Contribution of Ih and GABAB to synaptically induced afterhyperpolarizations in CA1: A brake on the NMDA response

Journal of Neurophysiology

Volumn 92, Issue 4, 2004, Pages 2027-2039

  Otmakhova, Nonna A ^a   Lisman, John E ^a  

^a BRANDEIS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 HYDROXYSACLOFEN; 4 (N ETHYL N PHENYLAMINO) 1,2 DIMETHYL 6 (METHYLAMINO)PYRIMIDINIUM CHLORIDE; 4 AMINOBUTYRIC ACID B RECEPTOR; ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; CALCIUM ION; N METHYL DEXTRO ASPARTIC ACID; 2-HYDROXYSACLOFEN; 4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID RECEPTOR BLOCKING AGENT; BACLOFEN; CALCIUM; DRUG DERIVATIVE; ICI D2788; ION CHANNEL; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PICROTOXIN; POTASSIUM CHANNEL; POTASSIUM CHANNEL BLOCKING AGENT; PYRIMIDINE DERIVATIVE;

AFTERHYPERPOLARIZATION; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CALCIUM MOBILIZATION; EXCITATORY POSTSYNAPTIC POTENTIAL; GABAERGIC SYSTEM; HIPPOCAMPUS; NEUROMODULATION; NONHUMAN; PRESYNAPTIC INHIBITION; PRIORITY JOURNAL; RAT; ANIMAL; CYTOLOGY; DRUG EFFECT; ELECTROPHYSIOLOGY; IN VITRO STUDY; LONG EVANS RAT; PATCH CLAMP; PERFORANT NERVE TRACT; PHYSIOLOGY; SYNAPSE;

ANIMALS; BACLOFEN; CALCIUM; ELECTROPHYSIOLOGY; EXCITATORY POSTSYNAPTIC POTENTIALS; GABA ANTAGONISTS; HIPPOCAMPUS; ION CHANNELS; PATCH-CLAMP TECHNIQUES; PERFORANT PATHWAY; PICROTOXIN; POTASSIUM CHANNEL BLOCKERS; POTASSIUM CHANNELS; PYRIMIDINES; RATS; RATS, LONG-EVANS; RECEPTORS, GABA-A; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPSES;

EID: 4644323652     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.00427.2004     Document Type: Article

References (84)

