Multiple Running Speed Signals in Medial Entorhinal Cortex

Neuron

Volumn 91, Issue 3, 2016, Pages 666-679

  Hinman, James R ^a   Brandon, Mark P ^a,b   Climer, Jason R ^a   Chapman, G William ^a   Hasselmo, Michael E ^a  

^a BOSTON UNIVERSITY   (United States)

^b DOUGLAS MENTAL HEALTH UNIVERSITY INSTITUTE   (Canada)

Author keywords

entorhinal cortex; grid cell; medial septum; path integration; theta rhythm

Indexed keywords

ADULT; ANIMAL EXPERIMENT; ARTICLE; CIRCADIAN RHYTHM; FIRING RATE; LOCOMOTION; MALE; MEDIAL ENTORHINAL CORTEX; MEDIAL SEPTUM; MEMORY; NERVOUS SYSTEM FUNCTION; NEUROMODULATION; NONHUMAN; OSCILLATION; PRIORITY JOURNAL; RAT; RUNNING SPEED SIGNAL; SEPTUM PELLUCIDUM; THETA RHYTHM; ACTION POTENTIAL; ANIMAL; BIOLOGICAL MODEL; ENTORHINAL CORTEX; PHYSIOLOGY; RUNNING; SEPTUM NUCLEUS; WALKING SPEED;

ACTION POTENTIALS; ANIMALS; ENTORHINAL CORTEX; MALE; MODELS, NEUROLOGICAL; RATS; RUNNING; SEPTAL NUCLEI; THETA RHYTHM; WALKING SPEED;

EID: 84978910309     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2016.06.027     Document Type: Article

References (67)

