Timing and balance of inhibition enhance the effect of long-term potentiation on cell firing

Journal of Neuroscience

Volumn 24, Issue 40, 2004, Pages 8873-8884

  Marder, Carrie P ^a   Buonomano, Dean V ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

CA1; EPSP spike potentiation; Hippocampus; Inhibition; Input output; Long term potentiation; Network

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR;

ANIMAL CELL; ARTICLE; BRAIN SLICE; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; HIPPOCAMPUS; INHIBITORY POSTSYNAPTIC POTENTIAL; LEARNING; LONG TERM POTENTIATION; MEMORY; NERVE CELL PLASTICITY; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT;

ACTION POTENTIALS; ANIMALS; CELLS, CULTURED; COMPUTER SIMULATION; EXCITATORY POSTSYNAPTIC POTENTIALS; HIPPOCAMPUS; KINETICS; LONG-TERM POTENTIATION; MODELS, NEUROLOGICAL; NEURAL INHIBITION; PYRAMIDAL CELLS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GABA-A;

EID: 5444248035     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2661-04.2004     Document Type: Article

References (71)

1. Abraham WC, Bliss TVP, Goddard GV (1985) Heterosynaptic changes accompany long-term but not short-term potentiation of the perforant path in the anaesthetized rat. J Physiol (Lond) 363:335-349.
2. Abraham WC, Gustafsson B, Wigstrom H (1987) Long-term potentiation involves enhanced synaptic excitation relative to synaptic inhibition in guinea-pig hippocampus. J Physiol (Lond) 394:367-380.
3. Andersen P, Sundberg SH, Sveen O, Swann JW, Wigstrom H (1980) Possible mechanisms for long-lasting potentiation of synaptic transmission in hippocampal slices from guinea pigs. J Physiol (Lond) 302:463-482.
4. Bliss TV, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31-39.
5. Bliss TVP, Gardner-Medwin AR (1973) Long-lasting potentiation of synaptic transmission in the dentate area of the unanaesthetized rabbit following stimulation of the perforant path. J Physiol (Lond) 232:357-374.
6. Bliss TVP, Lomo T (1973) Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol (Lond) 232:331-356.
7. Brown TH, Fricke RA, Perkel DH (1981) Passive electrical constants in three classes of hippocampal neurons. J Neurophysiol 46:812-827.
8. Brown TH, Kairiss EW, Keenan CL (1990) Hebbian synapses: biophysical mechanisms and algorithms. Annu Rev Neurosci 13:475-511.
9. Buonomano DV (1999) Distinct functional types of associative long-term potentiation in neocortical and hippocampal pyramidal neurons. J Neurosci 19:6748-6754.
10. Buonomano DV (2000) Decoding temporal information: a model based on short-term synaptic plasticity. J Neurosci 20:1129-1141.
11. Buonomano DV, Merzenich MM (1996) Associative synaptic plasticity in hippocampal CA1 neurons is not sensitive to unpaired presynaptic activity. J Neurophysiol 76:631-636.
12. Buonomano DV, Merzenich MM (1998) Net interaction between different forms of short-term synaptic plasticity and slow-IPSPs in the hippocampus and auditory cortex. J Neurophysiol 80:1765-1774.
13. Buzsáki G (1984) Feed-forward inhibition in the hippocampal formation. Prog Neurobiol 22:131-153.
14. Chavez-Noriega LE, Bliss TVP, Halliwell JV (1989) The EPSP-spike (E-S) component of long-term potentiation in the rat hippocampal slice is modulated by GABAergic but not cholinergic mechanisms. Neurosci Lett 104:58-64.
15. Chevaleyre V, Castillo PE (2003) Heterosynaptic LTD of hippocampal GABAergic synapses: a novel role of endocannabinoids in regulating excitability. Neuron 38:461-472.
16. Collinson N, Kuenzi FM, Jarolimek W, Maubach KA, Cothliff R, Sur C, Smith A, Out FM, Howell O, Atack JR, McKernan RM, Seabrook GR, Dawson GR, Whiting PJ, Rosahl TW (2002) Enhanced learning and memory and altered GABAergic synaptic transmission in mice lacking the alpha 5 sub-unit of the GABAA receptor. J Neurosci 22:5572-5580.
17. Cowan AI, Stricker C, Reece LJ, Redman SJ (1998) Long-term plasticity at excitatory synapses on aspinous interneurons in area CA1 lacks synaptic specificity. J Neurophysiol 79:13-20.
18. Crestani F, Keist R, Fritschy J-M, Benke D, Vogt K, Prut L, Bluthmann H, Mohler H, Rudolph U (2002) Trace fear conditioning involves hippocampal α5 GABAA receptors. Proc Natl Acad Sci USA 99:8980-8985.
19. Crook JM, Eysel UT (1992) GABA-induced inactivation of functionally characterized sites in cat visual cortex (Area 18): effects on orientation tuning. J Neurosci 12:1816-1825.