1. Abbott LF and Blum KI. Functional significance of long-term potentiation for sequence learning and prediction. Cereb Cortex 6: 406-416, 1996.
2. Adam TJ, Finlayson PG, and Schwarz DW. Membrane properties of principal neurons of the lateral superior olive. J Neurophysiol 86: 922-934, 2001.
3. Andrasfalvy BK and Magee JC. Distance-dependent increase in AMPA receptor number in the dendrites of adult hippocampal CA1 pyramidal neurons. J Neurosci 21: 9151-9159, 2001.
4. Andreasen M and Lambert JD. Factors determining the efficacy of distal excitatory synapses in rat hippocampal CA1 pyramidal neurones. J Physiol 507: 441-462, 1998.
5. Andreasen M and Lambert JD. Somatic amplification of distally generated subthreshold EPSPs in rat hippocampal pyramidal neurones. J Physiol 519: 85-100, 1999.
6. Ault B and Nadler JV. Baclofen selectively inhibits transmission at synapses made by axons of CA3 pyramidal cells in the hippocampal slice. J Pharmacol Exp Ther 223: 291-297, 1982.
7. Bal T and McCormick DA. Synchronized oscillations in the inferior olive are controlled by the hyperpolarization-activated cation current I(h). J Neurophysiol 77: 3145-3156, 1997.
8. Behrends JC and ten Bruggencate G. Cholinergic modulation of synaptic inhibition in the guinea pig hippocampus in vitro: excitation of GABAergic interneurons and inhibition of GABA-release. J Neurophysiol 69: 626-629, 1993.
9. Benardo LS, Masukawa LM, and Prince DA. Electrophysiology of isolated hippocampal pyramidal dendrites. J Neurosci 2: 1614-1622, 1982.
10. Burgess N, Becker S, King JA, and O'Keefe J. Memory for events and their spatial context: models and experiments. Philos Trans R Soc Lond B Biol Sci 356: 1493-1503, 2001.
11. Burgess N, Maguire EA, and O'Keefe J. The human hippocampus and spatial and episodic memory. Neuron 35: 625-641, 2002.
12. Carnevale NT and Johnston D. Electrophysiological characterization of remote chemical synapses. J Neurophysiol 47: 606-621, 1982.
13. Cash S and Yuste R. Linear summation of excitatory inputs by CA1 pyramidal neurons. Neuron 22: 383-394, 1999.
14. Chapman CA and Lacaille JC. Intrinsic theta-frequency membrane potential oscillations in hippocampal CA1 interneurons of stratum lacunosum-moleculare. J Neurophysiol 81: 1296-1307, 1999.
15. Chevaleyre V and Castillo PE. Assessing the role of Ih channels in synaptic transmission and mossy fiber LTP. Proc Natl Acad Sci USA 99: 9538-9543, 2002.
16. Colbert CM and Levy WB. Electrophysiological and pharmacological characterization of perforant path synapses in CA1: mediation by glutamate receptors. J Neurophysiol 68: 1-8, 1992.
17. Connors BW and Prince DA. Effects of local anesthetic QX-314 on the membrane properties of hippocampal pyramidal neurons. J Pharmacol Exp Ther 220: 476-481, 1982.
18. Dvorak-Carbone H and Schuman EM. Patterned activity in stratum lacunosum moleculare inhibits CA1 pyramidal neuron firing. J Neurophysiol 82: 3213-3222, 1999.
19. Eichenbaum H. The hippocampus and declarative memory: cognitive mechanisms and neural codes. Behav Brain Res 127: 199-207, 2001.
20. Empson RM and Heinemann U. Perforant path connections to area CA1 are predominantly inhibitory in the rat hippocampal-entorhinal cortex combined slice preparation. Hippocampus 5: 104-107, 1995.
21. Funahashi M, Mitoh Y, and Matsuo R. Electrophysiological properties of the rat area postrema neurons displaying both the transient outward current and the hyperpolarization-activated inward current. Brain Res Bull 58: 337-343, 2002.
22. Gasparini S and DiFrancesco D. Action of the hyperpolarization-activated current (Ih) blocker ZD 7288 in hippocampal CA1 neurons. Pfluegers Arch 435: 99-106, 1997.
23. Golding NL and Spruston N. Dendritic sodium spikes are variable triggers of axonal action potentials in hippocampal CA1 pyramidal neurons. Neuron 21: 1189-1200, 1998.
24. Hasselmo ME and Schnell E. Laminar selectivity of the cholinergic suppression of synaptic transmission in rat hippocampal region CA1: computational modeling and brain slice physiology. J Neurosci 14: 3898-3914, 1994.
25. + channels in dendrites of hippocampal CA1 pyramidal neurons by activation of PKA and PKC. J Neurosci 18: 3521-3528, 1998.
26. + channel regulation of signal propagation in dendrites of hippocampal pyramidal neurons. Nature 387: 869-875, 1997.
27. Huerta PT and Lisman JE. Heightened synaptic plasticity of hippocampal CA1 neurons during a cholinergically induced rhythmic state. Nature 364: 723-725, 1993.
28. Huerta PT and Lisman JE. Synaptic plasticity during the cholinergic theta-frequency oscillation in vitro. Hippocampus 6: 58-61, 1996.
