Locomotion, Theta Oscillations, and the Speed-Correlated Firing of Hippocampal Neurons Are Controlled by a Medial Septal Glutamatergic Circuit

Neuron

Volumn 86, Issue 5, 2015, Pages 1253-1264

  Fuhrmann, Falko ^a   Justus, Daniel ^a   Sosulina, Liudmila ^a   Kaneko, Hiroshi ^a   Beutel, Tatjana ^a   Friedrichs, Detlef ^a   Schoch, Susanne ^b   Schwarz, MartinKarl ^c   Fuhrmann, Martin ^a   Remy, Stefan ^a,b  

^a GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

^b UNIVERSITY HOSPITAL BONN   (Germany)

^c UNIVERSITY OF BONN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALVEUS; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; GLUTAMATERGIC SYNAPSE; HIPPOCAMPAL CA1 REGION; HIPPOCAMPUS THETA RHYTHM; INTERNEURON; LOCOMOTION; MEDIAL SEPTAL GLUTAMATERGIC CIRCUIT; MOUSE; NEGATIVE FEEDBACK; NERVE CELL MEMBRANE STEADY POTENTIAL; NERVE FUNCTION; NONHUMAN; PERFORANT NERVE TRACT; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SCHAFFER COLLATERAL PATHWAY; VELOCITY; ANIMAL; FEMALE; HIPPOCAMPUS; MALE; NERVE CELL; NERVE CELL NETWORK; PHYSIOLOGY; SEPTUM PELLUCIDUM; THETA RHYTHM; TRANSGENIC MOUSE;

ANIMALS; FEMALE; HIPPOCAMPUS; LOCOMOTION; MALE; MICE; MICE, TRANSGENIC; NERVE NET; NEURONS; SEPTUM OF BRAIN; THETA RHYTHM;

EID: 84930543097     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2015.05.001     Document Type: Article

References (68)

