Synaptic strength at the temporoammonic input to the hippocampal CA1 region in vivo is regulated by NMDA receptors, metabotropic glutamate receptors and voltage-gated calcium channels

Neuroscience

Volumn 309, Issue , 2015, Pages 191-199

  Aksoy Aksel, A ^a,b   Manahan Vaughan, D ^a,b  

^a RUHR UNIVERSITY BOCHUM   (Germany)

^b RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

CA1; Hippocampus; In vivo; Perforant path; Synaptic plasticity; Temporoammonic

Indexed keywords

2 (2,3 DICARBOXYCYCLOPROPYL)GLYCINE; 2 AMINO 5 PHOSPHONOVALERIC ACID; CALCIUM CHANNEL L TYPE; GALLOPAMIL; METABOTROPIC RECEPTOR 2; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; VOLTAGE GATED CALCIUM CHANNEL; 2-(2,3-DICARBOXYCYCLOPROPYL)GLYCINE; 2-AMINO-5-PHOSPHOPENTANOIC ACID; AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; CYCLOPROPANE DERIVATIVE; GLYCINE; METABOTROPIC RECEPTOR; VALINE;

ADULT; ANIMAL EXPERIMENT; ARTICLE; BRAIN DEPTH STIMULATION; CONTROLLED STUDY; DENTATE GYRUS; HIPPOCAMPAL CA1 REGION; IN VIVO STUDY; LONG TERM POTENTIATION; MALE; NERVE CELL PLASTICITY; NERVOUS SYSTEM PARAMETERS; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; SYNAPSE; SYNAPTIC TRANSMISSION; SYNAPTOSOME; TEMPOROAMMONIC INPUT; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; DOSE RESPONSE; DRUG EFFECTS; ELECTROCORTICOGRAPHY; ELECTRODE IMPLANT; ELECTROSTIMULATION; EXCITATORY POSTSYNAPTIC POTENTIAL; METABOLISM; PERFORANT NERVE TRACT; PHYSIOLOGY; WISTAR RAT;

ANIMALS; CA1 REGION, HIPPOCAMPAL; CALCIUM CHANNELS, L-TYPE; CYCLOPROPANES; DENTATE GYRUS; DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTRIC STIMULATION; ELECTROCORTICOGRAPHY; ELECTRODES, IMPLANTED; EXCITATORY POSTSYNAPTIC POTENTIALS; GALLOPAMIL; GLYCINE; LONG-TERM POTENTIATION; MALE; NEUROTRANSMITTER AGENTS; PERFORANT PATHWAY; RATS, WISTAR; RECEPTORS, METABOTROPIC GLUTAMATE; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPSES; VALINE;

EID: 84945470160     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2015.03.014     Document Type: Article

References (47)