29. Isaacson JS, Solis JM, and Nicoll RA. Local and diffuse synaptic actions of GABA in the hippocampus. Neuron 10: 165-175, 1993.
30. Jones RS. Frequency-dependent alterations in synaptic transmission in entorhinal-hippocampal pathways. Hippocampus 5: 125-128, 1995.
31. Kepecs A and Raghavachari S. 3 state neurons for contextual processing. In: Advances in Neural Information Processing Systems, edited by Dietterich TG, Becker S, and Ghahnamani Z, 2002, p. 1-8.
32. Knierim JJ. Hippocampus and memory. Can we have our place and fear it too? Neuron 37: 372-374, 2003.
33. Koulakov AA, Raghavachari S, Kepecs A, and Lisman JE. Model for a robust neural integrator. Nat Neurosci 5: 775-782, 2002.
34. Kulik A, Vida I, Lujan R, Haas CA, Lopez-Bendito G, Shigemoto R, and Frotscher M. Subcellular localization of metabotropic GABA(B) receptor subunits GABA(B1a/b) and GABA(B2) in the rat hippocampus. J Neurosci 23: 11026-11035, 2003.
35. Lambert NA and Wilson WA. Discrimination of post- and presynaptic GABAB receptor-mediated responses by tetrahydroaminoacridine in area CA3 of the rat hippocampus. J Neurophysiol 69: 630-635, 1993.
36. Larkman PM and Kelly JS. Modulation of the hyperpolarisation-activated current, Ih, in rat facial motoneurones in vitro by ZD-7288. Neuropharmacology 40: 1058-1072, 2001.
37. Larkum ME, Zhu JJ, and Sakmann B. A new cellular mechanism for coupling inputs arriving at different cortical layers. Nature 398: 338-341, 1999.
38. Levy WB. A computational approach to hippocampal function. In: Computational Models of Learning in Simple Neural Systems, edited by Hawkins RD and Bower GH. New York: Academic Press, 1989, p. 243-305.
39. Lisman JE. Relating hippocampal circuitry to function: recall of memory sequences by reciprocal dentate-CA3 interactions. Neuron 22: 233-242, 1999.
40. Lisman JE and Otmakhova NA. 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 11: 551-568, 2001.
41. Lisman JE, Fellous JM, and Wang XJ. A role for NMDA-receptor channels in working memory. Nat Neurosci 1: 273-275, 1998.
42. Lupica CR, Bell JA, Hoffman AF, and Watson PL. Contribution of the hyperpolarization-activated current (I(h)) to membrane potential and GABA release in hippocampal interneurons. J Neurophysiol 86: 261-268, 2001.
43. MacLean JN, Zhang Y, Johnson BR, and Harris-Warrick RM. Activity-independent homeostasis in rhythmically active neurons. Neuron 37: 109-120, 2003.
44. Madison DV and Nicoll RA. Cyclic adenosine 3′,5′- monophosphate mediates beta-receptor actions of noradrenaline in rat hippocampal pyramidal cells. J Physiol 372: 245-259, 1986.
45. Magee JC. Dendritic hyperpolarization-activated currents modify the integrative properties of hippocampal CA1 pyramidal neurons. J Neurosci 18: 7613-7624, 1998.
46. Magee JC. Dendritic Ih normalizes temporal summation in hippocampal CA1 neurons. Nat Neurosci 2: 508-514, 1999.
47. Magee JC and Cook EP. Somatic EPSP amplitude is independent of synapse location in hippocampal pyramidal neurons. Nat Neurosci 3: 895-903, 2000.
48. Major G, Larkman AU, Jonas P, Sakmann B, and Jack JJ. Detailed passive cable models of whole-cell recorded CA3 pyramidal neurons in rat hippocampal slices. J Neurosci 14: 4613-4638, 1994.
49. Margulis M and Tang CM. Temporal integration can readily switch between sublinear and supralinear summation. J Neurophysiol 79: 2809-2813, 1998.
50. Mathie A, Wooltorton JR, and Watkins CS. Voltage-activated potassium channels in mammalian neurons and their block by novel pharmacological agents. Gen Pharmacol 30: 13-24, 1998.
51. Mel BW. Synaptic integration in an excitable dendritic tree. J Neurophysiol 70: 1086-1101, 1993.
52. Miyashita T and Kubo Y. Localization and developmental changes of the expression of two inward rectifying K(+)-channel proteins in the rat brain. Brain Res 750: 251-263, 1997.
53. Nettleton JS and Spain WJ. Linear to supralinear summation of AMPA-mediated EPSPs in neocortical pyramidal neurons. J Neurophysiol 83: 3310-3322, 2000.
54. Nicoll RA and Alger BE. Synaptic excitation may activate a calcium-dependent potassium conductance in hippocampal pyramidal cells. Science 212: 957-959, 1981.
55. Otmakhova NA and Lisman JE. Dopamine selectively inhibits the direct cortical pathway to the CA1 hippocampal region. J Neurosci 19: 1437-1445, 1999.
56. Otmakhova NA, Otmakhov N, and Lisman JE. Pathway-specific properties of AMPA and NMDA-mediated transmission in CA1 hippocampal pyramidal cells. J Neurosci 22: 1199-1207, 2002.
57. Otmakhova NA, Otmakhov N, Mortenson LH, and Lisman JE. Inhibition of the cAMP pathway decreases early long-term potentiation at CA1 hippocampal synapses. J Neurosci 20: 4446-4451, 2000.
