Developmental regulation of nicotinic acetylcholine receptor‐mediated [3H]norepinephrine release from rat cerebellum
Abstract
Presynaptic modulation of synaptic transmission is the primary function of central nicotinic acetylcholine receptors (nAChRs) in developing and adult brain. nAChR activation regulates release of various neurotransmitters, including norepinephrine (NA). Given evidence that NA may serve a critical functional role in cerebellar development, we have undertaken studies to determine whether nAChRs modulate NA release in developing cerebellum. In vitro experiments using cerebellar slices examined the effects of nAChR stimulation on release of radiolabeled NA ([3H]NA). Our data indicate the presence of functional nAChRs on NA terminals in immature cerebellum and subsequent developmental regulation of receptor properties. During postnatal week one, the maximally effective dose of nicotine released 35.0 +/- 1.2% of cerebellar [3H]NA stores. There was a subsequent decline in maximal nicotine-stimulated NA release until postnatal day 30, when Emax values were statistically indistinguishable from adult. Although the efficacy of nicotine changed substantially throughout development, EC50 values did not differ significantly (EC50 = 4.4-12.0 micro m). Pharmacological analysis indicated that this developmental shift in maximum nicotine effect reflects a change in the properties of the nAChRs. These data support recent findings of a possible functional role of nAChRs in regulating cerebellar ontogeny, and provides further support for the role of NA as a neurotrophic factor during development.
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Presynaptic nicotinic ACh receptors
Wonnacott, S. (1997) · Trends in Neurosciences · doi:10.1016/s0166-2236(96)10073-4 · Cited by 1,308 · see citing works
Bayer, S. A., Altman, J., Russo, R. J., & Zhang, X. (1993) · PubMed · Cited by 912 · 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
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
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
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
Lauder, J. M., & Bloom, F. E. (1974) · The Journal of Comparative Neurology · doi:10.1002/cne.901550407 · Cited by 658 · see citing works
Luetje, C., & Patrick, J. (1991) · The Journal of Neuroscience · doi:10.1523/jneurosci.11-03-00837.1991 · Cited by 558 · see citing works
The cells and molecules that make a cerebellum
Goldowitz, D. (1998) · Trends in Neurosciences · doi:10.1016/s0166-2236(98)01313-7 · Cited by 493 · 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
Ontogeny of monoamine neurons in the locus coeruleus, raphe nuclei and substantia nigra of the rat
Lauder, J. M., & Bloom, F. E. (1975) · The Journal of Comparative Neurology · doi:10.1002/cne.901630302 · Cited by 412 · see citing works
Chavez-Noriega, L. E., Crona, J. H., Washburn, M. S., Urrutia, A., Elliott, K. J., & Johnson, E. C. (1997) · PubMed · Cited by 392 · see citing works
Le Novere, N., Zoli, M., & Changeux, J. (1996) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1996.tb01206.x · Cited by 385 · see citing works
Grady, S., Marks, M. J., Wonnacott, S., & Collins, A. C. (1992) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1992.tb08322.x · Cited by 350 · 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., Barbosa, C. T. F., & Albuquerque, E. X. (1997) · PubMed · Cited by 326 · see citing works
Modulation of long-term synaptic depression in visual cortex by acetylcholine and norepinephrine
