Selective cholinergic immunolesioning affects synaptic plasticity in developing visual cortex

European Journal of Neuroscience

Volumn 21, Issue 7, 2005, Pages 1807-1814

  Kuczewski, N ^a   Aztiria, E ^a   Leanza, G ^b   Domenici, Luciano ^a,c  

^a SISSA   (Italy)

^b UNIVERSITY OF TRIESTE   (Italy)

^c CNR   (Italy)

Author keywords

192 IgG saporin; Basal forebrain; ChAT; Field potential; LTP; Muscarinic; Rat

Indexed keywords

ACETYLCHOLINE; IMMUNOGLOBULIN G; MESSENGER RNA; MUSCARINIC M1 RECEPTOR; MUSCARINIC M2 RECEPTOR; SAPORIN;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; BRAIN INJURY; CELL MATURATION; CHOLINERGIC SYSTEM; CHOLINERGIC TRANSMISSION; CONCENTRATION RESPONSE; CONTROLLED STUDY; ELECTRIC POTENTIAL; FEMALE; FOREBRAIN; LONG TERM POTENTIATION; MALE; NERVE CELL PLASTICITY; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; RAT; SENSORY NERVE; SYNAPSE; SYNAPTIC TRANSMISSION; VISUAL CORTEX;

ACETYLCHOLINE; ANIMALS; ANIMALS, NEWBORN; ANTIBODIES, MONOCLONAL; CHOLINE O-ACETYLTRANSFERASE; CHOLINERGIC AGENTS; DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTROPHYSIOLOGIC TECHNIQUES, CARDIAC; FEMALE; HIPPOCAMPUS; IMMUNOTOXINS; MALE; N-GLYCOSYL HYDROLASES; NEURONAL PLASTICITY; NEURONS; RATS; RATS, WISTAR; RECEPTORS, MUSCARINIC; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SYNAPTIC TRANSMISSION; VISUAL CORTEX;

EID: 18844381653     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2005.04014.x     Document Type: Article

References (48)

