, H. J. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.5646-08.2009 · Cited by 276 · see citing works
A conserved switch in sensory processing prepares developing neocortex for vision
Colonnese, M. T., Kaminska, A., Minlebaev, M., Milh, M., Bloem, B., Lescure, S., Moriette, G., Chiron, C., Ben-Ari, Y., & Khazipov, R. (2010) · Neuron · doi:10.1016/j.neuron.2010.07.015 · Cited by 273 · see citing works
Self-citationForm and function of sleep spindles across the lifespan
Clawson, B. C., Durkin, J., & Aton, S. J. (2016) · Neural Plasticity · doi:10.1155/2016/6936381 · Cited by 178 · see citing works
“Spindle bursts occur either spontaneously or are evoked by stimulation in visual cortex in rats [103, 104] and ferrets [105, 106], as well as barrel cortex in rats [107].”
BackgroundCortical development, electroencephalogram rhythms, and the sleep/wake cycle
Cirelli, C., & Tononi, G. (2015) · Biological Psychiatry · doi:10.1016/j.biopsych.2014.12.017 · Cited by 117 · see citing works
Sleep, plasticity, and sensory neurodevelopment
Blumberg, M. S., Dooley, J. C., & Tiriac, A. (2022) · Neuron · doi:10.1016/j.neuron.2022.08.005 · Cited by 93 · see citing works
Spindle activity orchestrates plasticity during development and sleep
Lindemann, C., Ahlbeck, J., Bitzenhofer, S. H., & Hanganu-Opatz, I. L. (2016) · Neural Plasticity · doi:10.1155/2016/5787423 · Cited by 59 · see citing works
Cholinergic Control in Developing Prefrontal–Hippocampal Networks
Janiesch, P. C., Krüger, H.-S., Pöschel, B., & Hanganu-Opatz, I. L. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.2644-11.2011 · Cited by 49 · see citing works
- Authors
- Hanganu, I. L., Staiger, J. F., Ben-Ari, Y., & Khazipov, R.
- Affiliations
- Inserm (FR)
- University of Freiburg (DE)
- ORCID
- Staiger, Jochen F.
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2007-05-23
- Volume
- 27
- Issue
- 21
- Pages
- 5694-5705
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6672769
- OpenAlex
- W1968879370
- Cited by
- 67
- References
- 156
- Citations by year
- 2026: 3 · 2025: 1 · 2024: 1 · 2023: 3 · 2022: 1 · 2021: 4 · 2020: 2 · 2019: 3 · 2018: 2 · 2017: 5 · 2016: 6 · 2015: 3 · 2014: 5 · 2013: 6 · 2012: 6
- FWCI
- 2.00
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion, other-oa)
- Funders
- Deutsche Forschungsgemeinschaft
- Agence Nationale de la Recherche
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
- Keywords
- cholinergic modulation, primary visual cortex, acetylcholine, muscarinic receptors, atropine, physostigmine, acetylcholinesterase, saporin lesion, retinal waves, cortical development, in vivo neuronal activity
- MeSH terms
- Animals, Animals, Newborn, Cholinergic Fibers, Male, Synaptic Transmission, Receptors, Muscarinic, Visual Cortex, Visual Pathways, Cholinergic Agents, Cholinergic Agonists, Cholinergic Antagonists, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review