Synergy of direct and indirect cholinergic septo-hippocampal pathways coordinates firing in hippocampal networks

Journal of Neuroscience

Volumn 35, Issue 22, 2015, Pages 8394-8410

  Dannenberg, Holger ^a   Pabst, Milan ^a   Braganza, Oliver ^a   Schoch, Susanne ^a   Niediek, Johannes ^a   Bayraktar, Melike ^a   Mormann, Florian ^a   Beck, Heinz ^a,b  

^a UNIVERSITY HOSPITAL BONN   (Germany)

^b GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

Author keywords

Acetylcholine; Encoding; Hippocampus; In vivo electrophysiology; Medial septum; Theta oscillation

Indexed keywords

ELONGATION FACTOR 1ALPHA; ACETYLCHOLINE; CHANNELRHODOPSIN 2, HUMAN; CHOLINE ACETYLTRANSFERASE; PARVALBUMIN; RHODOPSIN;

ADULT; ANIMAL EXPERIMENT; ARTICLE; COORDINATION; DIAGONAL BAND OF BROCA; EVOKED RESPONSE; FEMALE; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MALE; NERVE CELL INHIBITION; NERVE CELL NETWORK; NERVE STIMULATION; NONHUMAN; OPTOGENETICS; PATCH CLAMP TECHNIQUE; PRIORITY JOURNAL; SCORING SYSTEM; VIRAL GENE DELIVERY SYSTEM; ACTION POTENTIAL; ANIMAL; CHOLINERGIC NERVE CELL; CYTOLOGY; DEPENDOPARVOVIRUS; DRUG EFFECTS; GENETIC TRANSDUCTION; GENETICS; HEART RATE; METABOLISM; MOUSE; NERVE CELL; NERVE TRACT; PHOTOACOUSTICS; PHOTOSTIMULATION; PHYSIOLOGY; SEPTUM NUCLEUS; THETA RHYTHM; TIME; TRANSGENIC MOUSE;

ACETYLCHOLINE; ACTION POTENTIALS; ANIMALS; CHOLINE O-ACETYLTRANSFERASE; CHOLINERGIC NEURONS; DEPENDOVIRUS; HEART RATE; HIPPOCAMPUS; MICE; MICE, TRANSGENIC; NEURAL PATHWAYS; NEURONS; PARVALBUMINS; PHOTIC STIMULATION; PHOTOACOUSTIC TECHNIQUES; RHODOPSIN; SEPTAL NUCLEI; THETA RHYTHM; TIME FACTORS; TRANSDUCTION, GENETIC;

EID: 84930463939     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4460-14.2015     Document Type: Article

References (68)