20. Daoudal G, Debanne D (2003) Long-term plasticity of intrinsic excitability: learning rules and mechanisms. Learn Mem 10:456-465.
21. Daoudal G, Hanada Y, Debanne D (2002) Bidirectional plasticity of excitatory postsynaptic potential (EPSP)-spike coupling in CA1 hippocampal pyramidal neurons. Proc Natl Acad Sci USA 99:14512-14517.
22. Davies CH, Davies SN, Collingridge GL (1990) Paired-pulse depression of monosynaptic GABA-mediated inhibitory postsynaptic responses in rat hippocampus. J Physiol (Lond) 424:513-531.
23. Davies SN, Collingridge GL (1989) Role of excitatory amino acid receptors in synaptic transmission in area CA1 of rat hippocampus. Proc R Soc Lond B Biol Sci 236:373-384.
24. Destexhe A, Mainen ZF, Sejnowski TJ (1994) An efficient method for computing synaptic conductances based on a kinetic model of receptor binding. Neural Comput 6:14-18.
25. Evans MS, Viola-McCabe KE (1996) Midazolam inhibits long-term potentiation through modulation of GABAA receptors. Neuropharmacology 35:347-357.
26. Feldman DE (2000) Timing-based LTP and LTD at vertical inputs to layer II/III pyramidal cells in rat barrel cortex. Neuron 27:45-56.
27. Frick A, Magee J, Johnston D (2004) LTP is accompanied by an enhanced local excitability of pyramidal neuron dendrites. Nat Neurosci 7:126-135.
28. Fricker D, Miles R (2000) EPSP amplification and the precision of spike timing in hippocampal neurons. Neuron 28:559-569.
29. Gaiarsa J-L, Caillard O, Ben-Ari Y (2002) Long-term plasticity at GABAergic and glycinergic synapses: mechanisms and functional significance. Trends Neurosci 25:564-570.
30. Galarreta M, Hestrin S (1998) Frequency-dependent synaptic depression and the balance of excitation and inhibition in the neocortex. Nat Neurosci 1:587-594.
31. Hebb DO (1949) The organization of behavior: a neuropsychological theory. New York: Wiley.
32. Hines ML, Moore JW (1997) Computer simulations with NEURON. http://neuron.duke.edu/.
33. Jester JM, Campbell LW, Sejnowski TJ (1995) Associative EPSP-spike potentiation induced by pairing orthodromic and antidromic stimulation in rat hippocampal slices. J Physiol (Lond) 484 3:689-705.
34. Kairiss EW, Abraham WC, Bilkey DK, Goddard GV (1987) Field potential evidence for long-term potentiation of feed-forward inhibition in the rat dentate gyrus. Brain Res 401:87-94.
35. Karnup S, Stelzer A (1999) Temporal overlap of excitatory and inhibitory afferent input in guinea-pig CA1 pyramidal cells. J Physiol (Lond) 516 2:485-504.
36. Lacaille J-C, Mueller AL, Kunkel DD, Schwartzkroin PA (1987) Local circuit interactions between oriens/alveus interneurons and CA1 pyramidal cells in hippocampal slices: electrophysiology and morphology. J Neurosci 7:1979-1993.
37. Leung LS, Au AS (1994) Long-term potentiation as a function of test pulse intensity: a study using input/output profiles. Brain Res Bull 33:453-460.
38. Lu YM, Mansuy IM, Kandel ER, Roder J (2000) Calcineurin-mediated LTD of GABAergic inhibition underlies the increased excitability of CA1 neurons associated with LTP. Neuron 26:197-205.
39. Maccaferri G, McBain CJ (1996) Long-term potentiation in distinct subtypes of hippocampal nonpyramidal neurons. J Neurosci 16:5334-5343.
40. Malenka RC, Nicoll RA (1999) Long-term potentiation - a decade of progress? Science 285:1870-1874.
41. Marder CM, Buonomano DV (2003) Differential effects of short-and long-term potentiation on cell firing in the CA1 region of the hippocampus. J Neurosci 23:112-121.
42. Marshall L, Henze DA, Hirase H, Leinekugel X, Dragoi G, Buzsaki G (2002) Hippocampal pyramidal cell-interneuron spike transmission is frequency dependent and responsible for place modulation of interneuron discharge. J Neurosci 22:RC197(1-5).
43. Martin SJ, Grimwood PD, Morris RGM (2000) Synaptic plasticity and memory: an evaluation of the hypothesis. Annu Rev Neurosci 23:649-711.
44. McBain CJ, Maccaferri G (1997) Synaptic plasticity in hippocampal interneurons? A commentary. Can J Physiol Pharmacol 75:488-494.
45. McBain CJ, Freund TF, Mody I (1999) Glutamatergic synapses onto hippocampal interneurons: precision timing without lasting plasticity. Trends Neurosci 22:228-235.
46. McCormick D, Wang Z, Huguenard J (1993) Neurotransmitter control of neocortical neuronal activity and excitability. Cereb Cortex 3:387-398.