58. Pape HC. Queer current and pacemaker: the hyperpolarization-activated cation current in neurons. Annu Rev Physiol 58: 299-327, 1996.
59. Patil MM and Hasselmo ME. Modulation of inhibitory synaptic potentials in the piriform cortex. J Neurophysiol 81: 2103-2118, 1999.
60. Pedarzani P and Storm JF. Protein kinase A-independent modulation of ion channels in the brain by cyclic AMP. Proc Natl Acad Sci USA 92: 11716-11720, 1995.
61. Perkins KL and Wong RK. Intracellular QX-314 blocks the hyperpolarization-activated inward current Iq in hippocampal CA1 pyramidal cells. J Neurophysiol 73: 911-915, 1995.
62. Pham TM, Nurse S, and Lacaille JC. Distinct GABAB actions via synaptic and extrasynaptic receptors in rat hippocampus in vitro. J Neurophysiol 80: 297-308, 1998.
63. Pitler TA and Alger BE. Cholinergic excitation of GABAergic interneurons in the rat hippocampal slice. J Physiol 450: 127-142, 1992.
64. Poirazi P, Brannon T, and Mel BW. Arithmetic of subthreshold synaptic summation in a model CA1 pyramidal cell. Neuron 37: 977-987, 2003.
65. Pongracz F, Poolos NP, Kocsis JD, and Shepherd GM. A model of NMDA receptor-mediated activity in dendrites of hippocampal CA1 pyramidal neurons. J Neurophysiol 68: 2248-2259, 1992.
66. Poolos NP and Johnston D. Calcium-activated potassium conductances contribute to action potential repolarization at the soma but not the dendrites of hippocampal CA1 pyramidal neurons. J Neurosci 19: 5205-5212, 1999.
67. Regehr W, Kehoe JS, Ascher P, and Armstrong C. Synaptically triggered action potentials in dendrites. Neuron 11: 145-151, 1993.
68. Satoh TO and Yamada M. A bradycardiac agent ZD7288 blocks the hyperpolarization-activated current (I(h)) in retinal rod photoreceptors. Neuropharmacology 39: 1284-1291, 2000.
69. Savic N, Pedarzani P, and Sciancalepore M. Medium afterhyperpolarization and firing pattern modulation in interneurons of stratum radiatum in the CA3 hippocampal region. J Neurophysiol 85: 1986-1997, 2001.
70. Schiller J and Schiller Y. NMDA receptor-mediated dendritic spikes and coincident signal amplification. Curr Opin Neurobiol 11: 343-348, 2001.
71. 2+ channels in the proximal versus distal dendrites to synaptic integration in prefrontal cortical neurons. J Neurosci 17: 5936-5948, 1997.
72. Sekirnjak C and du Lac S. Intrinsic firing dynamics of vestibular nucleus neurons. J Neurosci 22: 2083-2095, 2002.
73. + current and I(h) by an inhalational anaesthetic and neurotransmitters in rat brainstem motoneurones. J Physiol 541: 717-729, 2002.
74. Sloviter RS, Ali-Akbarian L, Elliott RC, Bowery BJ, and Bowery NG. Localization of GABA(B) (R1) receptors in the rat hippocampus by immunocytochemistry and high resolution autoradiography, with specific reference to its localization in identified hippocampal interneuron subpopulations. Neuropharmacology 38: 1707-1721, 1999.
75. Solis JM and Nicoll RA. Pharmacological characterization of GABAB-mediated responses in the CA1 region of the rat hippocampal slice. J Neurosci 12: 3466-3472, 1992a.
76. Solis JM and Nicoll RA. Postsynaptic action of endogenous GABA released by nipecotic acid in the hippocampus. Neurosci Lett 147: 16-20, 1992b.
77. Spruston N, Jaffe DB, Williams SH, and Johnston D. Voltage- and space-clamp errors associated with the measurement of electrotonically remote synaptic events. J Neurophysiol 70: 781-802, 1993.
78. Stuart G and Sakmann B. Amplification of EPSPs by axosomatic sodium channels in neocortical pyramidal neurons. Neuron 15: 1065-1076, 1995.
79. Suzuki WA. Declarative versus episodic: two theories put to the test. Neuron 38: 5-7, 2003.
80. Takigawa T and Alzheimer C. Interplay between activation of GIRK current and deactivation of Ih modifies temporal integration of excitatory input in CA1 pyramidal cells. J Neurophysiol 89: 2238-2244, 2003.
81. Talbot MJ and Sayer RJ. Intracellular QX-314 inhibits calcium currents in hippocampal CA1 pyramidal neurons. J Neurophysiol 76: 2120-2124, 1996.
82. Vinogradova O. Functional organization of the limbic system in the process of registration of information: facts and hypotheses. In: The Hippocampus, edited by Isaacson RL and Pribram KH. New York: Plenum Press, 1984, p. 1-69.
83. Williams SR and Stuart GJ. Site independence of EPSP time course is mediated by dendritic I(h) in neocortical pyramidal neurons. J Neurophysiol 83: 3177-3182, 2000.
84. Worley PF, Baraban JM, McCarren M, Snyder SH, and Alger BE. Cholinergic phosphatidylinositol modulation of inhibitory, G protein-linked neurotransmitter actions: electrophysiological studies in rat hippocampus. Proc Nail Acad Sci USA 84: 3467-3471, 1987.