1. Aloisi AM, Casamenti F, Scali C, Pepeu G, Carli G (1997) Effects of novelty, pain and stress on hippocampal extracellular acetylcholine levels in male rats. Brain Res 748:219-226. CrossRef Medline
2. Alreja M, Wu M, Liu W, Atkins JB, Leranth C, Shanabrough M (2000) Muscarinic tone sustains impulse flow in the septohippocampal GABA but not cholinergic pathway: implications for learning and memory. J Neurosci 20:8103-8110. Medline
3. Andersen P, Bland HB, Myhrer T, Schwartzkroin PA (1979) Septohippocampal pathway necessary for dentate theta production. Brain Res 165:13-22. CrossRef Medline
4. Anzalone S, Roland J, Vogt B, Savage L (2009) Acetylcholine efflux from retrosplenial areas and hippocampal sectors during maze exploration. Behav Brain Res 201:272-278. CrossRef Medline
5. Bassant MH, Apartis E, Jazat-Poindessous FR, Wiley RG, Lamour YA (1995) Selective immunolesion of the basal forebrain cholinergic neurons: effects on hippocampal activity during sleep and wakefulness in the rat. Neurodegeneration 4:61-70. CrossRef Medline
6. Berger-Sweeney J, Stearns NA, Murg SL, Floerke-Nashner LR, Lappi DA, Baxter MG (2001) Selective immunolesions of cholinergic neurons in mice: effects on neuroanatomy, neurochemistry, and behavior. J Neurosci 21:8164-8173. Medline
7. Bialowas J, Frotscher M (1987) Choline acetyltransferase-immunoreactive neurons and terminals in the rat septal complex: a combined light and electron microscopic study. J Comp Neurol 259:298-307. CrossRef Medline
8. Bianchi L, Ballini C, Colivicchi MA, Della Corte L, Giovannini MG, Pepeu G (2003) Investigation on acetylcholine, aspartate, glutamate and GABA extracellular levels from ventral hippocampus during repeated exploratory activity in the rat. Neurochem Res 28:565-573. CrossRef Medline
9. Bland BH (1986) The physiology and pharmacology of hippocampal formation theta rhythms. Prog Neurobiol 26:1-54. CrossRef Medline
10. Buzsáki G (2002) Theta oscillations in the hippocampus. Neuron 33:325-340. CrossRef Medline
11. Buzsáki G, Moser EI (2013) Memory, navigation and theta rhythm in the hippocampal-entorhinal system. Nat Neurosci 16:130-138. CrossRef Medline
12. Cai L, Gibbs RB, Johnson DA (2012) Recognition of novel objects and their location in rats with selective cholinergic lesion of the medial eptum. Neurosci Lett 506:261-265. CrossRef Medline
13. Cea-del Rio CA, Lawrence JJ, Tricoire L, Erdelyi F, Szabo G, McBain CJ (2010) M3 muscarinic acetylcholine receptor expression confers differential cholinergic modulation to neurochemically distinct hippocampal basket cell subtypes. J Neurosci 30:6011-6024. CrossRef Medline
14. Chrobak JJ, Stackman RW, Walsh TJ (1989) Intraseptal administration of muscimol produces dose-dependent memory impairments in the rat. Behav Neural Biol 52:357-369. CrossRef Medline
15. Csicsvari J, Hirase H, Czurko A, Buzsáki G. (1998) Reliability and state dependence of pyramidal cell-interneuron synapses in the hippocampus: an ensemble approach in the behaving rat. Neuron 21:179-189. CrossRef Medline
16. Donovick PJ (1968) Effects of localized septal lesions on hippocampal EEG activity and behavior in rats. J Comp Physiol Psychol 66:569-578. CrossRef Medline
17. Freund TF, Antal M (1988) GABA-containing neurons in the septum control inhibitory interneurons in the hippocampus. Nature 336:170-173. CrossRef Medline
18. Giovannini MG, Rakovska A, Benton RS, Pazzagli M, Bianchi L, Pepeu G (2001) Effects of novelty and habituation on acetylcholine, GABA, and glutamate release from the frontal cortex and hippocampus of freely moving rats. Neuroscience 106:43-53. CrossRef Medline
19. Givens B, Olton DS (1994) Local modulation of basal forebrain: effects on working and reference memory. J Neurosci 14:3578-3587. Medline
20. Gorelova N, Reiner PB (1996) Role of the afterhyperpolarization in control of discharge properties of septal cholinergic neurons in vitro. J Neurophysiol 75:695-706. Medline
21. Grandchamp R, Delorme A (2011) Single-trial normalization for eventrelated spectral decomposition reduces sensitivity to noisy trials. Front Psychol 2.
22. Green JD, Arduini AA (1954) Hippocampal electrical activity in arousal. J Neurophysiol 17:533-557. Medline
23. Griffith WH, Matthews RT (1986) Electrophysiology of AChE-positive neurons in basal forebrain slices. Neurosci Lett 71:169-174. CrossRef Medline
24. Hangya B, Borhegyi Z, Szilágyi N, Freund TF, Varga V (2009) GABAergic neurons of the medial septum lead the hippocampal network during theta activity. J Neurosci 29:8094-8102. CrossRef Medline
