Hippocampal global remapping for different sensory modalities in flying bats

Nature Neuroscience

Volumn 19, Issue 7, 2016, Pages 952-958

  Geva Sagiv, Maya ^a,b   Romani, Sandro ^c   Las, Liora ^a   Ulanovsky, Nachum ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; BRAIN MAPPING; COGNITION; CONTROLLED STUDY; ECHOLOCATION; HIPPOCAMPAL CA1 REGION; INTERNEURON; MALE; NONHUMAN; PRIORITY JOURNAL; ROUSETTUS AEGYPTIACUS; SUBICULUM; THEORETICAL MODEL; VISION; ANIMAL; ANIMAL BEHAVIOR; BAT; DEPTH PERCEPTION; HIPPOCAMPUS; MEMORY; NERVE CELL; NERVE CELL NETWORK; PHYSIOLOGY;

ANIMALS; BEHAVIOR, ANIMAL; CHIROPTERA; HIPPOCAMPUS; MEMORY; NERVE NET; NEURONS; SPACE PERCEPTION;

EID: 84973097777     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.4310     Document Type: Article

References (52)

1. O'Keefe, J., & Nadel L The Hippocampus as a Cognitive Map (Oxford University Press, 1978).
2. Eichenbaum, H., & Cohen, N.J. Can we reconcile the declarative memory and spatial navigation views on hippocampal function?. Neuron 83, 764-770 (2014).
3. Wilson, M.A., & McNaughton, B.L. Dynamics of the hippocampal ensemble code for space. Science 261, 1055-1058 (1993).
4. Leutgeb, S., Leutgeb, J.K., Treves, A., Moser, M.-B., & Moser, E.I. Distinct ensemble codes in hippocampal areas CA3 and CA1. Science 305, 1295-1298 (2004).
5. McHugh, T.J., Blum, K.I., Tsien, J.Z., Tonegawa, S., & Wilson, M.A. Impaired hippocampal representation of space in CA1-specific NMDAR1 knockout mice. Cell 87, 1339-1349 (1996).
6. Ono, T., Nakamura, K., Nishijo, H., & Eifuku, S. Monkey hippocampal neurons related to spatial and nonspatial functions. J. Neurophysiol. 70, 1516-1529 (1993).
7. Ekstrom, A.D. et al. Cellular networks underlying human spatial navigation. Nature 425, 184-188 (2003).
8. Ulanovsky, N., & Moss, C.F. Hippocampal cellular and network activity in freely moving echolocating bats. Nat. Neurosci. 10, 224-233 (2007).
9. Ulanovsky, N., & Moss, C.F. Dynamics of hippocampal spatial representation in echolocating bats. Hippocampus 21, 150-161 (2011).
10. Yartsev, M.M., Witter, M.P., & Ulanovsky, N. Grid cells without theta oscillations in the entorhinal cortex of bats. Nature 479, 103-107 (2011).
11. Yartsev, M.M., & Ulanovsky, N. Representation of three-dimensional space in the hippocampus of flying bats. Science 340, 367-372 (2013).
12. Quirk, G.J., Muller, R.U., & Kubie, J.L. The firing of hippocampal place cells in the dark depends on the rat?s recent experience. J. Neurosci. 10, 2008-2017 (1990).
13. Markus, E.J., Barnes, C.A., McNaughton, B.L., Gladden, V.L., & Skaggs, W.E. Spatial information content and reliability of hippocampal CA1 neurons: effects of visual input. Hippocampus 4, 410-421 (1994).
14. Save, E., Nerad, L., & Poucet, B. Contribution of multiple sensory information to place field stability in hippocampal place cells. Hippocampus 10, 64-76 (2000).
15. Heffner, R.S., Koay, G., & Heffner, H.E. Sound localization in an Old-World fruit bat (Rousettus aegyptiacus): acuity, use of binaural cues, and relationship to vision. J. Comp. Psychol. 113, 297-306 (1999).
16. Yovel, Y., Falk, B., Moss, C.F., & Ulanovsky, N. Optimal localization by pointing off axis. Science 327, 701-704 (2010).
17. Yovel, Y., Geva-Sagiv, M., & Ulanovsky, N. Click-based echolocation in bats: not so primitive after all. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 197, 515-530 (2011).
18. Geva-Sagiv, M., Las, L., Yovel, Y., & Ulanovsky, N. Spatial cognition in bats and rats: from sensory acquisition to multiscale maps and navigation. Nat. Rev. Neurosci. 16, 94-108 (2015).
19. Danilovich S. et al. Bats regulate biosonar based on the availability of visual information. Curr. Biol. 25, R1124-R1125 (2015).
20. Sharp, P.E., & Green, C. Spatial correlates of firing patterns of single cells in the subiculum of the freely moving rat. J. Neurosci. 14, 2339-2356 (1994).
