Cholinergic modulation of excitatory synaptic input integration in hippocampal CA1

Journal of Physiology

Volumn 588, Issue 19, 2010, Pages 3727-3742

  McQuiston, A Rory ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID B RECEPTOR; 4 AMINOBUTYRIC ACID B RECEPTOR BLOCKING AGENT; ACETYLCHOLINE; ATROPINE; BICUCULLINE; CARBACHOL; CGP 54626; CHOLINERGIC RECEPTOR; INWARDLY RECTIFYING POTASSIUM CHANNEL; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CHANNEL GATING; CHOLINERGIC STIMULATION; CONTROLLED STUDY; ENTORHINAL CORTEX; EXCITATORY POSTSYNAPTIC POTENTIAL; HIPPOCAMPUS; NEUROMODULATION; NONHUMAN; PERFORANT NERVE TRACT; PREPULSE INHIBITION; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; RECEPTOR UPREGULATION; SYNAPTIC TRANSMISSION; THETA RHYTHM; ACTION POTENTIAL; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; CHOLINERGIC ACTIVITY; DEPOLARIZATION; ELECTROSTIMULATION; EXCITATION; EXCITATORY POSTSYNAPTIC POTENTIAL SUMMATION; FIELD EXCITATORY POSTSYNAPTIC POTENTIAL; FIRING RATE; HIPPOCAMPAL CA1 REGION; HIPPOCAMPUS THETA RHYTHM; MALE; POSITIVE FEEDBACK; SCHAFFER COLLATERAL PATHWAY; SPRAGUE DAWLEY RAT; STRATUM LACUNOSUM MOLECULARE; STRATUM RADIATUM; VOLTAGE SENSITIVE DYE IMAGING; WHOLE CELL PATCH CLAMP; YOUNG ADULT;

ACTION POTENTIALS; ANIMALS; CA1 REGION, HIPPOCAMPAL; CARBACHOL; COLORING AGENTS; ELECTROPHYSIOLOGICAL PHENOMENA; EVOKED POTENTIALS; EXCITATORY POSTSYNAPTIC POTENTIALS; EXTRACELLULAR MATRIX; GABA AGONISTS; GABA ANTAGONISTS; MALE; MUSCARINIC AGONISTS; ORGANOPHOSPHORUS COMPOUNDS; PARASYMPATHETIC NERVOUS SYSTEM; PATCH-CLAMP TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, CHOLINERGIC; RECEPTORS, GABA-B; STARTLE REACTION;

EID: 77957283217     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2010.188581     Document Type: Article

References (51)