1. Ahmed O.J., Mehta M.R. The hippocampal rate code: anatomy, physiology and theory. Trends Neurosci. 2009, 32:329-338.
2. Andersen P. The Hippocampus Book 2007, Oxford University Press, Oxford.
3. Ang C.W., Carlson G.C., Coulter D.A. Hippocampal CA1 circuitry dynamically gates direct cortical inputs preferentially at theta frequencies. J.Neurosci. 2005, 25:9567-9580.
4. Bell K.A., Shim H., Chen C.K., McQuiston A.R. Nicotinic excitatory postsynaptic potentials in hippocampal CA1 interneurons are predominantly mediated by nicotinic receptors that contain α4 and β2 subunits. Neuropharmacology 2011, 61:1379-1388.
5. Bland B.H., Oddie S.D. Theta band oscillation and synchrony in the hippocampal formation and associated structures: the case for its role in sensorimotor integration. Behav. Brain Res. 2001, 127:119-136.
6. Brandon M.P., Koenig J., Leutgeb J.K., Leutgeb S. New and distinct hippocampal place codes are generated in a new environment during septal inactivation. Neuron 2014, 82:789-796.
7. Buzsáki G. Theta oscillations in the hippocampus. Neuron 2002, 33:325-340.
8. Buzsáki G., Leung L.W., Vanderwolf C.H. Cellular bases of hippocampal EEG in the behaving rat. Brain Res. 1983, 287:139-171.
9. Colom L.V., Castaneda M.T., Reyna T., Hernandez S., Garrido-Sanabria E. Characterization of medial septal glutamatergic neurons and their projection to the hippocampus. Synapse 2005, 58:151-164.
10. Czurkó A., Hirase H., Csicsvari J., Buzsáki G. Sustained activation of hippocampal pyramidal cells by 'space clamping' in a running wheel. Eur. J. Neurosci. 1999, 11:344-352.
11. Ekstrom A.D., Meltzer J., McNaughton B.L., Barnes C.A. NMDA receptor antagonism blocks experience-dependent expansion of hippocampal "place fields". Neuron 2001, 31:631-638.
12. Elfant D., Pál B.Z., Emptage N., Capogna M. Specific inhibitory synapses shift the balance from feedforward to feedback inhibition of hippocampal CA1 pyramidal cells. Eur. J. Neurosci. 2008, 27:104-113.
13. English D.F., Peyrache A., Stark E., Roux L., Vallentin D., Long M.A., Buzsáki G. Excitation and inhibition compete to control spiking during hippocampal ripples: intracellular study in behaving mice. J.Neurosci. 2014, 34:16509-16517.
14. Fonseca M.S., Murakami M., Mainen Z.F. Activation of dorsal raphe serotonergic neurons promotes waiting but is not reinforcing. Curr. Biol. 2015, 25:306-315.
15. Freund T.F., Antal M. GABA-containing neurons in the septum control inhibitory interneurons in the hippocampus. Nature 1988, 336:170-173.
16. Frotscher M., Léránth C. Cholinergic innervation of the rat hippocampus as revealed by choline acetyltransferase immunocytochemistry: a combined light and electron microscopic study. J.Comp. Neurol. 1985, 239:237-246.
17. Fu Y., Tucciarone J.M., Espinosa J.S., Sheng N., Darcy D.P., Nicoll R.A., Huang Z.J., Stryker M.P. A cortical circuit for gain control by behavioral state. Cell 2014, 156:1139-1152.
18. Geisler S., Wise R.A. Functional implications of glutamatergic projections to the ventral tegmental area. Rev. Neurosci. 2008, 19:227-244.
19. Gloveli T., Dugladze T., Saha S., Monyer H., Heinemann U., Traub R.D., Whittington M.A., Buhl E.H. Differential involvement of oriens/pyramidale interneurones in hippocampal network oscillations invitro. J.Physiol. 2005, 562:131-147.
20. Golding N.L., Spruston N. Dendritic sodium spikes are variable triggers of axonal action potentials in hippocampal CA1 pyramidal neurons. Neuron 1998, 21:1189-1200.
21. Golding N.L., Staff N.P., Spruston N. Dendritic spikes as a mechanism for cooperative long-term potentiation. Nature 2002, 418:326-331.
22. Green J.D., Arduini A.A. Hippocampal electrical activity in arousal. J.Neurophysiol. 1954, 17:533-557.
23. Hangya B., Borhegyi Z., Szilágyi N., Freund T.F., Varga V. GABAergic neurons of the medial septum lead the hippocampal network during theta activity. J.Neurosci. 2009, 29:8094-8102.
24. Hosp J.A., Pekanovic A., Rioult-Pedotti M.S., Luft A.R. Dopaminergic projections from midbrain to primary motor cortex mediate motor skill learning. J.Neurosci. 2011, 31:2481-2487.