25. Harris KD, Henze DA, Csicsvari J, Hirase H, Buzsáki G (2000) Accuracy of tetrode spike separation as determined by simultaneous intracellular and extracellular measurements. J Neurophysiol 84:401-414. Medline
26. Hasselmo ME, Schnell E, Barkai E (1995) Dynamics of learning and recall at excitatory recurrent synapses and cholinergic modulation in rat hippocampal region CA3. J Neurosci 15:5249-5262. Medline
27. Hasselmo ME, Bodelón C, Wyble BP (2002) A proposed function for hippocampal theta rhythm: separate phases of encoding and retrieval enhance reversal of prior learning. Neural Comput 14:793-817. CrossRef Medline
28. Hölscher C, Anwyl R, Rowan MJ (1997) Stimulation on the positive phase of hippocampal theta rhythm induces long-term potentiation that can Be depotentiated by stimulation on the negative phase in area CA1 in vivo. J Neurosci 17:6470-6477. Medline
29. Huh CY, Goutagny R, Williams S (2010) Glutamatergic neurons of the mouse medial septum and diagonal band of Broca synaptically drive hippocampal pyramidal cells: relevance for hippocampal theta rhythm. J Neurosci 30:15951-15961. CrossRef Medline
30. Hyman JM, Wyble BP, Goyal V, Rossi CA, Hasselmo ME (2003) Stimulation in hippocampal region CA1 in behaving rats yields long-term potentiation when delivered to the peak of theta and long-term depression when delivered to the trough. J Neurosci 23:11725-11731. Medline
31. Ji D, Dani JA (2000) Inhibition and disinhibition of pyramidal neurons by activation of nicotinic receptors on hippocampal interneurons. J Neurophysiol 83:2682-2690. Medline
32. Konopacki J, MacIver MB, Bland BH, Roth SH (1987) Carbachol-induced EEG “theta” activity in hippocampal brain slices. Brain Res 405:196-198. CrossRef Medline
33. Kowalczyk T, Bocian R, Konopacki J (2013) The generation of theta rhythm in hippocampal formation maintained in vitro. Eur J Neurosci 37:679-699. CrossRef Medline
34. Kramis R, Vanderwolf CH, Bland BH (1975) Two types of hippocampal rhythmical slow activity in both the rabbit and the rat: relations to behavior and effects of atropine, diethyl ether, urethane, and pentobarbital. Exp Neurol 49:58-85. CrossRef Medline
35. Lawrence JJ, Statland JM, Grinspan ZM, McBain CJ (2006) Cell typespecific dependence of muscarinic signalling in mouse hippocampal stratum oriens interneurones. J Physiol 570:595-610. CrossRef Medline
36. Lawson VH, Bland BH (1993) The role of the septohippocampal pathway in the regulation of hippocampal field activity and behavior: analysis by the intraseptal microinfusion of carbachol, atropine, and procaine. Exp Neurol 120:132-144. CrossRef Medline
37. Lee MG, Chrobak JJ, Sik A, Wiley RG, Buzsáki G (1994) Hippocampal theta activity following selective lesion of the septal cholinergic system. Neuroscience 62:1033-1047. CrossRef Medline
38. Leranth C, Frotscher M (1989) Organization of the septal region in the rat brain: cholinergic-GABAergic interconnections and the termination of hippocampo-septal fibers. J Comp Neurol 289:304-314. CrossRef Medline
39. Liebe S, Hoerzer GM, Logothetis NK, Rainer G (2012) Theta coupling between V4 and prefrontal cortex predicts visual short-term memory performance. Nat Neurosci 15:456-462, S1-S2. Medline
40. Lovett-Barron M, Kaifosh P, Kheirbek MA, Danielson N, Zaremba JD, Reardon TR, Turi GF, Hen R, Zemelman BV, Losonczy A (2014) Dendritic inhibition in the hippocampus supports fear learning. Science 343:857-863. CrossRef Medline
41. Markram H, Segal M (1990) Electrophysiological characteristics of cholinergic and non-cholinergic neurons in the rat medial septum-diagonal band complex. Brain Res 513:171-174. CrossRef Medline
42. Mesulam MM, Mufson EJ, Wainer BH, Levey AI (1983) Central cholinergic pathways in the rat: an overview based on an alternative nomenclature (Ch1-Ch6). Neuroscience 10:1185-1201. CrossRef Medline
43. Moreau PH, Cosquer B, Jeltsch H, Cassel JC, Mathis C (2008) Neuroanatomical and behavioral effects of a novel version of the cholinergic immunotoxin mu p75-saporin in mice. Hippocampus 18:610-622. CrossRef Medline
44. agel G, Brauner M, Liewald JF, Adeishvili N, Bamberg E, Gottschalk A (2005) Light activation of channelrhodopsin-2 in excitable cells of Caenorhabditis elegans triggers rapid behavioral responses. Curr Biol 15: 2279-2284. CrossRef Medline
45. Nagode DA, Tang AH, Karson MA, Klugmann M, Alger BE (2011) Optogenetic release of ACh induces rhythmic bursts of perisomatic IPSCs in hippocampus. PLoS One 6:e27691. CrossRef Medline
46. Nagode DA, Tang AH, Yang K, Alger BE (2014) Optogenetic identification of an intrinsic cholinergically driven inhibitory oscillator sensitive to cannabinoids and opioids in hippocampal CA1. J Physiol 592:103-123. CrossRef Medline