1. Akaneya, Y., Tsumoto, T., Kinoshita, S. & Hatanaka, H. (1997) Brain-derived neurotrophic factor enhances long-term potentiation in rat visual cortex. J. Neurosci., 17, 6707-6716.
2. Bear, M.F. & Singer, W. (1986) Modulation of visual cortical plasticity by acetylcholine and noradrenaline. Nature, 320, 172-176.
3. Bermudez-Rattoni, F., Ramirez-Lugo, L., Gutierrez, R. & Miranda, M.I. (2004) Molecular signals into the insular cortex and amygdala during aversive gustatory memory formation. Cell. Mol. Neurobiol., 24, 25-36.
4. Brancucci, A., Kuczewski, N., Covaceuszach, S., Cattaneo, A. & Domenici, L. (2004) NGF favors LTD over LTP in layer II-III neurons of rat visual cortex. J. Physiol. (Lond.), 559, 497-506.
5. Brocher, S., Artola, A. & Singer, W. (1992) Agonists of cholinergic and noradrenergic receptors facilitate synergistically the induction of long-term potentiation in slices of rat visual cortex. Brain Res., 573, 27-36.
6. Burgard, E.C. & Sarvey, J.M. (1990) Muscarinic receptor activation facilitates the induction of long-term potentiation (LTP) in the rat dentate gyrus. Neurosci. Lett., 116, 34-39.
7. Calarco, C.A. & Robertson, R.T. (1995) Development of basal forebrain projections to visual cortex: DiI studies in rat. J. Comp. Neurol., 354, 608-626.
8. Deutsch, J.A. (1971) The cholinergic synapse and the site of memory. Science, 174, 788-794.
9. Domenici, L., Harding, G.W. & Burkhalter, A. (1995) Patterns of synaptic activity in forward and feedback pathways within rat visual cortex. J. Neurophysiol., 74, 2649-2664.
10. Drachman, D.A. & Leavitt, T.J. (1974) Human memory and the cholinergic system. A relationship to aging? Arch. Neurol., 30, 113-121.
11. Eckenstein, P.P., Baughman, R.W. & Quinn, J. (1988) An anatomical study of cholinergic innervation in rat cerebral cortex. Neuroscience, 25, 457-474.
12. Gu, Q. (2002) Neuromodulatory transmitter systems in the cortex and their role in cortical plasticity. Neuroscience, 111, 815-835.
13. Gu, Q. & Singer, W. (1989) The role of muscarinic acetylcholine receptors in ocular dominance plasticity. In Frotscher, M. & Misgeld, U. (Eds), Central Cholinergic Synaptic Transmission, Birkhäuser, Basel, pp. 305-314.
14. Gu, Q. & Singer, W. (1993) Effects of intracortical infusion of anticholinergic drags on neuronal plasticity in kitten striate cortex. Eur. J. Neurosci., 5, 475-485.
15. Haruta, H., Kamishita, T., Hicks, T.P., Takahashi, M.P. & Tsumoto, T. (1994) Induction of LTD but not LTP through metabotropic gluatamate receptors in visual cortex. Neuroreport, 5, 1829-1832.
16. Hasselmo, M.E. (1999) Neuromodulation: acetylcholine and memory consolidation. Trends Cogn. Sci., 3, 351-359.
17. Hasselmo, M.E. & Barkai, E. (1995) Cholinergic modulation of activity-dependent synaptic plasticity in the piriform cortex and associative memory function in a network biophysical simulation. J. Neurosci., 15, 6592-6604.
18. Hedreen, J.C., Bacon, S.J. & Price, D.L. (1985) A modified histochemical technique to visualize acetylcholinesterase-containing axons. J. Histochem. Cytochem., 33, 34-40.
19. Hohmann, C.F. & Berger-Sweeney, J. (1998) Cholinergic regulation of cortical development and plasticity. New twists to an old story. Perspect. Dev. Neurobiol., 5, 401-425.
20. Hohmann, C.F., Brooks, A.R. & Coyle, J.T. (1988) Neonatal lesions of the basal forebrain cholinergic neurons result in abnormal cortical development. Brain Res., 470, 253-264.
21. Hohmann, C.F., Kwiterovich, K.K., Oster-Granite, M.L. & Coyle, J.T. (1991) Newborn basal forebrain lesions disrupt cortical cytodifferentiation as visualized by rapid Golgi staining. Cereb. Cortex, 1, 143-157.
22. Jones, M.W., French, P.J., Bliss, T.V. & Rosenblum, K. (1999) Molecular mechanisms of long-term potentiation in the insular cortex in vivo. J. Neurosci., 19, RC36.
23. Katz, L.C. & Shatz, C.J. (1996) Synaptic activity and the construction of cortical circuits. Science, 274, 1133-1138.
24. Kirkwood, A., Dudek, S.M., Gold, J.T., Aizenman, C.D. & Bear, M.F. (1993) Common forms of synaptic plasticity in the hippocampus and neocortex in vitro. Science, 260, 1518-1521.
25. Kirkwood, A., Rioult, M.C. & Bear, M.F. (1996) Experience-dependent modification of synaptic plasticity in visual cortex. Nature, 381, 526-528.
26. Kirkwood, A., Rozas, C., Kirkwood, J., Ferez, F. & Bear, M.F. (1999) Modulation of long-term synaptic depression in visual cortex by acetylcholine and norepinephrine. J. Neurosci., 19, 1599-1609.
