Cholinergic afferent stimulation induces axonal function plasticity in adult hippocampal granule cells

Neuron

Volumn 85, Issue 2, 2015, Pages 346-363

  Martinello, Katiuscia ^a   Huang, Zhuo ^a   Lujan, Rafael ^b   Tran, Baouyen ^c   Watanabe, Masahiko ^d   Cooper, Edward C ^c   Brown, David A ^e   Shah, Mala M ^a  

^a UNIVERSITY OF LONDON   (United Kingdom)

^b UNIVERSITY OF CASTILLA LA MANCHA   (Spain)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

^d HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^e UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCHOLINE; CALCIUM CHANNEL CAV3.2; CALCIUM CHANNEL T TYPE; CALCIUM ION; MUSCARINIC M1 RECEPTOR; POTASSIUM CHANNEL KV7.2; POTASSIUM CHANNEL KV7.3; UNCLASSIFIED DRUG; VOLTAGE GATED CALCIUM CHANNEL; VOLTAGE GATED POTASSIUM CHANNEL; CACNA1H PROTEIN, MOUSE; CALCIUM; MUSCARINIC RECEPTOR; POTASSIUM; POTASSIUM CHANNEL KCNQ2; POTASSIUM CHANNEL KCNQ3;

ACTION POTENTIAL; ADULT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; CHOLINERGIC NERVE; CHOLINERGIC STIMULATION; CONTROLLED STUDY; DENTATE GYRUS; GRANULE CELL; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MALE; MOSSY FIBER; MOUSE; NERVE CELL PLASTICITY; NERVE EXCITABILITY; NERVE STIMULATION; NONHUMAN; PROTEIN LOCALIZATION; RAT; SENSORY NERVE; SYNAPTIC POTENTIAL; ANIMAL; CYTOLOGY; HIPPOCAMPAL MOSSY FIBER; METABOLISM; NERVE CELL; NERVE FIBER; PHYSIOLOGY; SENSORY NERVE CELL; SYNAPTIC TRANSMISSION;

ACETYLCHOLINE; ACTION POTENTIALS; ANIMALS; AXONS; CALCIUM; CALCIUM CHANNELS, T-TYPE; CHOLINERGIC FIBERS; DENTATE GYRUS; HIPPOCAMPUS; KCNQ2 POTASSIUM CHANNEL; KCNQ3 POTASSIUM CHANNEL; MICE; MOSSY FIBERS, HIPPOCAMPAL; NEURONAL PLASTICITY; NEURONS; NEURONS, AFFERENT; POTASSIUM; RECEPTOR, MUSCARINIC M1; RECEPTORS, MUSCARINIC; SYNAPTIC POTENTIALS; SYNAPTIC TRANSMISSION;

EID: 84921435641     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2014.12.030     Document Type: Article

References (47)

