Impaired spatial selectivity and intact phase precession in two-dimensional virtual reality

Nature Neuroscience

Volumn 18, Issue 1, 2015, Pages 121-128

  Aghajan, Zahra M ^a   Acharya, Lavanya ^a   Moore, Jason J ^a   Cushman, Jesse D ^a   Vuong, Cliff ^a   Mehta, Mayank R ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASSOCIATION; CONTROLLED STUDY; DEPTH PERCEPTION; FORAGING; HEAD MOVEMENT; HIPPOCAMPUS; HIPPOCAMPUS POTENTIAL; LOCOMOTION; MALE; MAZE TEST; NERVE CELL; NERVE POTENTIAL; NONHUMAN; OPTIC FLOW; PRIORITY JOURNAL; RAT; REWARD; SPATIAL BEHAVIOR; SPATIAL LEARNING; SPATIAL SELECTIVITY; SPIKE; TASK PERFORMANCE; THETA RHYTHM; VIRTUAL REALITY; ANIMAL; COMPUTER GRAPHICS; COMPUTER INTERFACE; ELECTROPHYSIOLOGY; LONG EVANS RAT; MOTIVATION; PHOTOSTIMULATION; PHYSIOLOGY; PSYCHOMOTOR PERFORMANCE;

ANIMALS; COMPUTER GRAPHICS; ELECTROPHYSIOLOGICAL PROCESSES; GOALS; HIPPOCAMPUS; LOCOMOTION; MALE; PHOTIC STIMULATION; PSYCHOMOTOR PERFORMANCE; RATS; RATS, LONG-EVANS; SPACE PERCEPTION; USER-COMPUTER INTERFACE;

EID: 84925284639     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.3884     Document Type: Article

References (53)

