Properties of long-term synaptic plasticity and metaplasticity in organotypic slice cultures of rat hippocampus
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Abstract
The aim of this study was to investigate whether synaptic plasticity and metaplasticity in slice cultures of the young rat hippocampus were comparable to previously reported synaptic plasticity and metaplasticity in acute adult hippocampal slices. This is relevant since differences do exist between the preparations as a result of age and the ex vivo maintenance. We prepared and maintained slice cultures from 5- to 6-day-old rats according to the porous membrane method. After 12–16 days in vitro, extracellular low-frequency stimulation (LFS) and high-frequency stimulation (HFS) protocols were applied to the Schaffer collaterals, and extracellular field potentials were recorded in area CA1. LFS and HFS induced long-term depression (LTD) and long-term potentiation (LTP), respectively. LTP could be reversed by LFS, as could LTD by HFS 60 min after induction. Plotting the amount of LTD and LTP versus stimulation protocol demonstrated frequency-dependence of the sign and extent of plasticity. Priming activation of group 1 metabotropic glutamate receptors (mGluRs) with DHPG facilitated subsequent LTP, revealing a metaplastic effect similar to that observed in acute slices. Immunohistochemistry for group 1 mGluR subtypes mGluR1α and mGluR5 showed both receptors to be present in these cultures. We conclude that synaptic plasticity and mGluR-mediated metaplasticity are largely comparable to those effects found in acute in vitro techniques.
Keywords
Culture fEPSP LTP LTD mGluRNotes
Acknowledgements
We thank Professor W.C. Abraham and Dr. D. Ireland for comments and Ursula Rentzmann for labelling assistance. The work was supported by The Danish Medical Research Council; Grant number: 22-02-0380 and INTAS; Grant number: 2000-0441 and The Obel Family Foundation.
References
- Abraham WC (1996) Activity-dependent regulation of synaptic plasticity (metaplasticity) in the hippocampus. In: Kato N (ed)The hippocampus: functions and clinical relevance. Elsevier Science, BVGoogle Scholar
- Abraham WC, Bear MF (1996) Metaplasticity: the plasticity of synaptic plasticity. Trends Neurosci 19:126–130CrossRefPubMedGoogle Scholar
- Abraham WC, Tate WP (1997) Metaplasticity: a new vista across the field of synaptic plasticity. Prog Neurobiol 52:303–323CrossRefPubMedGoogle Scholar
- Bahr BA, Kessler M, Rivera S, Vanderklish PW, Hall RA, Mutneja MS, Gall C, Hoffman KB (1995) Stable maintenance of glutamate receptors and other synaptic components in long-term hippocampal slices. Hippocampus 5:425–439CrossRefPubMedGoogle Scholar
- Barrionuevo G, Schottler F, Lynch G (1980) The effect of repetitive low frequency stimulation on control and potentiated synaptic responses in the hippocampus. Life Sci 27:2385–2391CrossRefPubMedGoogle Scholar
- Berghorn KA, Bonnett JH, Hoffman GE (1994) cFos immunoreactivity is enhanced with biotin amplification. J Histochem Cytochem 42:1635–1642PubMedGoogle Scholar
- Bienenstock EL, Cooper LN, Munro PW (1982) Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex. J Neurosci 2:32–48PubMedGoogle Scholar
- Bortolotto ZA, Collingridge GL (1993) Characterisation of LTP induced by the activation of glutamate metabotropic receptors in area CA1 of the hippocampus. Neuropharmacology 32:1–9CrossRefPubMedGoogle Scholar
- Cohen AS, Abraham WC (1996) Facilitation of long-term potentiation by prior activation of metabotropic glutamate receptor. J Neurophysiol 76:953–962PubMedGoogle Scholar
- Cohen AS, Raymond CR, Abraham WC (1998) Priming of long-term potentiation induced by activation of metabotropic glutamate receptors coupled to phospholipase C. Hippocampus 8:160–170PubMedCrossRefGoogle Scholar
- Debanne D, Guerineau NC, Gähwiler BH, Thompson SM (1995) Physiology and pharmacology of unitary synaptic connections between pairs of cells in areas CA3 and CA1 of rat hippocampal slice cultures. J Neurophysiol 73:1282–1294PubMedGoogle Scholar