1. Acsády L., Káli S. Models, structure, function: the transformation of cortical signals in the dentate gyrus. Prog. Brain Res. 2007, 163:577-599.
2. Alkondon M., Pereira E.F., Wonnacott S., Albuquerque E.X. Blockade of nicotinic currents in hippocampal neurons defines methyllycaconitine as a potent and specific receptor antagonist. Mol. Pharmacol. 1992, 41:802-808.
3. Aznavour N., Watkins K.C., Descarries L. Postnatal development of the cholinergic innervation in the dorsal hippocampus of rat: Quantitative light and electron microscopic immunocytochemical study. J.Comp. Neurol. 2005, 486:61-75.
4. Battefeld A., Tran B.T., Gavrilis J., Cooper E.C., Kole M.H. Heteromeric Kv7.2/7.3 channels differentially regulate action potential initiation and conduction in neocortical myelinated axons. J.Neurosci. 2014, 34:3719-3732.
5. Bean B.P. The action potential in mammalian central neurons. Nat. Rev. Neurosci. 2007, 8:451-465.
6. Bender K.J., Ford C.P., Trussell L.O. Dopaminergic modulation of axon initial segment calcium channels regulates action potential initiation. Neuron 2010, 68:500-511.
7. Brazhnik E.S., Fox S.E. Action potentials and relations to the theta rhythm of medial septal neurons invivo. Exp. Brain Res. 1999, 127:244-258.
8. Brown D.A., Passmore G.M. Neural KCNQ (Kv7) channels. Br. J. Pharmacol. 2009, 156:1185-1195.
9. Buchanan K.A., Petrovic M.M., Chamberlain S.E., Marrion N.V., Mellor J.R. Facilitation of long-term potentiation by muscarinic M(1) receptors is mediated by inhibition of SK channels. Neuron 2010, 68:948-963.
10. Buzsáki G. Theta oscillations in the hippocampus. Neuron 2002, 33:325-340.
11. Catterall W.A. Voltage-gated calcium channels. Cold Spring Harb. Perspect. Biol. 2011, 3:a003947.
12. Cole A.E., Nicoll R.A. Acetylcholine mediates a slow synaptic potential in hippocampal pyramidal cells. Science 1983, 221:1299-1301.
13. Cooper E.C., Harrington E., Jan Y.N., Jan L.Y. M channel KCNQ2 subunits are localized to key sites for control of neuronal network oscillations and synchronization in mouse brain. J.Neurosci. 2001, 21:9529-9540.
14. Coulter D.A., Carlson G.C. Functional regulation of the dentate gyrus by GABA-mediated inhibition. Prog. Brain Res. 2007, 163:235-243.
15. Debanne D., Campanac E., Bialowas A., Carlier E., Alcaraz G. Axon physiology. Physiol. Rev. 2011, 91:555-602.
16. Devaux J.J., Kleopa K.A., Cooper E.C., Scherer S.S. KCNQ2 is a nodal K+ channel. J.Neurosci. 2004, 24:1236-1244.
17. Dreyfus F.M., Tscherter A., Errington A.C., Renger J.J., Shin H.S., Uebele V.N., Crunelli V., Lambert R.C., Leresche N. Selective T-type calcium channel block in thalamic neurons reveals channel redundancy and physiological impact of I(T)window. J.Neurosci. 2010, 30:99-109.
18. Falkenburger B.H., Dickson E.J., Hille B. Quantitative properties and receptor reserve of the DAG and PKC branch of G(q)-coupled receptor signaling. J.Gen. Physiol. 2013, 141:537-555.
19. Gamper N., Shapiro M.S. Regulation of ion transport proteins by membrane phosphoinositides. Nat. Rev. Neurosci. 2007, 8:921-934.
20. Grubb M.S., Burrone J. Building and maintaining the axon initial segment. Curr. Opin. Neurobiol. 2010, 20:481-488.
21. Gu Z., Yakel J.L. Timing-dependent septal cholinergic induction of dynamic hippocampal synaptic plasticity. Neuron 2011, 71:155-165.
22. Hasselmo M.E., Sarter M. Modes and models of forebrain cholinergic neuromodulation of cognition. Neuropsychopharmacology 2011, 36:52-73.
23. Henze D.A., Wittner L., Buzsáki G. Single granule cells reliably discharge targets in the hippocampal CA3 network invivo. Nat. Neurosci. 2002, 5:790-795.
24. Huang Z., Lujan R., Martinez-Hernandez J., Lewis A.S., Chetkovich D.M., Shah M.M. TRIP8b-independent trafficking and plasticity of adult cortical presynaptic HCN1 channels. J.Neurosci. 2012, 32:14835-14848.
25. Jones B.E. Activity, modulation and role of basal forebrain cholinergic neurons innervating the cerebral cortex. Prog. Brain Res. 2004, 145:157-169.