Kirkwood, A., Rozas, C., Kirkwood, J., Perez, F., & Bear, M. F. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-05-01599.1999 · Cited by 315 · see citing works
Relationship of Sudden Infant Death Syndrome to Maternal Smoking During and After Pregnancy
Schoendorf, K. C., & Kiely, J. (1992) · PEDIATRICS · doi:10.1542/peds.90.6.905 · Cited by 303 · see citing works
Partial agonist properties of cytisine on neuronal nicotinic receptors containing the beta 2 subunit
Papke, R. L., & Heinemann, S. F. (1994) · Molecular Pharmacology · doi:10.1016/s0026-895x(25)09896-7 · Cited by 259 · see citing works
Evidence for "preterminal" nicotinic receptors on GABAergic axons in the rat interpeduncular nucleus
Léna, C., Changeux, J., & Mulle, C. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-06-02680.1993 · Cited by 255 · see citing works
Pugh, P., & Berg, D. K. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-02-00889.1994 · Cited by 252 · see citing works
Vizi, E. S., & Lendvai, B. (1999) · Brain Research Reviews · doi:10.1016/s0165-0173(99)00016-8 · Cited by 228 · see citing works
The α7 nicotinic acetylcholine receptor in neuronal plasticity
Broide, R. S., & Leslie, F. M. (1999) · Molecular Neurobiology · doi:10.1007/bf02741361 · Cited by 210 · see citing works
Self-citationAramakis, V. B., & Metherate, R. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-20-08485.1998 · Cited by 182 · see citing works
Diversity and distribution of nicotinic acetylcholine receptors in the locus ceruleus neurons
Léna, C., d’Exaerde, A. D. K., Cordero‐Erausquin, M., Novère, N. G. L., Jiménez, M. D. M. A., & Changeux, J. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.21.12126 · Cited by 181 · see citing works
Higgins, S. (2002) · Current Opinion in Obstetrics & Gynecology · doi:10.1097/00001703-200204000-00007 · Cited by 157 · see citing works
Cholinergic regulation of neurite outgrowth from isolated chick sympathetic neurons in culture
Small, D. H., Reed, G., Whitefield, B., & Nurcombe, V. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-01-00144.1995 · Cited by 144 · see citing works
Sudden Infant Death Syndrome and Smoking in the United States and Sweden
MacDorman, M. F., Cnattingius, S., Hoffman, H. J., Kramer, M. S., & Haglund, B. (1997) · American Journal of Epidemiology · doi:10.1093/oxfordjournals.aje.a009260 · Cited by 140 · see citing works
Alkondon, M., Rocha, E. S., Maelicke, A., & Albuquerque, E. X. (1996) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)20801-1 · Cited by 135 · 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
Self-citationMarks, M. J., Whiteaker, P., Calcaterra, J., Stitzel, J. A., Bullock, A. E., Grady, S. R., Picciotto, M. R., Changeux, J., & Collins, A. C. (1999) · PubMed · Cited by 126 · see citing works
A prospective study of smoking during pregnancy and SIDS
Wisborg, K. (2000) · Archives of Disease in Childhood · doi:10.1136/adc.83.3.203 · 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
Self-citationNeuron–Glia Signaling via α1Adrenoceptor-Mediated Ca2+Release in Bergmann Glial CellsIn Situ
Kulik, A., Haentzsch, A., Lückermann, M., Reichelt, W., & Ballanyi, K. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-19-08401.1999 · Cited by 119 · see citing works
Kirischuk, S., Tuschick, S., Verkhratsky, A., & Kettenmann, H. (1996) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1996.tb01288.x · Cited by 109 · see citing works
Sudden Infant Death Syndrome: A Failure of Compensatory Cerebellar Mechanisms?
