Theta oscillations regulate the speed of locomotion via a hippocampus to lateral septum pathway

Nature Communications

Volumn 6, Issue , 2015, Pages

  Bender, Franziska ^a,b   Gorbati, Maria ^a,b   Cadavieco, Marta Carus ^a,b   Denisova, Natalia ^a,b   Gao, Xiaojie ^a,b   Holman, Constance ^a,b   Korotkova, Tatiana ^a,b   Ponomarenko, Alexey ^a,b  

^a LEIBNIZ INSTITUT FÜR MOLEKULARE PHARMAKOLOGIE   (Germany)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN; CELLS AND CELL COMPONENTS; GENETIC ANALYSIS; INHIBITION; LOCOMOTION; PHYSIOLOGY; RODENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EXPLORATORY BEHAVIOR; HIPPOCAMPUS; HIPPOCAMPUS THETA RHYTHM; LATERAL SEPTUM; LOCOMOTION; MALE; MOTOR COORDINATION; MOUSE; NONHUMAN; OSCILLATION; POSITION; PYRAMIDAL NERVE CELL; RUNNING; SPATIAL ORIENTATION; VELOCITY; ANIMAL; C57BL MOUSE; OPTOGENETICS; PHYSIOLOGY; RANDOMIZATION; SEPTUM PELLUCIDUM; THETA RHYTHM; TRANSGENIC MOUSE;

ANIMALIA; MUS;

4 AMINOBUTYRIC ACID RECEPTOR;

ANIMALS; GABAERGIC NEURONS; HIPPOCAMPUS; LOCOMOTION; MALE; MICE, INBRED C57BL; MICE, TRANSGENIC; OPTOGENETICS; RANDOM ALLOCATION; SEPTUM OF BRAIN; SPATIAL NAVIGATION; THETA RHYTHM;

EID: 84943805922     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms9521     Document Type: Article

References (70)