26. Kole M.H., Stuart G.J. Signal processing in the axon initial segment. Neuron 2012, 73:235-247.
27. Krueppel R., Remy S., Beck H. Dendritic integration in hippocampal dentate granule cells. Neuron 2011, 71:512-528.
28. Lee M.G., Hassani O.K., Alonso A., Jones B.E. Cholinergic basal forebrain neurons burst with theta during waking and paradoxical sleep. J.Neurosci. 2005, 25:4365-4369.
29. Leterrier C., Dargent B. No Pasaran! Role of the axon initial segment in the regulation of protein transport and the maintenance of axonal identity. Semin. Cell Dev. Biol. 2014, 27:44-51.
30. Lübke J., Frotscher M., Spruston N. Specialized electrophysiological properties of anatomically identified neurons in the hilar region of the rat fascia dentata. J.Neurophysiol. 1998, 79:1518-1534.
31. Lukacs V., Yudin Y., Hammond G.R., Sharma E., Fukami K., Rohacs T. Distinctive changes in plasma membrane phosphoinositides underlie differential regulation of TRPV1 in nociceptive neurons. J.Neurosci. 2013, 33:11451-11463.
32. Ogawa Y., Schafer D.P., Horresh I., Bar V., Hales K., Yang Y., Susuki K., Peles E., Stankewich M.C., Rasband M.N. Spectrins and ankyrinB constitute a specialized paranodal cytoskeleton. J.Neurosci. 2006, 26:5230-5239.
33. Ohkuma M., Kawai F., Miyachi E. Acetylcholine enhances excitability by lowering the threshold of spike generation in olfactory receptor cells. J.Neurophysiol. 2013, 110:2082-2089.
34. Papke R.L., Wecker L., Stitzel J.A. Activation and inhibition of mouse muscle and neuronal nicotinic acetylcholine receptors expressed in Xenopus oocytes. J.Pharmacol. Exp. Ther. 2010, 333:501-518.
35. Park J.Y., Spruston N. Synergistic actions of metabotropic acetylcholine and glutamate receptors on the excitability of hippocampal CA1 pyramidal neurons. J.Neurosci. 2012, 32:6081-6091.
36. Park J.Y., Kang H.W., Moon H.J., Huh S.U., Jeong S.W., Soldatov N.M., Lee J.H. Activation of protein kinase C augments T-type Ca2+ channel activity without changing channel surface density. J.Physiol. 2006, 577:513-523.
37. Pelkey K.A., McBain C.J. Target-cell-dependent plasticity within the mossy fibre-CA3 circuit reveals compartmentalized regulation of presynaptic function at divergent release sites. J.Physiol. 2008, 586:1495-1502.
38. Pernía-Andrade A.J., Jonas P. Theta-gamma-modulated synaptic currents in hippocampal granule cells invivo define a mechanism for network oscillations. Neuron 2014, 81:140-152.
39. Picciotto M.R., Higley M.J., Mineur Y.S. Acetylcholine as a neuromodulator: cholinergic signaling shapes nervous system function and behavior. Neuron 2012, 76:116-129.
40. Schmidt-Hieber C., Bischofberger J. Fast sodium channel gating supports localized and efficient axonal action potential initiation. J.Neurosci. 2010, 30:10233-10242.
41. Selyanko A.A., Brown D.A. Intracellular calcium directly inhibits potassium M channels in excised membrane patches from rat sympathetic neurons. Neuron 1996, 16:151-162.
42. Shah M.M., Migliore M., Valencia I., Cooper E.C., Brown D.A. Functional significance of axonal Kv7 channels in hippocampal pyramidal neurons. Proc. Natl. Acad. Sci. USA 2008, 105:7869-7874.
43. Shen W., Hamilton S.E., Nathanson N.M., Surmeier D.J. Cholinergic suppression of KCNQ channel currents enhances excitability of striatal medium spiny neurons. J.Neurosci. 2005, 25:7449-7458.
44. Sholl D.A. Dendritic organization in the neurons of the visual and motor cortices of the cat. J.Anat. 1953, 87:387-406.
45. Simon A.P., Poindessous-Jazat F., Dutar P., Epelbaum J., Bassant M.H. Firing properties of anatomically identified neurons in the medial septum of anesthetized and unanesthetized restrained rats. J.Neurosci. 2006, 26:9038-9046.
46. Skaggs W.E., McNaughton B.L., Wilson M.A., Barnes C.A. Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus 1996, 6:149-172.
47. Yamasaki M., Matsui M., Watanabe M. Preferential localization of muscarinic M1 receptor on dendritic shaft and spine of cortical pyramidal cells and its anatomical evidence for volume transmission. J.Neurosci. 2010, 30:4408-4418.