47. Oostenveld R, Fries P, Maris E, Schoffelen JM (2011) FieldTrip: Open source software for advanced analysis of MEG, EEG, and invasive electrophysiological data. Comput Intell Neurosci 2011:156869. Medline
48. Orr G, Rao G, Houston FP, McNaughton BL, Barnes CA (2001) Hippocampal synaptic plasticity is modulated by theta rhythm in the fascia dentata of adult and aged freely behaving rats. Hippocampus 11:647-654. CrossRef Medline
49. Pavlides C, Greenstein YJ, Grudman M, Winson J (1988) Long-term potentiation in the dentate gyrus is induced preferentially on the positive phase of theta-rhythm. Brain Res 439:383-387. CrossRef Medline
50. Paxinos G, Franklin KBJ (2008) The mouse brain in stereotaxic coordinates, the coronal plates and diagrams, Ed 3. Amsterdam: Academic.
51. Petsche H, Stumpf C, Gogolak G (1962) The significance of the rabbit’s septum as a relay station between the midbrain and the hippocampus. I. The control of hippocampus arousal activity by the septum cells. Electroencephalogr Clin Neurophysiol 14:202-211. CrossRef Medline
52. Pinto L, Goard MJ, Estandian D, Xu M, Kwan AC, Lee SH, Harrison TC, Feng G, Dan Y (2013) Fast modulation of visual perception by basal forebrain cholinergic neurons. Nat Neurosci 16:1857-1863. CrossRef Medline
53. Quiroga RQ, Nadasdy Z, Ben-Shaul Y (2004) Unsupervised spike detection and sorting with wavelets and superparamagnetic clustering. Neural Comput 16:1661-1687. CrossRef Medline
54. Rawlins JN, Feldon J, Gray JA (1979) Septo-hippocampal connections and the hippocampal theta rhythm. Exp Brain Res 37:49-63. CrossRef Medline
55. Rogers JL, Kesner RP (2003) Cholinergic modulation of the hippocampus during encoding and retrieval. Neurobiol Learn Mem 80:332-342. CrossRef Medline
56. Rutishauser U, Ross IB, Mamelak AN, Schuman EM (2010) Human memory strength is predicted by theta-frequency phase-locking of single neurons. Nature 464:903-907. CrossRef Medline
57. Serafin M, Williams S, Khateb A, Fort P, Mühlethaler M (1996) Rhythmic firing of medial septum non-cholinergic neurons. Neuroscience 75:671-675. CrossRef Medline
58. Sotty F, Danik M, Manseau F, Laplante F, Quirion R, Williams S (2003) Distinct electrophysiological properties of glutamatergic, cholinergic and GABAergic rat septohippocampal neurons: novel implications for hippocampal rhythmicity. J Physiol 551:927-943. CrossRef Medline
59. Stanley EM, Wilson MA, Fadel JR (2012) Hippocampal neurotransmitter efflux during one-trial novel object recognition in rats. Neurosci Lett 511:38-42. CrossRef Medline
60. Stewart M, Fox SE (1990) Do septal neurons pace the hippocampal theta rhythm? Trends Neurosci 13:163-168. CrossRef Medline
61. Stumpf C, Petsche H, Gogolak G (1962) The significance of the rabbit’s septum as a relay station between the midbrain and the hippocampus. II. The differential influence of drugs upon both the septal cell firing pattern and the hippocampus theta activity. Electroencephalogr Clin Neurophysiol 14:212-219. CrossRef Medline
62. Tóth K, Freund TF, Miles R (1997) Disinhibition of rat hippocampal pyramidal cells by GABAergic afferents from the septum. J Physiol 500:463-474. CrossRef Medline
63. van Loo KM, Schaub C, Pernhorst K, Yaari Y, Beck H, Schoch S, Becker AJ (2012) Transcriptional regulation of T-type calcium channel CaV3.2: bidirectionality by early growth response 1 (Egr1) and repressor element 1 (RE-1) protein-silencing transcription factor (REST). J Biol Chem 287: 15489-15501. CrossRef Medline
64. Vandecasteele M, Varga V, Berényi A, Papp E, Barthó P, Venance L, Freund TF, Buzsáki G (2014) Optogenetic activation of septal cholinergic neurons suppresses sharp wave ripples and enhances theta oscillations in the hippocampus. Proc Natl Acad Sci U S A
65. Varga V, Hangya B, Kránitz K, Ludányi A, Zemankovics R, Katona I, Shigemoto R, Freund TF, Borhegyi Z (2008) The presence of pacemakerHCN channels identifies theta rhythmic GABAergic neurons in the medial septum. J Physiol 586:3893-3915. CrossRef Medline
66. Widmer H, Ferrigan L, Davies CH, Cobb SR (2006) Evoked slow muscarinic acetylcholinergic synaptic potentials in rat hippocampal interneurons. Hippocampus 16:617-628. CrossRef Medline
67. Wulff P, Ponomarenko AA, Bartos M, Korotkova TM, Fuchs EC, Bähner F, Both M, Tort AB, Kopell NJ, Wisden W, Monyer H (2009) Hippocampal theta rhythm and its coupling with gamma oscillations require fast inhibition onto parvalbumin-positive interneurons. Proc Natl Acad Sci U S A 106:3561-3566. CrossRef Medline
68. Yoder RM, Pang KC (2005) Involvement of GABAergic and cholinergic medial septal neurons in hippocampal theta rhythm. Hippocampus 15:381-392. CrossRef Medline