1. Alkondon M, Albuquerque EX. Nicotinic acetylcholine receptor a7 and a4b2 subtypes differentially control GABAergic input to CA1 neurons in rat hippocampus. J Neurophysiol 2001, 86:3043-3055.
2. Alkondon M, Pereira EF, Albuquerque EX. α-Bungarotoxin- and methyllycaconitine-sensitive nicotinic receptors mediate fast synaptic transmission in interneurons of rat hippocampal slices. Brain Res 1998, 810:257-263.
3. Alkondon M, Pereira EF, Barbosa CT, Albuquerque EX. Neuronal nicotinic acetylcholine receptor activation modulates γ-aminobutyric acid release from CA1 neurons of rat hippocampal slices. J Pharmacol Exp Ther 1997, 283:1396-1411.
4. Andrade R. Blockade of neurotransmitter-activated K+ conductance by QX-314 in the rat hippocampus. Eur J Pharmacol 1991, 199:259-262.
5. Ang CW, Carlson GC, Coulter DA. Hippocampal CA1 circuitry dynamically gates direct cortical inputs preferentially at theta frequencies. J Neurosci 2005, 25:9567-9580.
6. Behrends JC, 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 1993, 69:626-629.
7. Buhler AV, Dunwiddie TV. Regulation of the activity of hippocampal stratum oriens interneurons by a7 nicotinic acetylcholine receptors. Neuroscience 2001, 106:55-67.
8. Buzsaki G. Theta oscillations in the hippocampus. Neuron 2002, 33:325-340.
9. Chrobak JJ, Buzsaki G. Gamma oscillations in the entorhinal cortex of the freely behaving rat. J Neurosci 1998, 18:388-398.
10. Cole AE, Nicoll RA. Acetylcholine mediates a slow synaptic potential in hippocampal pyramidal cells. Science 1983, 221:1299-1301.
11. Cole AE, Nicoll RA. Characterization of a slow cholinergic post-synaptic potential recorded in vitro from rat hippocampal pyramidal cells. J Physiol 1984a, 352:173-188.
12. Cole AE, Nicoll RA. The pharmacology of cholinergic excitatory responses in hippocampal pyramidal cells. Brain Res 1984b, 305:283-290.
13. Drummond GB. Reporting ethical matters in The Journal of Physiology: standards and advice. J Physiol 2009, 587:713-719.
14. Dudman JT, Tsay D, Siegelbaum SA. A role for synaptic inputs at distal dendrites: instructive signals for hippocampal long-term plasticity. Neuron 2007, 56:866-879.
15. Dvorak-Carbone H, Schuman EM. Patterned activity in stratum lacunosum moleculare inhibits CA1 pyramidal neuron firing. J Neurophysiol 1999, 82:3213-3222.
16. Empson RM, Heinemann U. The perforant path projection to hippocampal area CA1 in the rat hippocampal-entorhinal cortex combined slice. J Physiol 1995, 484:707-720.
17. Enoki R, Inoue M, Hashimoto Y, Kudo Y, Miyakawa H. GABAergic control of synaptic summation in hippocampal CA1 pyramidal neurons. Hippocampus 2001, 11:683-689.
18. Enoki R, Namiki M, Kudo Y, Miyakawa H. Optical monitoring of synaptic summation along the dendrites of CA1 pyramidal neurons. Neuroscience 2002, 113:1003-1014.
19. Frank LM, Brown EN, Wilson MA. A comparison of the firing properties of putative excitatory and inhibitory neurons from CA1 and the entorhinal cortex. J Neurophysiol 2001, 86:2029-2040.
20. Fraser DD, MacVicar BA. Cholinergic-dependent plateau potential in hippocampal CA1 pyramidal neurons. J Neurosci 1996, 16:4113-4128.
21. Frazier CJ, Buhler AV, Weiner JL, Dunwiddie TV. Synaptic potentials mediated via α-bungarotoxin-sensitive nicotinic acetylcholine receptors in rat hippocampal interneurons. J Neurosci 1998a, 18:8228-8235.
22. Frazier CJ, Rollins YD, Breese CR, Leonard S, Freedman R, Dunwiddie TV. Acetylcholine activates an a-bungarotoxin-sensitive nicotinic current in rat hippocampal interneurons, but not pyramidal cells. J Neurosci 1998b, 18:1187-1195.
23. Hajos N, Papp EC, Acsady L, Levey AI, Freund TF. Distinct interneuron types express m2 muscarinic receptor immunoreactivity on their dendrites or axon terminals in the hippocampus. Neuroscience 1998, 82:355-376.
24. Hasselmo ME. What is the function of hippocampal theta rhythm?- Linking behavioral data to phasic properties of field potential and unit recording data. Hippocampus 2005, 15:936-949.
25. Hasselmo ME, Schnell E. Laminar selectivity of the cholinergic suppression of synaptic transmission in rat hippocampal region CA1: computational modeling and brain slice physiology. J Neurosci 1994, 14:3898-3914.
26. Hounsgaard J. Presynaptic inhibitory action of acetylcholine in area CA1 of the hippocampus. Exp Neurol 1978, 62:787-797.