1. O'Keefe, J. & Dostrovsky, J. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res. 34, 171-175 (1971).
2. O'Keefe, J. & Nadel, L. The Hippocampus as a Cognitive Map (Clarendon Press, 1978).
3. Muller, R.U. & Kubie, J.L. The effects of changes in the environment on the spatial fring of hippocampal complex-spike cells. J. Neurosci. 7, 1951-1968 (1987).
4. Shapiro, M.L., Tanila, H. & Eichenbaum, H. Cues that hippocampal place cells encode: dynamic and hierarchical representation of local and distal stimuli. Hippocampus 7, 624-642 (1997).
5. Knierim, J.J. Dynamic interactions between local surface cues, distal landmarks, and intrinsic circuitry in hippocampal place cells. J. Neurosci. 22, 6254-6264 (2002).
6. O'Keefe, J. & Conway, D.H. Hippocampal place units in the freely moving rat: why they fre where they fre. Exp. Brain Res. 31, 573-590 (1978).
7. Save, E., Nerad, L. & Poucet, B. Contribution of multiple sensory information to place feld stability in hippocampal place cells. Hippocampus 10, 64-76 (2000).
8. Battaglia, F.P., Sutherland, G.R. & McNaughton, B.L. Local sensory cues and place cell directionality: additional evidence of prospective coding in the hippocampus. J. Neurosci. 24, 4541-4550 (2004).
9. Anderson, M.I. & Jeffery, K.J. Heterogeneous modulation of place cell fring by changes in context. J. Neurosci. 23, 8827-8835 (2003).
10. Aikath, D., Weible, A.P., Rowland, D.C. & Kentros, C.G. Role of self-generated odor cues in contextual representation. Hippocampus 24, 1039-1051 (2014).
11. Gothard, K.M., Skaggs, W.E. & McNaughton, B.L. Dynamics of mismatch correction in the hippocampal ensemble code for space: interaction between path integration and environmental cues. J. Neurosci. 16, 8027-8040 (1996).
12. Markus, E.J. et al. Interactions between location and task affect the spatial and directional fring of hippocampal neurons. J. Neurosci. 15, 7079-7094 (1995).
13. Terrazas, A. et al. Self-motion and the hippocampal spatial metric. J. Neurosci. 25, 8085-8096 (2005).
14. Stackman, R.W. & Taube, J.S. Firing properties of head direction cells in the rat anterior thalamic nucleus: dependence on vestibular input. J. Neurosci. 17, 4349-4358 (1997).
15. Stackman, R.W., Clark, A.S. & Taube, J.S. Hippocampal spatial representations require vestibular input. Hippocampus 12, 291-303 (2002).
16. Calton, J.L. et al. Hippocampal place cell instability after lesions of the head direction cell network. J. Neurosci. 23, 9719-9731 (2003).
17. Angelaki, D.E. & Cullen, K.E. Vestibular system: the many facets of a multimodal sense. Annu. Rev. Neurosci. 31, 125-150 (2008).
18. O'Keefe, J. & Recce, M.L. Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3, 317-330 (1993).
19. Mehta, M.R., Lee, A.K. & Wilson, M.A. Role of experience and oscillations in transforming a rate code into a temporal code. Nature 417, 741-746 (2002).
20. Huxter, J.R., Senior, T.J., Allen, K. & Csicsvari, J. Theta phase-specifc codes for two-dimensional position, trajectory and heading in the hippocampus. Nat. Neurosci. 11, 587-594 (2008).
21. Ravassard, P. et al. Multisensory control of hippocampal spatiotemporal selectivity. Science 340, 1342-1346 (2013).
22. Pastalkova, E., Itskov, V., Amarasingham, A., Buzsaki, G. & Buzsáki, G. Internally generated cell assembly sequences in the rat hippocampus. Science 321, 1322-1327 (2008).
23. MacDonald, C.J., Lepage, K.Q., Eden, U.T. & Eichenbaum, H. Hippocampal "time cells" bridge the gap in memory for discontiguous events. Neuron 71, 737-749 (2011).
24. Jezek, K., Henriksen, E.J., Treves, A., Moser, E.I. & Moser, M.-B. Theta-paced fickering between place-cell maps in the hippocampus. Nature 478, 246-249 (2011).
25. Hahn, T.T.G., McFarland, J.M., Berberich, S., Sakmann, B. & Mehta, M.R. Spontaneous persistent activity in entorhinal cortex modulates cortico-hippocampal interaction in vivo. Nat. Neurosci. 15, 1531-1538 (2012).
26. Miller, J.F. et al. Neural activity in human hippocampal formation reveals the spatial context of retrieved memories. Science 342, 1111-1114 (2013).
27. Ekstrom, A.D. et al. Cellular networks underlying human spatial navigation. Nature 425, 184-188 (2003).
28. Jacobs, J., Kahana, M.J., Ekstrom, A.D., Mollison, M.V. & Fried, I. A sense of direction in human entorhinal cortex. Proc. Natl. Acad. Sci. USA 107, 6487-6492 (2010).
29. Rolls, E.T. Spatial view cells and the representation of place in the primate hippocampus. Hippocampus 9, 467-480 (1999).
30. Dombeck, D.A., Harvey, C.D., Tian, L., Looger, L.L. & Tank, D.W. Functional imaging of hippocampal place cells at cellular resolution during virtual navigation. Nat. Neurosci. 13, 1433-1440 (2010).
31. Harvey, C.D., Collman, F., Dombeck, D.A. & Tank, D.W. Intracellular dynamics of hippocampal place cells during virtual navigation. Nature 461, 941-946 (2009).
32. Schmidt-Hieber, C. & Häusser, M. Cellular mechanisms of spatial navigation in the medial entorhinal cortex. Nat. Neurosci. 16, 325-331 (2013).
33. Chen, G., King, J.A., Burgess, N. & O'Keefe, J. How vision and movement combine in the hippocampal place code. Proc. Natl. Acad. Sci. USA 110, 378-383 (2013).
34. Cei, A., Girardeau, G., Drieu, C., El Kanbi, K. & Zugaro, M. Reversed theta sequences of hippocampal cell assemblies during backward travel. Nat. Neurosci. 17, 719-724 (2014).
35. Hölscher, C., Schnee, A., Dahmen, H., Setia, L. & Mallot, H.A. Rats are able to navigate in virtual environments. J. Exp. Biol. 208, 561-569 (2005).
36. Cushman, J.D. et al. Multisensory control of multimodal behavior: do the legs know what the tongue is doing? PLoS ONE 8, e80465 (2013).
37. Aronov, D. & Tank, D.W. Engagement of neural circuits underlying 2D spatial navigation in a rodent virtual reality system. Neuron 84, 442-456 (2014).
38. Hafting, T., Fyhn, M., Bonnevie, T., Moser, M.B. & Moser, E.I. Hippocampus-independent phase precession in entorhinal grid cells. Nature 453, 1248-1252 (2008).
39. Mehta, M.R. Neuronal dynamics of predictive coding. Neuroscientist 7, 490-495 (2001).
40. Cheng, J. & Ji, D. Rigid fring sequences undermine spatial memory codes in a neurodegenerative mouse model. Elife 2, e00647 (2013).
41. Louie, K. & Wilson, M.A. Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep. Neuron 29, 145-156 (2001).
42. Gelbard-Sagiv, H., Mukamel, R., Harel, M., Malach, R. & Fried, I. Internally generated reactivation of single neurons in human hippocampus during free recall. Science 322, 96-101 (2008).
43. Hahn, T.T.G., McFarland, J.M., Berberich, S., Sakmann, B. & Mehta, M.R. Spontaneous persistent activity in entorhinal cortex modulates cortico-hippocampal interaction in vivo. Nat. Neurosci. 15, 1531-1538 (2012).
44. Resnik, E., McFarland, J.M., Sprengel, R., Sakmann, B. & Mehta, M.R. The effects of GluA1 deletion on the hippocampal population code for position. J. Neurosci. 32, 8952-8968 (2012).
45. Mehta, M.R. Contribution of Ih to LTP, place cells, and grid cells. Cell 147, 968-970 (2011).
46. Russell, N.A., Horii, A., Smith, P.F., Darlington, C.L. & Bilkey, D.K. Lesions of the vestibular system disrupt hippocampal theta rhythm in the rat. J. Neurophysiol. 96, 4-14 (2006).
47. Nitz, D.A. Path shape impacts the extent of CA1 pattern recurrence both within and across environments. J. Neurophysiol. 105, 1815-1824 (2011).
48. Mehta, M.R., Quirk, M.C. & Wilson, M.A. Experience-dependent asymmetric shape of hippocampal receptive felds. Neuron 25, 707-715 (2000).
49. Mehta, M.R., Barnes, C.A. & McNaughton, B.L. Experience-dependent, asymmetric expansion of hippocampal place felds. Proc. Natl. Acad. Sci. USA 94, 8918-8921 (1997).
50. Mehta, M.R. & McNaughton, B.L. Expansion and shift of hippocampal place felds: evidence for synaptic potentiation during behavior. in Computational Neuroscience Trends (ed. Bower, J.) 741-745 (Plenum Press, New York, 1996).
51. Vanderwolf, C.H. Hippocampal electrical activity and voluntary movement in the rat. Electroencephalogr. Clin. Neurophysiol. 26, 407-418 (1969).
52. Berens, P. CircStat: a MATLAB toolbox for circular statistics. J. Stat. Softw. 31, 1-21 (2009).
53. Bonnevie, T. et al. Grid cells require excitatory drive from the hippocampus. Nat. Neurosci. 16, 309-317 (2013).