1. Abraham W.C., Tate W.P. Metaplasticity: a new vista across the field of synaptic plasticity. Prog Neurobiol 1997, 52(4):303-323.
2. Aksoy-Aksel A., Manahan-Vaughan D. The temporoammonic input to the hippocampal CA1 region displays distinctly different synaptic plasticity compared to the Schaffer collateral input in vivo: significance for synaptic information processing. Front Synap Neurosci 2013, 5:5.
3. Altinbilek B., Manahan-Vaughan D. A specific role for group II metabotropic glutamate receptors in hippocampal long-term depression and spatial memory. Neuroscience 2009, 158:149-158.
4. Bauer E.P., Schafe G.E., LeDoux J.E. NMDA receptors and L-type voltage-gated calcium channels contribute to long-term potentiation and different components of fear memory formation in the lateral amygdala. J Neurosci 2002, 22(12):5239-5249.
5. Borroni A.M., Fichtenholtz H., Woodside B.L., Teyler T.J. Role of voltage-dependent calcium channel long-term potentiation (LTP) and NMDA LTP in spatial memory. J Neurosci 2000, 20(24):9272-9276.
6. Brun V.H. Place cells and place recognition maintained by direct entorhinal-hippocampal circuitry. Science 2002, 296(5576):2243-2246.
7. Da Silva W.C., Cardoso G., Bonini J.S., Benetti F., Izquierdo I. Memory reconsolidation and its maintenance depend on L-voltage-dependent calcium channels and CaMKII functions regulating protein turnover in the hippocampus. Proc Natl Acad Sci USA 2013, 110(16):6566-6570.
8. Davis S.E., Bauer E.P. L-type voltage-gated calcium channels in the basolateral amygdala are necessary for fear extinction. J Neurosci 2012, 32(39):13582-13586.
9. Freir D.B., Herron C.E. Inhibition of L-type voltage dependent calcium channels causes impairment of long-term potentiation in the hippocampal CA1 region in vivo. Brain Res 2003, 967(1-2):27-36.
10. Golding N.L., Staff N.P., Spruston N. Dendritic spikes as a mechanism for cooperative long-term potentiation. Nature 2002, 418:326-331.
11. Grover L.M., Teyler T.J. Two components of long-term potentiation induced by different patterns of afferent activation. Nature 1990, 347(6292):477-479.
12. Hagena H., Manahan-Vaughan D. Frequency facilitation at mossy fiber-CA3 synapses of freely behaving rats contributes to the induction of persistent LTD via an adenosine-A1 receptor-regulated mechanism. Cereb Cortex 2010, 20(5):1121-1130.
13. Holscher C., Anwyl R., Rowan M.J. Activation of group-II metabotropic glutamate receptors blocks induction of long-term potentiation and depotentiation in area CA1 of the rat in vivo. Eur J Pharmacol 1997, 322(2-3):155-163.
14. Huang L.Q., Rowan M.J., Anwyl R. mGluR II agonist inhibition of LTP induction, and mGluR II antagonist inhibition of LTD induction, in the dentate gyrus in vitro. NeuroReport 1997, 8(3):687-693.
15. Isomura Y., Fujiwara-Tsukamoto Y., Imanishi M., Nambu A., Takada M. Distance-dependent Ni(2+)-sensitivity of synaptic plasticity in apical dendrites of hippocampal CA1 pyramidal cells. J Neurophysiol 2002, 87:1169-1174.
16. Izumi Y., Zorumski C.F. Direct cortical inputs erase long-term potentiation at Schaffer collateral synapses. J Neurosci 2008, 28(38):9557-9563.
17. Kemp A., Manahan-Vaughan D. Hippocampal long-term depression and long-term potentiation encode different aspects of novelty acquisition. Proc Natl Acad Sci USA 2004, 101(21):8192-8197.
18. Kemp A., Manahan-Vaughan D. Hippocampal long-term depression: master or minion in declarative memory processes?. Trends Neurosci 2007, 30:111-118.
19. Kew J.N., Ducarre J.M., Pflimlin M.C., Mutel V., Kemp J.A. Activity-dependent presynaptic autoinhibition by group II metabotropic glutamate receptors at the perforant path inputs to the dentate gyrus and CA1. Neuropharmacology 2001, 40(1):20-27.
20. Kew J.N., Pflimlin M.C., Kemp J.A., Mutel V. Differential regulation of synaptic transmission by mGlu2 and mGlu3 at the perforant path inputs to the dentate gyrus and CA1 revealed in mGlu2-/- mice. Neuropharmacology 2002, 43(2):215-221.
21. Klausnitzer J., Manahan-Vaughan D. Frequency facilitation at mossy fiber-CA3 synapses of freely behaving rats is regulated by adenosine A1 receptors. J Neurosci 2008, 28:4836-4840.
22. Kulla A., Reymann K.G., Manahan-Vaughan D. Time-dependent induction of depotentiation in the dentate gyrus of freely moving rats: involvement of group 2 metabotropic glutamate receptors. Eur J Neurosci 1999, 11(11):3864-3872.