1. Alonso, A., Köhler, C., A study of the reciprocal connections between the septum and the entorhinal area using anterograde and retrograde axonal transport methods in the rat brain. J. Comp. Neurol. 225 (1984), 327–343.
2. Bender, F., Gorbati, M., Cadavieco, M.C., Denisova, N., Gao, X., Holman, C., Korotkova, T., Ponomarenko, A., Theta oscillations regulate the speed of locomotion via a hippocampus to lateral septum pathway. Nat. Commun., 6, 2015, 8521.
3. Blair, H.T., Gupta, K., Zhang, K., Conversion of a phase- to a rate-coded position signal by a three-stage model of theta cells, grid cells, and place cells. Hippocampus 18 (2008), 1239–1255.
4. Brandon, M.P., Bogaard, A.R., Libby, C.P., Connerney, M.A., Gupta, K., Hasselmo, M.E., Reduction of theta rhythm dissociates grid cell spatial periodicity from directional tuning. Science 332 (2011), 595–599.
5. Brandon, M.P., Bogaard, A.R., Schultheiss, N.W., Hasselmo, M.E., Segregation of cortical head direction cell assemblies on alternating θ cycles. Nat. Neurosci. 16 (2013), 739–748.
6. Buetfering, C., Allen, K., Monyer, H., Parvalbumin interneurons provide grid cell-driven recurrent inhibition in the medial entorhinal cortex. Nat. Neurosci. 17 (2014), 710–718.
7. Burak, Y., Fiete, I.R., Accurate path integration in continuous attractor network models of grid cells. PLoS Comput. Biol., 5, 2009, e1000291.
8. Burgess, N., Grid cells and theta as oscillatory interference: theory and predictions. Hippocampus 18 (2008), 1157–1174.
9. Burgess, N., Barry, C., O'Keefe, J., An oscillatory interference model of grid cell firing. Hippocampus 17 (2007), 801–812.
10. Bush, D., Burgess, N., A hybrid oscillatory interference/continuous attractor network model of grid cell firing. J. Neurosci. 34 (2014), 5065–5079.
11. Buzsáki, G., Theta oscillations in the hippocampus. Neuron 33 (2002), 325–340.
12. Chevaleyre, V., Siegelbaum, S.A., Strong CA2 pyramidal neuron synapses define a powerful disynaptic cortico-hippocampal loop. Neuron 66 (2010), 560–572.
13. Cho, J., Sharp, P.E., Head direction, place, and movement correlates for cells in the rat retrosplenial cortex. Behav. Neurosci. 115 (2001), 3–25.
14. Climer, J.R., DiTullio, R., Newman, E.L., Hasselmo, M.E., Eden, U.T., Examination of rhythmicity of extracellularly recorded neurons in the entorhinal cortex. Hippocampus 25 (2015), 460–473.
15. Csicsvari, J., Hirase, H., Czurkó, A., Mamiya, A., Buzsáki, G., Oscillatory coupling of hippocampal pyramidal cells and interneurons in the behaving Rat. J. Neurosci. 19 (1999), 274–287.
16. Czurkó, A., Huxter, J., Li, Y., Hangya, B., Muller, R.U., Theta phase classification of interneurons in the hippocampal formation of freely moving rats. J. Neurosci. 31 (2011), 2938–2947.
17. Fox, S.E., Wolfson, S., Ranck, J.B. Jr., Hippocampal theta rhythm and the firing of neurons in walking and urethane anesthetized rats. Exp. Brain Res. 62 (1986), 495–508.
18. 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 156 (2014), 1139–1152.
19. Fuhrmann, F., Justus, D., Sosulina, L., Kaneko, H., Beutel, T., Friedrichs, D., Schoch, S., Schwarz, M.K., Fuhrmann, M., Remy, S., Locomotion, theta oscillations, and the speed-correlated firing of hippocampal neurons are controlled by a medial septal glutamatergic circuit. Neuron 86 (2015), 1253–1264.
20. Fuhs, M.C., Touretzky, D.S., A spin glass model of path integration in rat medial entorhinal cortex. J. Neurosci. 26 (2006), 4266–4276.
21. Furtak, S.C., Ahmed, O.J., Burwell, R.D., Single neuron activity and theta modulation in postrhinal cortex during visual object discrimination. Neuron 76 (2012), 976–988.
22. Fyhn, M., Molden, S., Witter, M.P., Moser, E.I., Moser, M.B., Spatial representation in the entorhinal cortex. Science 305 (2004), 1258–1264.
23. Geisler, C., Robbe, D., Zugaro, M., Sirota, A., Buzsáki, G., Hippocampal place cell assemblies are speed-controlled oscillators. Proc. Natl. Acad. Sci. USA 104 (2007), 8149–8154.
24. Guanella, A., Verschure, P.F., A model of grid cells based on path integration mechanism. Kollias, S.D., Stafylopatis, A., Duch, W., Oja, E., (eds.) Artificial Neural Networks–ICANN 2006, 2006, Springer, 740–749.
25. Hafting, T., Fyhn, M., Molden, S., Moser, M.B., Moser, E.I., Microstructure of a spatial map in the entorhinal cortex. Nature 436 (2005), 801–806.
26. Hasselmo, M.E., Grid cell mechanisms and function: contributions of entorhinal persistent spiking and phase resetting. Hippocampus 18 (2008), 1213–1229.
27. Hasselmo, M.E., Neuronal rebound spiking, resonance frequency and theta cycle skipping may contribute to grid cell firing in medial entorhinal cortex. Philos. Trans. R. Soc. Lond. B Biol. Sci., 369, 2013, 20120523.
28. Hasselmo, M.E., Brandon, M.P., A model combining oscillations and attractor dynamics for generation of grid cell firing. Front. Neural Circuits, 6, 2012, 30.
29. Hasselmo, M.E., Shay, C.F., Grid cell firing patterns may arise from feedback interaction between intrinsic rebound spiking and transverse traveling waves with multiple heading angles. Front. Syst. Neurosci., 8, 2014, 201.
30. Hinman, J.R., Penley, S.C., Long, L.L., Escabí, M.A., Chrobak, J.J., Septotemporal variation in dynamics of theta: speed and habituation. J. Neurophysiol. 105 (2011), 2675–2686.
31. Hinman, J.R., Penley, S.C., Escabí, M.A., Chrobak, J.J., Ketamine disrupts theta synchrony across the septotemporal axis of the CA1 region of hippocampus. J. Neurophysiol. 109 (2013), 570–579.
32. Jeewajee, A., Barry, C., O'Keefe, J., Burgess, N., Grid cells and theta as oscillatory interference: electrophysiological data from freely moving rats. Hippocampus 18 (2008), 1175–1185.
33. Kay, K., Sosa, M., Chung, J.E., Karlsson, M.P., Larkin, M.C., Frank, L.M., A hippocampal network for spatial coding during immobility and sleep. Nature 531 (2016), 185–190.