Harper, R. M. (2000) · Pediatric Research · doi:10.1203/00006450-200008000-00004 · Cited by 100 · see citing works
Nakamura, S., & Sakaguchi, T. (1990) · Progress in Neurobiology · doi:10.1016/0301-0082(90)90018-c · Cited by 94 · see citing works
Brazell, M. P., Mitchell, S. N., & Gray, J. A. (1991) · Neuropharmacology · doi:10.1016/0028-3908(91)90116-s · Cited by 88 · see citing works
Nicotine-evoked [3H]5-hydroxytryptamine release from rat striatal synaptosomes
Reuben, M., & Clarke, P. B. S. (2000) · Neuropharmacology · doi:10.1016/s0028-3908(99)00147-1 · Cited by 84 · see citing works
Barazangi, N., & Role, L. W. (2001) · Journal of Neurophysiology · doi:10.1152/jn.2001.86.1.463 · Cited by 80 · see citing works
Regional patterns of cholinergic and glutamate activity in the developing and aging human brain
COURT, J. A., Perry, E. K., Johnson, M. H., Piggott, M. A., Kerwin, J. A., Perry, R. H., & Ince, P. G. (1993) · Developmental Brain Research · doi:10.1016/0165-3806(93)90085-o · Cited by 77 · see citing works
Altman, J., & Das, G. D. (1970) · Experimental Neurology · doi:10.1016/0014-4886(70)90159-7 · Cited by 66 · see citing works
The role of the cholinergic system in the development of the human cerebellum
COURT, J. A., Perry, E. K., Spurden, D., Griffiths, M., Kerwin, J. M., Morris, C. M., Johnson, M., Oakley, A. E., Birdsall, N. J. M., Clementi, F., et al. (1995) · Developmental Brain Research · doi:10.1016/0165-3806(96)83496-1 · Cited by 65 · see citing works
Hsieh, C. Y., Leslie, F. M., & Metherate, R. (2002) · Developmental Brain Research · doi:10.1016/s0165-3806(01)00314-5 · Cited by 54 · see citing works
Self-citationFrank, M. G., Srere, H. K., Ledezma, C., O’Hara, B. F., & Heller, H. C. (2001) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.2001.280.4.r1134 · Cited by 53 · see citing works
Cerebellar Cortex Delayed Maturation in Sudden Infant Death Syndrome
Cruz-Sánchez, F., Lucena, J., Ascaso, C., TOLOSA, E. S., Quintó, L., & ROSSI, M. L. (1997) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/00005072-199704000-00002 · Cited by 52 · see citing works
Effect of nicotine on cerebellar granule neuron development
Opanashuk, L. A., Pauly, J. R., & Hauser, K. F. (2001) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2001.01359.x · Cited by 51 · see citing works
Gallardo, K. A., & Leslie, F. M. (1998) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1998.70020663.x · Cited by 51 · see citing works
Self-citationCatecholaminergic terminals in the developing and adult rat cerebellum
Yamamoto, T., Ishikawa, M., & Tanaka, C. (1977) · Brain Research · doi:10.1016/0006-8993(77)90428-0 · Cited by 50 · see citing works
Developmental aspects of the locus coeruleus-noradrenaline system
Marshall, K. C., Christie, M. J., Finlayson, P. G., & Williams, J. T. (1991) · Progress in brain research · doi:10.1016/s0079-6123(08)63807-8 · Cited by 50 · see citing works
Nicotine exposure and the risk of SIDS
Milerad, J., & Sundell, H. (1993) · Acta Paediatrica · doi:10.1111/j.1651-2227.1993.tb12882.x · Cited by 48 · see citing works
Effects of 6-Hydroxydopamine-Induced Norepinephrine Depletion on Cerebellar Development
Lovell, K. L. (2007) · Developmental Neuroscience · doi:10.1159/000112695 · Cited by 48 · see citing works
Expression of α 7 neuronal nicotinic receptors during postnatal development of the rat cerebellum
del Toro, E. D., Juiz, J. M., Smillie, F. I., Lindstrom, J. M., & Criado, M. (1997) · Developmental Brain Research · doi:10.1016/s0165-3806(96)00185-x · Cited by 48 · see citing works
Tetrodotoxin-sensitivity of nicotine-evoked dopamine release from rat striatum