27. Kojic, L., Gu, Q., Douglas, R.M. & Cynader, M.S. (2001) Laminar distribution of cholinergic- and serotonergic-dependent plasticity within kitten visual cortex. Brain Res. Dev. Brain Res., 126, 157-162.
28. Leanza, G., Muir, J., Nilsson, O.G., Wiley, R.G., Dunnett, S.B. & Bjorklund, A. (1996a) Selective immunolesioning of the basal forebrain cholinergic system disrupts short-term memory in rats. Eur. J. Neurosci., 8, 1535-1544.
29. Leanza, G., Nilsson, O.G., Nikkhah, G., Wiley, R.G. & Bjorklund, A. (1996b) Effects of neonatal lesions of the basal forebrain cholinergic system by 192 immunoglobulin G-saporin: biochemical, behavioural and morphological characterization. Neuroscience, 74, 119-141.
30. Leanza, G., Nilsson, O.G., Wiley, R.G. & Bjorklund, A. (1995) Selective lesioning of the basal forebrain cholinergic system by intraventricular 192 IgG-saporin: behavioural, biochemical and stereological studies in the rat. Eur. J. Neurosci., 7, 329-343.
31. Linster, C., Maloney, M., Patil, M. & Hasselmo, M.E. (2003) Enhanced cholinergic suppression of previously strengthened synapses enables the formation of self-organized representations in olfactory cortex. Neurobiol. Learn. Mem., 80, 302-314.
32. Mesulam, M.M., Mufson, E.J., Warner, B.H. & Levey, A.I. (1983) Central cholinergic pathways in the rat: an overview based on an alternative nomenclature (Ch1-Ch6). Neuroscience, 10, 1185-1201.
33. Mitzdorf, U. (1985) Current source-density method and application in cat cerebral cortex: investigation of evoked potentials and EEG phenomena. Physiol. Rev., 65, 37-100.
34. Mitzdorf, U. & Singer, W. (1980) Monocular activation of visual cortex in normal and monocularly deprived cats: an analysis of evoked potentials. J. Physiol. (Lond.), 304, 203-220.
35. Motooka, Y., Kondoh, T., Nomura, T., Tamaki, N., Tozaki, H., Kanno, T. & Nishizaki, T. (2001) Selective cholinergic denervation inhibits expression of long-term potentiation in the adult but not infant rat hippocampus. Brain Res. Dev. Brain Res., 129, 119-123.
36. Pesavento, E., Capsoni, S., Domenici, L. & Cattaneo, A. (2002) Acute cholinergic rescue of synaptic plasticity in the neurodegenerating cortex of anti-nerve-growth-factor mice. Eur. J. Neurosci., 15, 1030-1036.
37. Pesavento, E., Margotti, E., Righi, M., Cattaneo, A. & Domenici, L. (2000) Blocking the NGF-TrkA interaction rescues the developmental loss of LTP in the rat visual cortex: role of the cholinergic system. Neuron, 25, 165-175.
38. Rasband, W.S. & Bright, D.S. (1995) NIH Image: a public domain image processing program for the Macintosh. Microbeam Anal. Soc. J., 4, 37-149.
39. Robertson, R.T., Gallardo, K.A., Claytor, K.J., Ha, D.H., Ku, K.H., Yu B.P., Lauterborn, J.C. & Wiley, R.G., Yu J., Gall, C.M. & Leslie, F.M. (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.
40. Rogers, J.L. & Kesner, R.P. (2003) Cholinergic modulation of the hippocampus during encoding and retrieval. Neurobiol. Learn. Mem., 80, 332-342.
41. Rolls, E.T. (1996) A theory of hippocampal function in memory. Hippocampus, 6, 601-620.
42. Rossner, S., Schliebs, R., Perez-Polo, J.R., Wiley, R.G. & Bigl, V. (1995) Differential changes in cholinergic markers from selected brain regions after specific immunolesion of the rat cholinergic basal forebrain system. J. Neurosci. Res., 40, 31-43.
43. Sachdev, R.N., Lu, S.M., Wiley, R.G. & Ebner, F.F. (1998) Role of the basal forebrain cholinergic projection in somatosensory cortical plasticity. J. Neurophysiol., 79, 3216-3228.
44. 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. Visual Neurosci., 14, 111-123.
45. Tanaka, Y., Sakurai, M. & Hayashi, S. (1989) Effect of scopolamine and HP 029, a cholinesterase inhibitor, on long-term potentiation in hippocampal slices of the guinea pig. Neurosci. Lett., 98, 179-183.
46. Waite, J.J., Wardlow, M.L., Chen, A.C., Lappi, D.A., Wiley, R.G. & Thal, L.J. (1994) Time course of cholinergic and monoaminergic changes in rat brain after immunolesioning with 192 IgG-saporin. Neurosi. Lett., 169, 154-158.
47. Wiley, R.G. (1992) Neural lesioning with ribosome-inactivating proteins: suicide transport and immunolesioning. Trends Neurosci., 15, 285-290.
48. Wilson, D.A., Fletcher, M.L. & Sullivan, R.M. (2004) Acetylcholine and olfactory perceptual learning. Learn. Mem., 11, 28-34.