1. Buzsaki, G., Moser, E. I. Memory, navigation and theta rhythm in the hippocampal-entorhinal system. Nat. Neurosci. 16, 130-138 (2013).
2. Hartley, T., Lever, C., Burgess, N., O'Keefe, J. Space in the brain: how the hippocampal formation supports spatial cognition. Philos. Trans. R Soc. Lond. B Biol. Sci. 369, 20120510 (2014).
3. Maurer, A. P., McNaughton, B. L. Network and intrinsic cellular mechanisms underlying theta phase precession of hippocampal neurons. Trends Neurosci. 30, 325-333 (2007).
4. Vanderwolf, C. H. Hippocampal electrical activity and voluntary movement in the rat. Electroencephalogr. Clin. Neurophysiol. 26, 407-418 (1969).
5. Grastyan, E., Karmos, G., Vereczkey, L., Martin, J., Kellenyi, L. Hypothalamic motivational processes as reflected by their hippocampal electrical correlates. Science 149, 91-93 (1965).
6. Vertes, R. P., Hoover, W. B., Viana Di Prisco, G. Theta rhythm of the hippocampus: subcortical control and functional significance. Behav. Cogn. Neurosci. Rev. 3, 173-200 (2004).
7. Hasselmo, M. E., Hay, J., Ilyn, M., Gorchetchnikov, A. Neuromodulation, theta rhythm and rat spatial navigation. Neural Netw. 15, 689-707 (2002).
8. Bland, B. H., Vanderwolf, C. H. Diencephalic and hippocampal mechanisms of motor activity in the rat: effects of posterior hypothalamic stimulation on behavior and hippocampal slow wave activity. Brain Res. 43, 67-88 (1972).
9. McFarland, W. L., Teitelbaum, H., Hedges, E. K. Relationship between hippocampal theta activity and running speed in the rat. J. Comp. Physiol. Psychol. 88, 324-328 (1975).
10. Geisler, C., Robbe, D., Zugaro, M., Sirota, A., Buzsaki, G. Hippocampal place cell assemblies are speed-controlled oscillators. Proc. Natl Acad. Sci. USA 104, 8149-8154 (2007).
11. Fuhrmann, F. et al. Locomotion, theta oscillations, and the speed-correlated firing of hippocampal neurons are controlled by a medial septal glutamatergic circuit. Neuron 86, 1253-1264 (2015).
12. Bland, B. H., Vanderwolf, C. H. Electrical stimulation of the hippocampal formation: behavioral and bioelectrical effects. Brain Res. 43, 89-106 (1972).
13. Oddie, S. D., Bland, B. H. Hippocampal formation theta activity and movement selection. Neurosci. Biobehav. Rev. 22, 221-231 (1998).
14. Risold, P. Y., Swanson, L. W. Structural evidence for functional domains in the rat hippocampus. Science 272, 1484-1486 (1996).
15. Sheehan, T. P., Chambers, R. A., Russell, D. S. Regulation of affect by the lateral septum: implications for neuropsychiatry. Brain Res. Brain Res. Rev. 46, 71-117 (2004).
16. Luo, A. H., Tahsili-Fahadan, P., Wise, R. A., Lupica, C. R., Aston-Jones, G. Linking context with reward: a functional circuit from hippocampal CA3 to ventral tegmental area. Science 333, 353-357 (2011).
17. Sinnamon, H. M. Preoptic and hypothalamic neurons and the initiation of locomotion in the anesthetized rat. Prog. Neurobiol. 41, 323-344 (1993).
18. Grillner, S., Wallen, P., Saitoh, K., Kozlov, A., Robertson, B. Neural bases of goal-directed locomotion in vertebrates-an overview. Brain Res. Rev. 57, 2-12 (2008).
19. Wulff, P. et al. Hippocampal theta rhythm and its coupling with gamma oscillations require fast inhibition onto parvalbumin-positive interneurons. Proc. Natl Acad. Sci. USA 106, 3561-3566 (2009).
20. Csicsvari, J., Hirase, H., Czurko, A., Mamiya, A., Buzsaki, G. Oscillatory coupling of hippocampal pyramidal cells and interneurons in the behaving Rat. J. Neurosci. 19, 274-287 (1999).
21. Varga, C., Golshani, P., Soltesz, I. Frequency-invariant temporal ordering of interneuronal discharges during hippocampal oscillations in awake mice. Proc. Natl Acad. Sci. USA 109, E2726-E2734 (2012).
22. Klausberger, T. et al. Brain-state-and cell-type-specific firing of hippocampal interneurons in vivo. Nature 421, 844-848 (2003).
23. Goshen, I. et al. Dynamics of retrieval strategies for remote memories. Cell 147, 678-689 (2011).