Marshall, D., Soliakov, L. S., Redfern, P. H., & Wonnacott, S. (1996) · Neuropharmacology · doi:10.1016/s0028-3908(96)00117-7 · Cited by 47 · see citing works
Acute synaptic modulation by nicotinic agonists in developing cerebellar Purkinje cells of the rat
Kawa, K. (2002) · The Journal of Physiology · doi:10.1113/jphysiol.2001.012885 · Cited by 43 · see citing works
Titmus, M., Tsai, H.-J., Lima, R. C., & Udin, S. B. (1999) · Neuroscience · doi:10.1016/s0306-4522(98)00625-3 · Cited by 41 · see citing works
Nicotinic Agonist Modulation of Neurotransmitter Levels in the Rat Frontoparietal Cortex
Summers, K. L., Kem, W. R., & Giacobini, E. (1997) · The Japanese Journal of Pharmacology · doi:10.1254/jjp.74.139 · Cited by 40 · see citing works
Gould, E., & Butcher, L. L. (1987) · Developmental Brain Research · doi:10.1016/0165-3806(87)90218-5 · Cited by 40 · see citing works
Evidence for cholinergic regulation of basal norepinephrine release in the rat olfactory bulb
El-Etri, M. M., Ennis, M. J., Griff, E. R., & Shipley, M. T. (1999) · Neuroscience · doi:10.1016/s0306-4522(99)00169-4 · Cited by 38 · see citing works
Postnatal development of two nicotinic cholinergic receptors in seven mouse brain regions
Fiedler, E. P., Marks, M. J., & Collins, A. C. (1990) · International Journal of Developmental Neuroscience · doi:10.1016/0736-5748(90)90045-4 · Cited by 37 · see citing works
Shao, Y., & McCarthy, K. D. (1997) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1997.68062405.x · Cited by 33 · see citing works
Marks, M. J., Bullock, A. E., & Collins, A. C. (1995) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)10641-1 · Cited by 33 · see citing works
Leslie, F. M., Gallardo, K. A., & Park, M. K. (2002) · Neuropharmacology · doi:10.1016/s0028-3908(02)00019-9 · Cited by 32 · see citing works
Self-citationO’Hara, B. F., Macdonald, E. S., Clegg, D., Wiler, S. W., Waldowski, R. A., Cao, V. H., Miller, J. D., Heller, H. C., & Kilduff, T. S. (1999) · Molecular Brain Research · doi:10.1016/s0169-328x(99)00004-2 · Cited by 31 · see citing works
Fu, Y., Matta, S. G., McIntosh, J. M., & Sharp, B. M. (1999) · Neuroscience Letters · doi:10.1016/s0304-3940(99)00293-1 · Cited by 28 · see citing works
Clos, J., Ghandour, S., Eberhart, R., Vincendon, G., & Gombos, G. (2007) · Developmental Neuroscience · doi:10.1159/000111898 · Cited by 25 · see citing works
Verney, C., Grzanna, R., & Farkas‐Bargeton, E. (2007) · Developmental Neuroscience · doi:10.1159/000112788 · Cited by 24 · see citing works
Postnatal Development of the Acetylcholine System in Different Parts of the Rat Cerebellum
Kása, P., Bánsághy, K., Rakonczay, Z., & Gulya, K. (1982) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1982.tb08009.x · Cited by 23 · see citing works
Podkletnova, I., & Alho, H. (1998) · Journal of Chemical Neuroanatomy · doi:10.1016/s0891-0618(98)00006-4 · Cited by 18 · see citing works
Raymon, H. K., & Leslie, F. M. (1994) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1994.62031015.x · Cited by 16 · see citing works
Self-citationLocus coeruleus - cerebellum: interaction during development.
Sievers, J., & Klemm, H. P. (1982) · PubMed · Cited by 13 · see citing works
Robertson, R. T., Yu, B. P., Liu, H., Liu, N. H., & Kageyama, G. H. (1991) · Experimental Neurology · doi:10.1016/0014-4886(91)90159-a · Cited by 12 · see citing works
Heydorn, W. E., Nguyen, K. Q., Creed, G. J., Kostrzewa, R. M., & Jacobowitz, D. M. (1986) · Brain Research · doi:10.1016/0006-8993(86)91575-1 · Cited by 9 · see citing works
Morphological studies on the development of the rat locus coeruleus.