25. Huh C.Y., Goutagny R., Williams S. Glutamatergic neurons of themouse medial septum and diagonal band of Broca synaptically drive hippocampal pyramidal cells: relevance for hippocampal theta rhythm. J.Neurosci. 2010, 30:15951-15961.
26. Jarsky T., Roxin A., Kath W.L., Spruston N. Conditional dendritic spike propagation following distal synaptic activation of hippocampal CA1 pyramidal neurons. Nat. Neurosci. 2005, 8:1667-1676.
27. Kalivas P.W., Nemeroff C.B., Prange A.J. Increase in spontaneous motor activity following infusion of neurotensin into the ventral tegmental area. Brain Res. 1981, 229:525-529.
28. King C., Recce M., O'Keefe J. The rhythmicity of cells of the medial septum/diagonal band of Broca in the awake freely moving rat: relationships with behaviour and hippocampal theta. Eur. J. Neurosci. 1998, 10:464-477.
29. Kitamura T., Pignatelli M., Suh J., Kohara K., Yoshiki A., Abe K., Tonegawa S. Island cells control temporal association memory. Science 2014, 343:896-901.
30. Klausberger T., Somogyi P. Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. Science 2008, 321:53-57.
31. Köhler C., Chan-Palay V., Wu J.Y. Septal neurons containing glutamic acid decarboxylase immunoreactivity project to the hippocampal region in the rat brain. Anat. Embryol. (Berl.) 1984, 169:41-44.
32. Kunori N., Kajiwara R., Takashima I. Voltage-sensitive dye imaging of primary motor cortex activity produced by ventral tegmental area stimulation. J.Neurosci. 2014, 34:8894-8903.
33. Leão R.N., Mikulovic S., Leão K.E., Munguba H., Gezelius H., Enjin A., Patra K., Eriksson A., Loew L.M., Tort A.B., Kullander K. OLM interneurons differentially modulate CA3 and entorhinal inputs to hippocampal CA1 neurons. Nat. Neurosci. 2012, 15:1524-1530.
34. Leão R.N., Targino Z.H., Colom L.V., Fisahn A. Interconnection and synchronization of neuronal populations in the mouse medial septum/diagonal band of Broca. J.Neurophysiol. 2015, 113:971-980.
35. Lee R.S., Steffensen S.C., Henriksen S.J. Discharge profiles of ventral tegmental area GABA neurons during movement, anesthesia, and the sleep-wake cycle. J.Neurosci. 2001, 21:1757-1766.
36. Lee D., Lin B.J., Lee A.K. Hippocampal place fields emerge upon single-cell manipulation of excitability during behavior. Science 2012, 337:849-853.
37. Lein E.S., Hawrylycz M.J., Ao N., Ayres M., Bensinger A., Bernard A., Boe A.F., Boguski M.S., Brockway K.S., Byrnes E.J., et al. Genome-wide atlas of gene expression in the adult mouse brain. Nature 2007, 445:168-176.
38. Léránth C., Frotscher M. Cholinergic innervation of hippocampal GAD- and somatostatin-immunoreactive commissural neurons. J.Comp. Neurol. 1987, 261:33-47.
39. Lovett-Barron M., Kaifosh P., Kheirbek M.A., Danielson N., Zaremba J.D., Reardon T.R., Turi G.F., Hen R., Zemelman B.V., Losonczy A. Dendritic inhibition in the hippocampus supports fear learning. Science 2014, 343:857-863.
40. Manseau F., Danik M., Williams S. A functional glutamatergic neurone network in the medial septum and diagonal band area. J.Physiol. 2005, 566:865-884.
41. Maru E., Takahashi L.K., Iwahara S. Effects of median raphe nucleus lesions on hippocampal EEG in the freely moving rat. Brain Res. 1979, 163:223-234.
42. McFarland W.L., Teitelbaum H., Hedges E.K. Relationship between hippocampal theta activity and running speed in the rat. J.Comp. Physiol. Psychol. 1975, 88:324-328.
43. McNaughton B.L., Barnes C.A., O'Keefe J. The contributions of position, direction, and velocity to single unit activity in the hippocampus of freely-moving rats. Exp. Brain Res. 1983, 52:41-49.
44. Mink J.W., Sinnamon H.M., Adams D.B. Activity of basal forebrain neurons in the rat during motivated behaviors. Behav. Brain Res. 1983, 8:85-108.
45. Mogenson G.J., Jones D.L., Yim C.Y. From motivation to action: functional interface between the limbic system and the motor system. Prog. Neurobiol. 1980, 14:69-97.