27. Jarsky T, Roxin A, Kath WL, Spruston N. Conditional dendritic spike propagation following distal synaptic activation of hippocampal CA1 pyramidal neurons. Nat Neurosci 2005, 8:1667-1676.
28. Jones S, Yakel JL. Functional nicotinic ACh receptors on interneurones in the rat hippocampus. J Physiol 1997, 504:603-610.
29. Judge SJ, Hasselmo ME. Theta rhythmic stimulation of stratum lacunosum-moleculare in rat hippocampus contributes to associative LTP at a phase offset in stratum radiatum. J Neurophysiol 2004, 92:1615-1624.
30. Keita MS, Frankel-Kohn L, Bertrand N, Lecanu L, Monmaur P. Acetylcholine release in the hippocampus of the urethane anaesthetised rat positively correlates with both peak theta frequency and relative power in the theta band. Brain Res 2000, 887:323-334.
31. Lawrence JJ, Statland JM, Grinspan ZM, McBain CJ. Cell type-specific dependence of muscarinic signalling in mouse hippocampal stratum oriens interneurones. J Physiol 2006, 570:595-610.
32. Lee MG, Chrobak JJ, Sik A, Wiley RG, Buzsaki G. Hippocampal theta activity following selective lesion of the septal cholinergic system. Neuroscience 1994, 62:1033-1047.
33. Maccaferri G, McBain CJ. Passive propagation of LTD to stratum oriens-alveus inhibitory neurons modulates the temporoammonic input to the hippocampal CA1 region. Neuron 1995, 15:137-145.
34. McQuiston AR, Madison DV. Nicotinic receptor activation excites distinct subtypes of interneurons in the rat hippocampus. J Neurosci 1999a, 19:2887-2896.
35. McQuiston AR, Madison DV. Muscarinic receptor activity has multiple effects on the resting membrane potentials of CA1 hippocampal interneurons. J Neurosci 1999b, 19:5693-5702.
36. McQuiston AR, Madison DV. Muscarinic receptor activity induces an afterdepolarization in a subpopulation of hippocampal CA1 interneurons. J Neurosci 1999c, 19:5703-5710.
37. Mann EO, Tominaga T, Ichikawa M, Greenfield SA. Cholinergic modulation of the spatiotemporal pattern of hippocampal activity in vitro. Neuropharmacology 2005, 48:118-133.
38. Marrosu F, Portas C, Mascia MS, Casu MA, Fa M, Giagheddu M, Imperato A, Gessa GL. Microdialysis measurement of cortical and hippocampal acetylcholine release during sleep-wake cycle in freely moving cats. Brain Res 1995, 671:329-332.
39. Monmaur P, Collet A, Puma C, Frankel-Kohn L, Sharif A. Relations between acetylcholine release and electrophysiological characteristics of theta rhythm: a microdialysis study in the urethane-anesthetized rat hippocampus. Brain Res Bull 1997, 42:141-146.
40. O'Keefe J, Dostrovsky J. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res 1971, 34:171-175.
41. O'Keefe J, Recce ML. Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 1993, 3:317-330.
42. Parra P, Gulyas AI, Miles R. How many subtypes of inhibitory cells in the hippocampus?. Neuron 1998, 20:983-993.
43. Pitler TA, Alger BE. Cholinergic excitation of GABAergic interneurons in the rat hippocampal slice. J Physiol 1992, 450:127-142.
44. Remondes M, Schuman EM. Direct cortical input modulates plasticity and spiking in CA1 pyramidal neurons. Nature 2002, 416:736-740.
45. Skaggs WE, McNaughton BL, Wilson MA, Barnes CA. Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus 1996, 6:149-172.
46. Sudweeks SN, Yakel JL. Functional and molecular characterization of neuronal nicotinic ACh receptors in rat CA1 hippocampal neurons. J Physiol 2000, 527:515-528.
47. Takahashi H, Magee JC. Pathway interactions and synaptic plasticity in the dendritic tuft regions of CA1 pyramidal neurons. Neuron 2009, 62:102-111.
48. Tsubokawa H, Ross WN. Muscarinic modulation of spike backpropagation in the apical dendrites of hippocampal CA1 pyramidal neurons. J Neurosci 1997, 17:5782-5791.
49. Valentino RJ, Dingledine R. Presynaptic inhibitory effect of acetylcholine in the hippocampus. J Neurosci 1981, 1:784-792.
50. Widmer H, Ferrigan L, Davies CH, Cobb SR. Evoked slow muscarinic acetylcholinergic synaptic potentials in rat hippocampal interneurons. Hippocampus 2006, 16:617-628.
51. Wouterlood FG, Saldana E, Witter MP. Projection from the nucleus reuniens thalami to the hippocampal region: light and electron microscopic tracing study in the rat with the anterograde tracer Phaseolus vulgaris-leucoagglutinin. J Comp Neurol 1990, 296:179-203.