Sievers, J., & Lolova, I. S. (1981) · PubMed · Cited by 3 · see citing works
Flagged first, then by citations
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Sorted by citations
The dynamic effects of nicotine on the developing brain
Dwyer, J. B., McQuown, S. C., & Leslie, F. M. (2009) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2009.02.003 · Cited by 559 · see citing works
Self-citationSlotkin, T. A. (2004) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2003.06.001 · Cited by 544 · see citing works
Prenatal smoking exposure and dopaminergic genotypes interact to cause a severe ADHD subtype
Neuman, R. J., Lobos, E., Reich, W., Henderson, C. A., Sun, L.-W., & Todd, R. D. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.08.049 · Cited by 277 · see citing works
Nicotine and brain development
Dwyer, J. B., Broide, R. S., & Leslie, F. M. (2008) · Birth Defects Research Part C: Embryo Today: Reviews · doi:10.1002/bdrc.20118 · Cited by 256 · see citing works
Self-citationEngland, L. J., Aagaard, K., Bloch, M., Conway, K., Cosgrove, K., Grana, R., Gould, T. J., Hatsukami, D., Jensen, F., Kandel, D., et al. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.11.013 · Cited by 181 · see citing works
Self-citationVidair, C. A. (2004) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2003.12.016 · Cited by 122 · see citing works
Nicotinic Cholinergic Receptors in the Rat Cerebellum: Multiple Heteromeric Subtypes
Turner, J. R., & Kellar, K. J. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.2112-05.2005 · Cited by 89 · see citing works
Catecholamine Secretory Vesicle Stimulus-Transcription Coupling in Vivo
Mahata, S. K., Mahapatra, N. R., Mahata, M., Wang, T. C., Kennedy, B. P., Ziegler, M. G., & O’Connor, D. T. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m305545200 · Cited by 78 · see citing works
The Cerebellar Dopaminergic System
Flace, P., Livrea, P., Basile, G. A., Galletta, D., Bizzoca, A., Gennarini, G., Bertino, S., Branca, J. J. V., Gulisano, M., Bianconi, S., et al. (2021) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2021.650614 · Cited by 72 · see citing works
Lin, H., Vicini, S., Hsu, F., Doshi, S., Takano, H., Coulter, D. A., & Lynch, D. R. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1007397107 · Cited by 67 · see citing works
Neuroprotective role of curcumin in the cerebellum of streptozotocin-induced diabetic rats
Peeyush, K. T., Gireesh, G., Jobin, M., & Paulose, C. S. (2009) · Life Sciences · doi:10.1016/j.lfs.2009.09.012 · Cited by 63 · see citing works
Azam, L., & McIntosh, J. M. (2006) · Molecular Pharmacology · doi:10.1124/mol.106.024513 · Cited by 56 · see citing works
Nicotine-induced monoamine neurotransmitter changes in the brain of young rats
Shearman, E., Fallon, S., Sershen, H., & Lajtha, A. (2008) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2008.03.017 · Cited by 55 · see citing works
Huang, L. Z., Abbott, L. C., & Winzer‐Serhan, U. H. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2007.03.008 · Cited by 54 · see citing works
The cholinergic system in the cerebellum: from structure to function
Zhang, C., Zhou, P., & Yuan, T. (2016) · Reviews in the Neurosciences · doi:10.1515/revneuro-2016-0008 · Cited by 53 · see citing works
Prefrontal neuromodulation by nicotinic receptors for cognitive processes
Coura, R., & Granon, S. (2012) · Psychopharmacology · doi:10.1007/s00213-011-2596-6 · Cited by 51 · see citing works