- Debanne D, Gähwiler BH, Thompson SM (1996a) Cooperative interactions in the induction of long-term potentiation and depression of synaptic excitation between hippocampal CA3-CA1 cell pairs in vitro. Proc Natl Acad Sci USA 93:11225–11230CrossRefPubMedGoogle Scholar
- Debanne D, Guerineau NC, Gähwiler BH, Thompson SM (1996b) Paired-pulse facilitation and depression at unitary synapses in rat hippocampus: quantal fluctuation affects subsequent release. J Physiol 491:163–176PubMedGoogle Scholar
- Debanne D, Gähwiler BH, Thompson SM (1997) Bidirectional associative plasticity of unitary CA3-CA1 EPSPs in the rat hippocampus in vitro. J Neurophysiol 77:2851–2855PubMedGoogle Scholar
- Debanne D, Gähwiler BH, Thompson SM (1998) Long-term synaptic plasticity between pairs of individual CA3 pyramidal cells in rat hippocampal slice cultures. J Physiol 507:237–247CrossRefPubMedGoogle Scholar
- De Simoni A, Griesinger CB, Edwards FA (2003) Development of rat CA1 neurones in acute versus organotypic slices: role of experience in synaptic morphology and activity. J Physiol 550:135–147CrossRefPubMedGoogle Scholar
- Deupree DL, Turner DA, Watters CL (1991) Spatial performance correlates with in vitro potentiation in young and aged Fischer 344 rats. Brain Res 554:1–9CrossRefPubMedGoogle Scholar
- Dudek SM, Bear MF (1992) Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-D-aspartate receptor blockade. Proc Natl Acad Sci USA 89:4363–4367PubMedCrossRefGoogle Scholar
- Ehrlich I, Malinow R (2004) Postsynaptic density 95 controls AMPA receptor incorporation during long-term potentiation and experience-driven synaptic plasticity. J Neurosci 24(4):916–927CrossRefPubMedGoogle Scholar
- Errington ML, Galley PT, Bliss TV (2003) Long-term potentiation in the dentate gyrus of the anaesthetized rat is accompanied by an increase in extracellular glutamate: real-time measurements using a novel dialysis electrode. Philos Trans R Soc Lond B 358:675–687CrossRefGoogle Scholar
- Fujii S, Saito K, Miyakawa H, Ito K, Kato H (1991) Reversal of long-term potentiation (depotentiation) induced by tetanus stimulation of the input to CA1 neurons of guinea pig hippocampal slices. Brain Res 555:112–122CrossRefPubMedGoogle Scholar
- Gähwiler BH (1981) Organotypic monolayer cultures of nervous tissue. J Neurosci Methods 4:329–342CrossRefPubMedGoogle Scholar
- Gähwiler BH (1984) Development of the hippocampus in vitro: cell types, synapses and receptors. Neuroscience 11:751–760CrossRefPubMedGoogle Scholar
- Gähwiler BH, Capogna M, Debanne D, McKinney RA, Thompson SM (1997) Organotypic slice cultures: a technique has come of age. Trends Neurosci 20:471–477CrossRefPubMedGoogle Scholar
- Huber KM, Kayser MS, Bear MF (2000) Role for rapid dendritic protein synthesis in hippocampal mGluR-dependent long-term depression. Science 288:1254–1256CrossRefPubMedGoogle Scholar
- Jahnsen H, Kristensen BW, Thiebaud P, Noraberg J, Jakobsen B, Bove M, Martinoia S, Koudelka-Hep M, Grattarola M, Zimmer J (1999) Coupling of organotypic brain slice cultures to silicon-based arrays of electrodes. Methods 18:160–172CrossRefPubMedGoogle Scholar
- Kauderer BS, Kandel ER (2000) Capture of a protein synthesis-dependent component of long-term depression. Proc Natl Acad Sci USA 97:13342–13347CrossRefPubMedGoogle Scholar
- Kramar EA, Lynch G (2003) Developmental and regional differences in the consolidation of long-term potentiation. Neuroscience 118:387–398CrossRefPubMedGoogle Scholar
- Landfield PW, Pitler TA, Applegate MD (1986) The effects of high Mg2+-to-Ca2+ ratios on frequency potentiation in hippocampal slices of young and aged rats. J Neurophysiol 56:797–811PubMedGoogle Scholar
- Leutgeb JK, Frey JU, Behnisch T (2003) LTP in cultured hippocampal-entorhinal cortex slices from young adult (P25–30) rats. J Neurosci Methods 130:19–32CrossRefPubMedGoogle Scholar