24. Maurer, A. P., Vanrhoads, S. R., Sutherland, G. R., Lipa, P., McNaughton, B. L. Self-motion and the origin of differential spatial scaling along the septo-temporal axis of the hippocampus. Hippocampus 15, 841-852 (2005).
25. Mahler, S. V. et al. Designer receptors show role for ventral pallidum input to ventral tegmental area in cocaine seeking. Nat. Neurosci. 17, 577-585 (2014).
26. Gunaydin, L. A. et al. Ultrafast optogenetic control. Nat. Neurosci. 13, 387-392 (2010).
27. O'Keefe, J., Recce, M. L. Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3, 317-330 (1993).
28. Huxter, J. R., Senior, T. J., Allen, K., Csicsvari, J. Theta phase-specific codes for two-dimensional position, trajectory and heading in the hippocampus. Nat. Neurosci. 11, 587-594 (2008).
29. Korotkova, T., Fuchs, E. C., Ponomarenko, A., von Engelhardt, J., Monyer, H. NMDA receptor ablation on parvalbumin-positive interneurons impairs hippocampal synchrony, spatial representations, and working memory. Neuron 68, 557-569 (2010).
30. Dragoi, G., Buzsaki, G. Temporal encoding of place sequences by hippocampal cell assemblies. Neuron 50, 145-157 (2006).
31. Jezek, K., Henriksen, E. J., Treves, A., Moser, E. I., Moser, M. B. Theta-paced flickering between place-cell maps in the hippocampus. Nature 478, 246-249 (2011).
32. Kiss, J., Csaki, A., Bokor, H., Kocsis, K., Kocsis, B. Possible glutamatergic/aspartatergic projections to the supramammillary nucleus and their origins in the rat studied by selective [(3)H]D-aspartate labelling and immunocytochemistry. Neuroscience 111, 671-691 (2002).
33. Bland, B. H., Bird, J., Jackson, J., Natsume, K. Medial septal modulation of the ascending brainstem hippocampal synchronizing pathways in the freely moving rat. Hippocampus 16, 11-19 (2006).
34. Long, L. L., Hinman, J. R., Chen, C. M., Escabi, M. A., Chrobak, J. J. Theta dynamics in rat: speed and acceleration across the Septotemporal axis. PLoS ONE 9, e97987 (2014).
35. Kramis, R. C., Routtenberg, A. Dissociation of hippocampal EEG from its behavioral correlates by septal and hippocampal electrical stimulation. Brain Res. 125, 37-49 (1977).
36. Hangya, B., Borhegyi, Z., Szilagyi, N., Freund, T. F., Varga, V. GABAergic neurons of the medial septum lead the hippocampal network during theta activity. J. Neurosci. 29, 8094-8102 (2009).
37. Scarlett, D., Dypvik, A. T., Bland, B. H. Comparison of spontaneous and septally driven hippocampal theta field and theta-related cellular activity. Hippocampus 14, 99-106 (2004).
38. Kocsis, B., Vertes, R. P. Phase relations of rhythmic neuronal firing in the supramammillary nucleus and mammillary body to the hippocampal theta activity in urethane anesthetized rats. Hippocampus 7, 204-214 (1997).
39. Borhegyi, Z., Varga, V., Szilagyi, N., Fabo, D., Freund, T. F. Phase segregation of medial septal GABAergic neurons during hippocampal theta activity. J. Neurosci. 24, 8470-8479 (2004).
40. Bland, B. H., Oddie, S. D., Colom, L. V. Mechanisms of neural synchrony in the septohippocampal pathways underlying hippocampal theta generation. J. Neurosci. 19, 3223-3237 (1999).
41. Freund, T. F., Antal, M. GABA-containing neurons in the septum control inhibitory interneurons in the hippocampus. Nature 336, 170-173 (1988).
42. Toth, K., Freund, T. F., Miles, R. Disinhibition of rat hippocampal pyramidal cells by GABAergic afferents from the septum. J. Physiol. 500(Pt 2): 463-474 (1997).
43. Toth, K., Borhegyi, Z., Freund, T. F. Postsynaptic targets of GABAergic hippocampal neurons in the medial septum-diagonal band of broca complex. J. Neurosci. 13, 3712-3724 (1993).
44. Blasco-Ibanez, J. M., Freund, T. F. Synaptic input of horizontal interneurons in stratum oriens of the hippocampal CA1 subfield: structural basis of feed-back activation. Eur. J. Neurosci. 7, 2170-2180 (1995).
45. Jinno, S. et al. Neuronal diversity in GABAergic long-range projections from the hippocampus. J. Neurosci. 27, 8790-8804 (2007).
46. Mattis, J. et al. Frequency-dependent, cell type-divergent signaling in the hippocamposeptal projection. J. Neurosci. 34, 11769-11780 (2014).