Peeyush, K. T., Balakrishnan, S., Sherin, A., Anju, T. R., Jes, P., & Paulose, C. S. (2010) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2010.01.008 · Cited by 45 · see citing works
Unique effects of nicotine across the lifespan
Ren, M., Lotfipour, S., & Leslie, F. (2022) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2022.173343 · Cited by 40 · see citing works
Self-citationHypoglycemia induced changes in cholinergic receptor expression in the cerebellum of diabetic rats
Antony, S., Pandit, P. K. T., Mathew, J., Anju, T. R., & Paulose, C. S. (2010) · Journal of Biomedical Science · doi:10.1186/1423-0127-17-7 · Cited by 40 · see citing works
Authority), E. (. F. S., Hernandez‐Jerez, A., Coja, T., Paparella, M., Price, A., Henri, J., Focks, A., Louisse, J., Terron, A., Binaglia, M., et al. (2024) · EFSA Journal · doi:10.2903/j.efsa.2024.8759 · Cited by 37 · see citing works
Intergenerational transmission of tobacco use and dependence: A transdisciplinary perspective
Shenassa, E. D., McCaffery, J. M., NIAURA, R. S., Swan, G. E., Khroyan, T. V., Shakib, S., Mouttapa, M., Lerman, C. E., Lyons, M. J., Buka, S. L., et al. (2003) · Nicotine & Tobacco Research · doi:10.1080/14622200310001625500 · Cited by 36 · see citing works
Self-citationCoura, R. S., Cressant, A., Xia, J., de Chaumont, F., Olivo‐Marin, J. C., Pelloux, Y., Dalley, J. W., & Granon, S. (2013) · The FASEB Journal · doi:10.1096/fj.13-231084 · Cited by 33 · see citing works
Effects of Ethanol on Excitatory and Inhibitory Synaptic Transmission in Rat Cortical Neurons
Moriguchi, S., Zhao, X., Marszalec, W., Yeh, J. Z., & Narahashi, T. (2006) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.2006.00266.x · Cited by 33 · see citing works
Section I. The Cholinergic System
Smythies, J. (2005) · International review of neurobiology · doi:10.1016/s0074-7742(05)64001-9 · Cited by 32 · see citing works
Villégier, A., Lotfipour, S., Belluzzi, J. D., & Leslie, F. M. (2007) · Psychopharmacology · doi:10.1007/s00213-007-0799-7 · Cited by 29 · see citing works
Self-citationNicotinic receptor modulation of neurotransmitter release in the cerebellum
Filippi, G. D., Baldwinson, T., & Sher, E. (2005) · Progress in brain research · doi:10.1016/s0079-6123(04)48024-8 · Cited by 25 · see citing works
Turner, J. R., Ortinski, P. I., Sherrard, R. M., & Kellar, K. J. (2011) · The Cerebellum · doi:10.1007/s12311-011-0285-y · Cited by 22 · see citing works
Khalki, H., Khalki, L., Aboufatima, R., Ouachrif, A., Mountassir, M., Ahmed Benharref, A., & Chait, A. (2012) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2012.01.020 · Cited by 21 · see citing works
Gómez, C., Briñón, J. G., Colado, M. I., Orío, L., Vidal, M., Barbado, M. V., & Alonso, J. R. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.05.046 · Cited by 21 · see citing works
α7-Nicotinic Acetylcholine Receptor: Role in Early Odor Learning Preference in Mice
Hellier, J. L., Arevalo, N. L., Smith, L. P., Xiong, K.-N., & Restrepo, D. (2012) · PLoS ONE · doi:10.1371/journal.pone.0035251 · Cited by 18 · see citing works
The Role of the Cerebellum in Drug Reward: A Review
Wang, Y., & Yan, L. (2023) · Journal of Integrative Neuroscience · doi:10.31083/j.jin2206147 · Cited by 15 · see citing works
O’Leary, K. T., & Leslie, F. M. (2005) · Neuropharmacology · doi:10.1016/j.neuropharm.2005.08.013 · Cited by 13 · see citing works
Self-citationImpact of Intrauterine Insults on Fetal and Postnatal Cerebellar Development in Humans and Rodents
Westerhuis, J. A. W., Dudink, J., Wijnands, B. E. C. A., Zeeuw, C. I. D., & Canto, C. B. (2024) · Cells · doi:10.3390/cells13221911 · Cited by 11 · see citing works