46. Moruzzi G., Magoun H.W. Brain stem reticular formation and activation of the EEG. Electroencephalogr. Clin. Neurophysiol. 1949, 1:455-473.
47. Müller C., Beck H., Coulter D., Remy S. Inhibitory control of linear and supralinear dendritic excitation in CA1 pyramidal neurons. Neuron 2012, 75:851-864.
48. Oades R.D., Halliday G.M. Ventral tegmental (A10) system: neurobiology. 1. Anatomy and connectivity. Brain Res. 1987, 434:117-165.
49. Oddie S.D., Stefanek W., Kirk I.J., Bland B.H. Intraseptal procaine abolishes hypothalamic stimulation-induced wheel-running and hippocampal theta field activity in rats. J.Neurosci. 1996, 16:1948-1956.
50. Parker S.M., Sinnamon H.M. Forward locomotion elicited by electrical stimulation in the diencephalon and mesencephalon of the awake rat. Physiol. Behav. 1983, 31:581-587.
51. Pouille F., Scanziani M. Enforcement of temporal fidelity in pyramidal cells by somatic feed-forward inhibition. Science 2001, 293:1159-1163.
52. Puryear C.B., Kim M.J., Mizumori S.J. Conjunctive encoding of movement and reward by ventral tegmental area neurons in the freely navigating rodent. Behav. Neurosci. 2010, 124:234-247.
53. Royer S., Zemelman B.V., Losonczy A., Kim J., Chance F., Magee J.C., Buzsáki G. Control of timing, rate and bursts of hippocampal place cells by dendritic and somatic inhibition. Nat. Neurosci. 2012, 15:769-775.
54. Sinnamon H.M. Preoptic and hypothalamic neurons and the initiation of locomotion in the anesthetized rat. Prog. Neurobiol. 1993, 41:323-344.
55. Steinfels G.F., Heym J., Strecker R.E., Jacobs B.L. Raphe unit activity in freely moving cats is altered by manipulations of central but not peripheral motor systems. Brain Res. 1983, 279:77-84.
56. Stumpf C., Petsche H., Gogolak G. 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. 1962, 14:212-219.
57. Takahashi H., Magee J.C. Pathway interactions and synaptic plasticity in the dendritic tuft regions of CA1 pyramidal neurons. Neuron 2009, 62:102-111.
58. Thinschmidt J.S., Kinney G.G., Kocsis B. The supramammillary nucleus: is it necessary for the mediation of hippocampal theta rhythm?. Neuroscience 1995, 67:301-312.
59. Tóth K., Freund T.F., Miles R. Disinhibition of rat hippocampal pyramidal cells by GABAergic afferents from the septum. J.Physiol. 1997, 500:463-474.
60. Vandecasteele M., Varga V., Berényi A., Papp E., Barthó P., Venance L., Freund T.F., Buzsáki G. Optogenetic activation of septal cholinergic neurons suppresses sharp wave ripples and enhances theta oscillations in the hippocampus. Proc. Natl. Acad. Sci. USA 2014, 111:13535-13540.
61. Vanderwolf C.H. Hippocampal electrical activity and voluntary movement in the rat. Electroencephalogr. Clin. Neurophysiol. 1969, 26:407-418.
62. Varga V., Losonczy A., Zemelman B.V., Borhegyi Z., Nyiri G., Domonkos A., Hangya B., Holderith N., Magee J.C., Freund T.F. Fast synaptic subcortical control of hippocampal circuits. Science 2009, 326:449-453.
63. Vertes R.P., Fortin W.J., Crane A.M. Projections of the median raphe nucleus in the rat. J.Comp. Neurol. 1999, 407:555-582.
64. Wang D.V., Tsien J.Z. Conjunctive processing of locomotor signals by the ventral tegmental area neuronal population. PLoS ONE 2011, 6:e16528.
65. Wang Y., Romani S., Lustig B., Leonardo A., Pastalkova E. Theta sequences are essential for internally generated hippocampal firing fields. Nat. Neurosci. 2015, 18:282-288.
66. Whishaw I.Q., Vanderwolf C.H. Hippocampal EEG and behavior: changes in amplitude and frequency of RSA (theta rhythm) associated with spontaneous and learned movement patterns in rats and cats. Behav. Biol. 1973, 8:461-484.
67. Woodnorth M.A., McNaughton N. Different systems in the posterior hypothalamic nucleus of rats control theta frequency and trigger movement. Behav. Brain Res. 2005, 163:107-114.
68. Wyble B.P., Hyman J.M., Rossi C.A., Hasselmo M.E. Analysis of theta power in hippocampal EEG during bar pressing and running behavior in rats during distinct behavioral contexts. Hippocampus 2004, 14:662-674.