34. Kemere, C., Carr, M.F., Karlsson, M.P., Frank, L.M., Rapid and continuous modulation of hippocampal network state during exploration of new places. PLoS ONE, 8, 2013, e73114.
35. Kempter, R., Leibold, C., Buzsáki, G., Diba, K., Schmidt, R., Quantifying circular-linear associations: hippocampal phase precession. J. Neurosci. Methods 207 (2012), 113–124.
36. 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. 10 (1998), 464–477.
37. Koenig, J., Linder, A.N., Leutgeb, J.K., Leutgeb, S., The spatial periodicity of grid cells is not sustained during reduced theta oscillations. Science 332 (2011), 592–595.
38. Kondo, H., Zaborszky, L., Topographic organization of the basal forebrain projections to the perirhinal, postrhinal, and entorhinal cortex in rats. J. Comp. Neurol. 524 (2016), 2503–2515, 10.1002/cne.23967.
39. Kropff, E., Carmichael, J.E., Moser, M.B., Moser, E.I., Speed cells in the medial entorhinal cortex. Nature 523 (2015), 419–424.
40. 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, 2014, e97987.
41. 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 (2005), 841–852.
42. McFarland, W.L., Teitelbaum, H., Hedges, E.K., Relationship between hippocampal theta activity and running speed in the rat. J. Comp. Physiol. Psychol. 88 (1975), 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. 52 (1983), 41–49.
44. McNaughton, B.L., Battaglia, F.P., Jensen, O., Moser, E.I., Moser, M.B., Path integration and the neural basis of the ‘cognitive map’. Nat. Rev. Neurosci. 7 (2006), 663–678.
45. Mitchell, S.J., Rawlins, J.N., Steward, O., Olton, D.S., Medial septal area lesions disrupt theta rhythm and cholinergic staining in medial entorhinal cortex and produce impaired radial arm maze behavior in rats. J. Neurosci. 2 (1982), 292–302.
46. Mizumori, S.J., Perez, G.M., Alvarado, M.C., Barnes, C.A., McNaughton, B.L., Reversible inactivation of the medial septum differentially affects two forms of learning in rats. Brain Res. 528 (1990), 12–20.
47. Mizuseki, K., Sirota, A., Pastalkova, E., Buzsáki, G., Theta oscillations provide temporal windows for local circuit computation in the entorhinal-hippocampal loop. Neuron 64 (2009), 267–280.
48. Navratilova, Z., Giocomo, L.M., Fellous, J.M., Hasselmo, M.E., McNaughton, B.L., Phase precession and variable spatial scaling in a periodic attractor map model of medial entorhinal grid cells with realistic after-spike dynamics. Hippocampus 22 (2012), 772–789.
49. Newman, E.L., Hasselmo, M.E., Grid cell firing properties vary as a function of theta phase locking preferences in the rat medial entorhinal cortex. Front. Syst. Neurosci., 8, 2014, 193.
50. Niell, C.M., Stryker, M.P., Modulation of visual responses by behavioral state in mouse visual cortex. Neuron 65 (2010), 472–479.
51. Raudies, F., Hasselmo, M.E., Differences in visual-spatial input may underlie different compression properties of firing fields for grid cell modules in medial entorhinal cortex. PLoS Comput. Biol., 11, 2015, e1004596.
52. Rivas, J., Gaztelu, J.M., García-Austt, E., Changes in hippocampal cell discharge patterns and theta rhythm spectral properties as a function of walking velocity in the guinea pig. Exp. Brain Res. 108 (1996), 113–118.
53. Rowland, D.C., Weible, A.P., Wickersham, I.R., Wu, H., Mayford, M., Witter, M.P., Kentros, C.G., Transgenically targeted rabies virus demonstrates a major monosynaptic projection from hippocampal area CA2 to medial entorhinal layer II neurons. J. Neurosci. 33 (2013), 14889–14898.
54. Sargolini, F., Fyhn, M., Hafting, T., McNaughton, B.L., Witter, M.P., Moser, M.B., Moser, E.I., Conjunctive representation of position, direction, and velocity in entorhinal cortex. Science 312 (2006), 758–762.
55. Schmidt-Hieber, C., Häusser, M., Cellular mechanisms of spatial navigation in the medial entorhinal cortex. Nat. Neurosci. 16 (2013), 325–331.
56. Sławińska, U., Kasicki, S., The frequency of rat's hippocampal theta rhythm is related to the speed of locomotion. Brain Res. 796 (1998), 327–331.
57. Stensola, H., Stensola, T., Solstad, T., Frøland, K., Moser, M.B., Moser, E.I., The entorhinal grid map is discretized. Nature 492 (2012), 72–78.
58. Taube, J.S., The head direction signal: origins and sensory-motor integration. Annu. Rev. Neurosci. 30 (2007), 181–207.
59. Vanderwolf, C.H., Hippocampal electrical activity and voluntary movement in the rat. Electroencephalogr. Clin. Neurophysiol. 26 (1969), 407–418.
60. Welday, A.C., Shlifer, I.G., Bloom, M.L., Zhang, K., Blair, H.T., Cosine directional tuning of theta cell burst frequencies: evidence for spatial coding by oscillatory interference. J. Neurosci. 31 (2011), 16157–16176.
61. Whitlock, J.R., Pfuhl, G., Dagslott, N., Moser, M.B., Moser, E.I., Functional split between parietal and entorhinal cortices in the rat. Neuron 73 (2012), 789–802.
62. Wills, T.J., Barry, C., Cacucci, F., The abrupt development of adult-like grid cell firing in the medial entorhinal cortex. Front. Neural Circuits, 6, 2012, 21.
63. Winson, J., Loss of hippocampal theta rhythm results in spatial memory deficit in the rat. Science 201 (1978), 160–163.
64. Winter, S.S., Clark, B.J., Taube, J.S., Spatial navigation. Disruption of the head direction cell network impairs the parahippocampal grid cell signal. Science 347 (2015), 870–874.
65. Yeshenko, O., Guazzelli, A., Mizumori, S.J., Context-dependent reorganization of spatial and movement representations by simultaneously recorded hippocampal and striatal neurons during performance of allocentric and egocentric tasks. Behav. Neurosci. 118 (2004), 751–769.
66. Zhou, T.L., Tamura, R., Kuriwaki, J., Ono, T., Comparison of medial and lateral septal neuron activity during performance of spatial tasks in rats. Hippocampus 9 (1999), 220–234.
67. Zilli, E.A., Models of grid cell spatial firing published 2005-2011. Front. Neural Circuits, 6, 2012, 16.