Intact Numbers of Cerebellar Purkinje and Granule Cells in Sudden Infant Death Syndrome
Kiessling, M. C., Büttner, A., Butti, C., Müller-Starck, J., Milz, S., Hof, P. R., Frank, H., & Schmitz, C. (2013) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/nen.0b013e3182a31c31 · Cited by 10 · see citing works
Xu, Y., Zhang, B., Su, W.-H., Wu, M.-C., Bing, Y.-H., Cui, S.-B., Chu, C., Li, Y.-Z., & Qiu, D. (2018) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2018.11.022 · Cited by 6 · see citing works
Nicotinic Receptor Regulation of Developing Catecholamine Systems
Leslie, F. M., Azam, L., Gallardo, K. A., O’Leary, K. T., Franke, R. M., & Lotfipour, S. (2006) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780195183139.003.0023 · Cited by 5 · see citing works
Self-citationEffect of Moringa Oleifera Extract on Nicotine Induced Neurotoxicity in Female Rat and Their Embryos
Abdu, F., & Arabia, S. (2013) · Cited by 4 · see citing works
Bidirectional interactions between neuromodulatory systems and the cerebellum in brain function
Kim, T., Park, H., Jun, S., Park, J., Yamamoto, Y., & Tanaka, K. (2026) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2026.106716 · Cited by 1 · see citing works
Presynaptic Nicotinic Acetylcholine Receptors: Subtypes and Functions
Marks, M. J., Grady, S. R., McClure‐Begley, T. D., O’Neill, H. C., & Zambrano, C. A. (2014) · The Receptors · doi:10.1007/978-1-4939-1167-7_4 · Cited by 1 · see citing works
Sherin, A., & Paulose, C. S. (2010) · Dyuthi Digital Repository (Cochin University of Science and Technology) · Cited by 1 · see citing works
Kumar, T. P., & Paulose, C. S. (2010) · Dyuthi Digital Repository (Cochin University of Science and Technology)
Wang, H., Jin, X., Xu, Y., Chu, C., Pei, F., Song, X., & Qiu, D. (2022) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2022.174854
- Authors
- O'Leary, K. T., & Leslie, F. M.
- Affiliations
- University of California, Irvine (US)
- Venue
- Journal of Neurochemistry
- Publisher
- Wiley
- Published
- 2003-02-07
- Volume
- 84
- Issue
- 5
- Pages
- 952-959
- ISSN
- 0022-3042 (ISSN-L)
- 1471-4159
- OpenAlex
- W1498625688
- Cited by
- 42
- References
- 74
- Citations by year
- 2026: 1 · 2024: 2 · 2023: 1 · 2022: 2 · 2021: 1 · 2018: 1 · 2016: 2 · 2014: 1 · 2013: 3 · 2012: 3
- FWCI
- 1.50
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Neurochemistry (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Electronics and Telecommunications Research Institute
- U.S. Public Health Service
- National Institute on Drug Abuse (DA-10612, P50DA013332, R01DA010612, DA 13332)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nicotinic Acetylcholine Receptors Study
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Health Sciences › Medicine › Physiology › Smoking Behavior and Cessation
- Keywords
- nicotinic acetylcholine receptors, noradrenaline release, cerebellum, cerebellar development, presynaptic modulation, nicotine, postnatal development, receptor maturation, neurotrophic factors, synaptic transmission
- MeSH terms
- Age Factors, Aging, Animals, Animals, Newborn, Cerebellum, Dose-Response Relationship, Drug, Female, Fluoxetine, Male, Nicotine, Norepinephrine, Receptors, Nicotinic, Tritium, Rats, Sprague-Dawley, Gene Expression Regulation, Developmental, Nicotinic Agonists, Nicotinic Antagonists, Symporters, Norepinephrine Plasma Membrane Transport Proteins, Rats, In Vitro Techniques
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