- Luján R, Nusser Z, Roberts JDB, Shigemoto R, Somogyi P (1996) Perisynaptic localization of metabotropic glutamate receptors mGluR1 and mGluR5 on dendritic spines in the rat hippocampus. Eur J Neurosci 8:1488–1500PubMedCrossRefGoogle Scholar
- Malherbe P, Kew JN, Richards JG, Knoflach F, Kratzeisen C, Zenner MT, Faull RL, Kemp JA, Mutel V (2002) Identification and characterization of a novel splice variant of the metabotropic glutamate receptor 5 gene in human hippocampus and cerebellum. Brain Res Mol Brain Res 109:168–178CrossRefPubMedGoogle Scholar
- Mellentin C, Abraham WC (2001) Priming stimulation of group II metabotropic glutamate receptors inhibits the subsequent induction of rat hippocampal long-term depression in vitro. Neurosci Lett 307:13–16CrossRefPubMedGoogle Scholar
- Moore CI, Browning MD, Rose GM (1993) Hippocampal plasticity induced by primed burst, but not long-term potentiation, stimulation is impaired in area CA1 of aged Fischer 344 rats. Hippocampus 3:57–66CrossRefPubMedGoogle Scholar
- Mulkey RM, Malenka RC (1992) Mechanisms underlying induction of homosynaptic long-term depression in area CA1 of the hippocampus. Neuron 9:967–975CrossRefPubMedGoogle Scholar
- Muller D, Buchs PA, Stoppini L (1993) Time course of synaptic development in hippocampal organotypic cultures. Brain Res Dev Brain Res 71.1:93–100CrossRefGoogle Scholar
- Muller D, Wang C, Skibo G, Toni N. Cremer H, Calaora V, Rougon G, Kiss JZ (1996) PSA-NCAM is required for activity-induced synaptic plasticity. Neuron 17:413–422CrossRefPubMedGoogle Scholar
- Nakagami Y, Abe K, Nishiyama N, Matsuki N (2000) Laminin degradation by plasmin regulates long-term potentiation. J Neurosci 20:2003–2010PubMedGoogle Scholar
- Norris CM, Korol DL, Foster TC (1996) Increased susceptibility to induction of long-term depression and long-term potentiation reversal during aging. J Neurosci 16:5382–5392PubMedGoogle Scholar
- O’Dell TJ, Kandel ER (1994) Low-frequency stimulation erases LTP through and NMDA receptor-mediated activation of protein phosphatases. Learn Mem 1:129–139PubMedGoogle Scholar
- Palmer M J, Irving AJ, Seabrook GR, Jane DE, Collingridge GL (1997) The group 1 mGlu receptor agonist DHPG induces a novel form of LTD in the CA1 region of the hippocampus. Neuropharmacology 36:1517–1532CrossRefPubMedGoogle Scholar
- Raymond CR, Thompson VL, Tate WP, Abraham WC (2000) Metabotropic glutamate receptors trigger homosynaptic protein synthesis to prolong long-term potentiation. J Neurosci 20:969–976PubMedGoogle Scholar
- Shigemoto R, Kinoshita A, Wada E, Nomura S, Ohishi H, Tkada M, Flor P, Neki A, Abe T, Nakanishi S, Mizuno N (1997) Differential presynaptic localization of metabotropic glutamate receptor subtypes in the rat hippocampus. J Neurosci 17:7503–7522PubMedGoogle Scholar
- Shimono K, Baudry M, Ho L, Taketani M, Lynch G (2002a) Long-term recording of LTP in cultured hippocampal slices. Neural Plast 9:249–254PubMedCrossRefGoogle Scholar
- Shimono K, Baudry M, Panchenko V, Taketani M (2002b) Chronic multichannel recordings from organotypic hippocampal slice cultures:protection from excitotoxic effects of NMDA by non-competitive NMDA antagonists. J Neurosci Methods 120:193–202CrossRefPubMedGoogle Scholar
- Staubli U, Lynch G (1990) Stable depression of potentiated synaptic responses in the hippocampus with 1–5 Hz stimulation. Brain Res 513:113–118CrossRefPubMedGoogle Scholar
- Stoppini L, Buchs P-A, Muller D (1991) A simple method for organotypic cultures of nervous tissue. J Neurosci Methods 37:173–182CrossRefPubMedGoogle Scholar
- Wang H, Wagner JJ (1999) Priming-induced shift in synaptic plasticity in the rat hippocampus. J Neurophys 82:2024–2028Google Scholar
- Wagner JJ, Alger BE (1995) GABAergic and developmental influences on homosynaptic LTD and depotentiation and rat hippocampus. J Neurosci 15:1577–1586PubMedGoogle Scholar
- Wexler EM, Stanton PK (1993) Priming of homosyanptic long-term depression in hippocampus by previous synaptic activity. Neuroreport 4:591–594PubMedCrossRefGoogle Scholar