47. Manseau, F., Goutagny, R., Danik, M., Williams, S. The hippocamposeptal pathway generates rhythmic firing of GABAergic neurons in the medial septum and diagonal bands: an investigation using a complete septohippocampal preparation in vitro. J. Neurosci. 28, 4096-4107 (2008).
48. Kim, S. M., Frank, L. M. Hippocampal lesions impair rapid learning of a continuous spatial alternation task. PLos ONE 4, e5494 (2009).
49. Jarrard, L. E. Behavior of hippocampal lesioned rats in home cage and novel situations. Physiol. Behav. 3, 65-70 (1968).
50. McNaughton, B. L., Barnes, C. A., O'Keefe, J. The contributions of position, direction, and velocity to single unit activity in the hippocampus of freelymoving rats. Exp. Brain Res. 52, 41-49 (1983).
51. Colgin, L. L. et al. Frequency of gamma oscillations routes flow of information in the hippocampus. Nature 462, 353-357 (2009).
52. Sirota, A. et al. Entrainment of neocortical neurons and gamma oscillations by the hippocampal theta rhythm. Neuron 60, 683-697 (2008).
53. O'Keefe, J., Conway, D. H. Hippocampal place units in the freely moving rat: why they fire where they fire. Exp. Brain Res. 31, 573-590 (1978).
54. Leutgeb, S. et al. Independent codes for spatial and episodic memory in hippocampal neuronal ensembles. Science 309, 619-623 (2005).
55. McKenzie, S. et al. Hippocampal representation of related and opposing memories develop within distinct, hierarchically organized neural schemas. Neuron 83, 202-215 (2014).
56. Dupret, D., O'Neill, J., Pleydell-Bouverie, B., Csicsvari, J. The reorganization and reactivation of hippocampal maps predict spatial memory performance. Nat. Neurosci. 13, 995-1002 (2010).
57. Ferbinteanu, J., Shapiro, M. L. Prospective and retrospective memory coding in the hippocampus. Neuron 40, 1227-1239 (2003).
58. Wood, E. R., Dudchenko, P. A., Robitsek, R. J., Eichenbaum, H. Hippocampal neurons encode information about different types of memory episodes occurring in the same location. Neuron 27, 623-633 (2000).
59. Agarwal, G. et al. Spatially distributed local fields in the hippocampus encode rat position. Science 344, 626-630 (2014).
60. Gladfelter, W. E., Brobeck, J. R. Decreased spontaneous locomotor activity in the rat induced by hypothalamic lesions. Am. J. Physiol. 203, 811-817 (1962).
61. Mileykovskiy, B. Y., Kiyashchenko, L. I., Siegel, J. M. Behavioral correlates of activity in identified hypocretin/orexin neurons. Neuron 46, 787-798 (2005).
62. Lee, A. M. et al. Identification of a brainstem circuit regulating visual cortical state in parallel with locomotion. Neuron 83, 455-466 (2014).
63. Hippenmeyer, S. et al. A developmental switch in the response of DRG neurons to ETS transcription factor signaling. PLoS Biol. 3, e159 (2005).
64. Vong, L. et al. Leptin action on GABAergic neurons prevents obesity and reduces inhibitory tone to POMC neurons. Neuron 71, 142-154 (2011).
65. Kim, S. Y. et al. Diverging neural pathways assemble a behavioural state from separable features in anxiety. Nature 496, 219-223 (2013).
66. Armbruster, B. N., Li, X., Pausch, M. H., Herlitze, S., Roth, B. L. Evolving the lock to fit the key to create a family of G protein-coupled receptors potently activated by an inert ligand. Proc. Natl Acad. Sci. USA 104, 5163-5168 (2007).
67. Hazan, L., Zugaro, M., Buzsaki, G. Klusters, NeuroScope, NDManager: a free software suite for neurophysiological data processing and visualization. J. Neurosci. Methods 155, 207-216 (2006).
68. Harris, K. D., Henze, D. A., Csicsvari, J., Hirase, H., Buzsaki, G. Accuracy of tetrode spike separation as determined by simultaneous intracellular and extracellular measurements. J. Neurophysiol. 84, 401-414 (2000).
69. Siapas, A. G., Lubenov, E. V., Wilson, M. A. Prefrontal phase locking to hippocampal theta oscillations. Neuron 46, 141-151 (2005).
70. Jung, M. W., Wiener, S. I., McNaughton, B. L. Comparison of spatial firing characteristics of units in dorsal and ventral hippocampus of the rat. J. Neurosci. 14, 7347-7356 (1994).