47. McLean H, Caillard O, Ben-Ari Y, Gaiarsa J-L (1996) Bidirectional plasticity expressed by GABAergic synpases in the neonatal rat hippocampus. J Physiol (Lond) 496 2:471-477.
48. McMahon LL, Kauer JA (1997) Hippocampal interneurons express a novel form of synaptic plasticity. Neuron 18:295-305.
49. Miles R (1990) Variation in strength of inhibitory synapses in the CA3 region of guinea-pig hippocampus in vitro. J Physiol (Lond) 431:659-676.
50. Ouardouz M, Lacaille J-C (1995) Mechanisms of selective long-term potentiation of excitatory synapses in stratum oriens/alveus interneurons of rat hippocampal slices. J Neurophysiol 73:810-819.
51. Perez Y, Morin F, Lacaille J-C (2001) A hebbian form of long-term potentiation dependent on mGluR1a in hippocampal inhibitory interneurons. Proc Natl Acad Sci USA 98:9401-9406.
52. Pouille F, Scanziani M (2001) Enforcement of temporal fidelity in pyramidal cells by somatic feed-forward inhibition. Science 293:1159-1163.
53. Roepstorff A, Lambert JDC (1994) Factors contributing to the decay of the stimulus-evoked IPSC in rat hippocampal CA1 neurons. J Neurophysiol 72:2911-2926.
54. Shapley R, Hawken M, Ringach DL (2003) Dynamics of orientation selectivity in the primary visual cortex and the importance of cortical inhibition. Neuron 38:689-699.
55. Shew T, Yip S, Sastry BR (2000) Mechanisms involved in tetanus-induced potentiation of fast IPSCs in rat hippocampal CA1 neurons. J Neurophysiol 83:3388-3401.
56. Sillito AM (1975) The contribution of inhibitory mechanisms to the receptive field properties of neurons in the striate cortex of the cat. J Physiol (Lond) 250:305-329.
57. Sourdet V, Russier M, Daoudal G, Ankri N, Debanne D (2003) Long-term enhancement of neuronal excitability and temporal fidelity mediated by metabotropic glutamate receptor subtype 5. J Neurosci 23:10238-10248.
58. Spruston N, Johnston D (1992) Perforated patch-clamp analysis of the passive membrane properties of three classes of hippocampal neurons. J Neurophysiol 67:508-529.
59. Staff NP, Spruston N (2003) Intracellular correlate of EPSP-spike potentiation in CA1 pyramidal neurons is controlled by GABAergic modulation. Hippocampus 13:801-805.
60. Stelzer A, Simon G, Kovacs G, Rai R (1994) Synaptic disinhibition during maintenance of long-term potentiation in the CA1 hippocampal subfield. Proc Natl Acad Sci USA 91:3058-3062.
61. Taube JS, Schwartzkroin PA (1988) Mechanisms of long-term potentiation: EPSP/spike dissociation, intradendritic recordings, and glutamate sensitivity. J Neurosci 8:1632-1644.
62. Tomasulo RA, Levy WB, Steward O (1991) LTP-associated EPSP/spike dissociation in the dentate gyrus: GABAergic and non-GABAergic components. Brain Res 561:27-34.
63. von der Malsburg C (1973) Self-organization of orientation sensitive cells in the striate cortex. Kybernetik 14:84-100.
64. Wang Z, Xu NI, Wu CP, Duan S, Poo MM (2003) Bidirectional changes in spatial dendritic integration accompanying long-term synaptic modifications. Neuron 37:463-472.
65. Wathey JC, Lytton WW, Jester JM, Sejnowski TJ (1992) Computer simulations of EPSP-spike (E-S) potentiation in hippocampal CA1 pyramidal cells. J Neurosci 12:607-618.
66. Wehr M, Zador AM (2003) Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature 426:442-446.
67. Wigstrom H, Gustafsson B (1985) Facilitation of hippocampal long-lasting potentiation by GABA antagonists. Acta Physiol Scand 125:159-172.
68. Wilson RC, Levy WB, Steward O (1981) Changes in translation of synaptic excitation to dentate granule cell discharge accompanying long-term potentiation. II. An evaluation of mechanisms utilizing dentate gyrus dually innervated by surviving ipsilateral and sprouted crossed temporodentate inputs. J Neurophysiol 46:339-355.
69. Xie Z, Yip S, Morishita W, Sastry BR (1995) Tetanus-induced potentiation of inhibitory postsynaptic potentials in hippocampal CA1 neurons. Can J Physiol Pharmacol 73:1706-1713.
70. Zhang L, Weiner JL, Carlen PL (1993) Potentiation of γ-aminobutyric acid type A receptor-mediated synaptic currents by pentobarbital and diazepam in immature hippocampal CA1 neurons. J Pharmacol Exp Ther 266:1227-1235.
71. Zhang W, Linden DJ (2003) The other side of the engram: experience-driven changes in neuronal intrinsic excitability. Nat Rev Neurosci 4:885-900.