23. Lisman J.E., Otmakhova N.A. Storage, recall, and novelty detection of sequences by the hippocampus: elaborating on the SOCRATIC model to account for normal and aberrant effects of dopamine. Hippocampus 2001, 11(5):551-568.
24. Lisman J., Yasuda R., Raghavachari S. Mechanisms of CaMKII action in long-term potentiation. Nat Rev Neurosci 2012, 13(3):169-182.
25. Luscher C., Malenka R.C. NMDA receptor-dependent long-term potentiation and long-term depression (LTP/LTD). Cold Spring Harbor Perspect Biol 2012, 4(6).
26. Magee J.C. Dendritic hyperpolarization-activated currents modify the integrative properties of hippocampal CA1 pyramidal neurons. J Neurosci 1998, 18:7613-7624.
27. Manahan-Vaughan D. Group 1 and 2 metabotropic glutamate receptors play differential roles in hippocampal long-term depression and long-term potentiation in freely moving rats. J Neurosci 1997, 17(9):3303-3311.
28. Manahan-Vaughan D. Priming of group 2 metabotropic glutamate receptors facilitates induction of long-term depression in the dentate gyrus of freely moving rats. Neuropharmacology 1998, 37:1459-1464.
29. Manahan-Vaughan D., Reiser M., Pin J.P., Wilsch V., Reymann K.G., Riedel G. Physiological and pharmacological profile of trans-azetidine 2,4-dicarboxylic acid: metabotropic glutamate receptor agonism and effects on long-term potentiation. Neuroscience 1996, 72:999-1008.
30. Manahan-Vaughan D., Braunewell K.H., Reymann K.G. Subtype-specific involvement of metabotropic glutamate receptors in two forms of long-term potentiation in the dentate gyrus of freely moving rats. Neuroscience 1998, 86(3):709-721.
31. Martin S.J., Morris R.G. New life in an old idea: the synaptic plasticity and memory hypothesis revisited. Hippocampus 2002, 12(5):609-636.
32. Martin S.J., Grimwood P.D., Morris R.G. Synaptic plasticity and memory: an evaluation of the hypothesis. Annu Rev Neurosci 2000, 23:649-711.
33. Mehta M.R. Cooperative LTP can map memory sequences on dendritic branches. Trends Neurosci 2004, 27:69-72.
34. 2+ channels in NMDA receptor-independent synaptic plasticity and spatial memory. J Neurosci 2005, 25(43):9883-9892.
35. Morgan S.L., Teyler T.J. VDCCs and NMDARs underlie two forms of LTP in CA1 hippocampus in vivo. J Neurophysiol 1999, 82(2):736-740.
36. Mukherjee S., Manahan-Vaughan D. Role of metabotropic glutamate receptors in persistent forms of hippocampal plasticity and learning. Neuropharmacology 2013, 66:65-81.
37. Nakashiba T., Young J.Z., McHugh T.J., Buhl D.L., Tonegawa S. Transgenic inhibition of synaptic transmission reveals role of CA3 output in hippocampal learning. Science 2008, 319(5867):1260-1264.
38. Nicoll R.A., Malenka R.C. Expression mechanisms underlying NMDA receptor-dependent long-term potentiation. Ann N Y Acad Sci 1999, 868:515-525.
39. Pöschel B., Manahan-Vaughan D. Persistent (>24h) long-term depression in the dentate gyrus of freely moving rats is not dependent on activation of NMDA receptors, L-type voltage-gated calcium channels or protein synthesis. Neuropharmacology 2007, 52:46-54.
40. Remondes M., Schuman E.M. Direct cortical input modulates plasticity and spiking in CA1 pyramidal neurons. Nature 2002, 416(6882):736-740.
41. Remondes M., Schuman E.M. Molecular mechanisms contributing to long-lasting synaptic plasticity at the temporoammonic-CA1 synapse. Learn Mem 2003, 10(4):247-252.
42. Remondes M., Schuman E.M. Role for a cortical input to hippocampal area CA1 in the consolidation of a long-term memory. Nature 2004, 431(7009):699-703.
43. Shigemoto R., Kinoshita A., Wada E., Nomura S., Ohishi H., Takada M., Flor P.J., Neki A., Abe T., Nakanishi S., et al. Differential presynaptic localization of metabotropic glutamate receptor subtypes in the rat hippocampus. J Neurosci 1997, 17(19):7503-7522.
44. Speed H.E., Dobrunz L.E. Developmental changes in short-term facilitation are opposite at temporoammonic synapses compared to Schaffer collateral synapses onto CA1 pyramidal cells. Hippocampus 2009, 19(2):187-204.
45. Suh J., Rivest A.J., Nakashiba T., Tominaga T., Tonegawa S. Entorhinal cortex layer III input to the hippocampus is crucial for temporal association memory. Science 2011, 334(6061):1415-1420.
46. Witter M.P., Griffioen A.W., Jorritsma-Byham B., Krijnen J.L. Entorhinal projections to the hippocampal CA1 region in the rat: an underestimated pathway. Neurosci Lett 1988, 85(2):193-198.
47. Woodside B.L., Borroni A.M., Hammonds M.D., Teyler T.J. NMDA receptors and voltage-dependent calcium channels mediate different aspects of acquisition and retention of a spatial memory task. Neurobiol Learn Mem 2004, 81(2):105-114.