21. Kim, S.M., Ganguli, S., & Frank, L.M. Spatial information outflow from the hippocampal circuit: distributed spatial coding and phase precession in the subiculum. J. Neurosci. 32, 11539-11558 (2012).
22. Csicsvari, J., Hirase, H., Czurko, A., & Buzsáki, G. Reliability and state dependence of pyramidal cell-interneuron synapses in the hippocampus: an ensemble approach in the behaving rat. Neuron 21, 179-189 (1998).
23. Kjelstrup, K.B. et al. Finite scale of spatial representation in the hippocampus. Science 321, 140-143 (2008).
24. Rubin, A., Yartsev, M.M., & Ulanovsky, N. Encoding of head direction by hippocampal place cells in bats. J. Neurosci. 34, 1067-1080 (2014).
25. 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, 41-49 (1983).
26. Hollup, S.A., Molden, S., Donnett, J.G., Moser, M.-B., & Moser, E.I. Accumulation of hippocampal place fields at the goal location in an annular watermaze task. J. Neurosci. 21, 1635-1644 (2001).
27. Ravassard P. et al. Multisensory control of hippocampal spatiotemporal selectivity. Science 340, 1342-1346 (2013).
28. Boonman, A., Bar-On, Y., Cvikel, N., & Yovel, Y. It's not black or white-on the range of vision and echolocation in echolocating bats. Front. Physiol. 4, 248 (2013).
29. Fyhn, M., Hafting, T., Treves, A., Moser, M.-B., & Moser, E.I. Hippocampal remapping and grid realignment in entorhinal cortex. Nature 446, 190-194 (2007).
30. Hartley, T., Burgess, N., Lever, C., Cacucci, F., & O'Keefe, J. Modeling place fields in terms of the cortical inputs to the hippocampus. Hippocampus 10, 369-379 (2000).
31. Sheynikhovich, D., Chavarriaga, R., Strösslin, T., Arleo, A., & Gerstner, W. Is there a geometric module for spatial orientation?. Insights from a rodent navigation model. Psychol. Rev. 116, 540-566 (2009).
32. Romani, S., & Tsodyks, M. Short-term plasticity based network model of place cells dynamics. Hippocampus 25, 94-105 (2015).
33. Barry C. et al. The boundary vector cell model of place cell firing and spatial memory. Rev. Neurosci. 17, 71-97 (2006).
34. Strösslin, T., Sheynikhovich, D., Chavarriaga, R., & Gerstner, W. Robust self-localisation and navigation based on hippocampal place cells. Neural Netw. 18, 1125-1140 (2005).
35. 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, 663-678 (2006).
36. Nitz, D., & McNaughton, B. Differential modulation of CA1 and dentate gyrus interneurons during exploration of novel environments. J. Neurophysiol. 91, 863-872 (2004).
37. Frank, L.M., Stanley, G.B., & Brown, E.N. Hippocampal plasticity across multiple days of exposure to novel environments. J. Neurosci. 24, 7681-7689 (2004).
38. Dupret, D., O'Neill, J., & Csicsvari, J. Dynamic reconfiguration of hippocampal interneuron circuits during spatial learning. Neuron 78, 166-180 (2013).
39. Harris, E., Witter, M.P., Weinstein, G., & Stewart, M. Intrinsic connectivity of the rat subiculum: I. Dendritic morphology and patterns of axonal arborization by pyramidal neurons. J. Comp. Neurol. 435, 490-505 (2001).
40. Amaral, D., & Lavenex, P. in The Hippocampus Book eds. Andersen, P., Morris, R.G., Amaral, D.G., Bliss, T.V., & O'Keefe, J.) 37-115 (Oxford University Press, 2007).
41. Redish, A.D Beyond the Cognitive Map: From Place Cells to Episodic Memory (MIT Press, 1999
42. 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).
43. Samsonovich, A., & McNaughton, B.L. Path integration and cognitive mapping in a continuous attractor neural network model. J. Neurosci. 17, 5900-5920 (1997).
44. Schmitzer-Torbert, N., Jackson, J., Henze, D., Harris, K., & Redish, A.D. Quantitative measures of cluster quality for use in extracellular recordings. Neuroscience 131, 1-11 (2005).
45. Wilent, W.B., & Nitz, D.A. Discrete place fields of hippocampal formation interneurons. J. Neurophysiol. 97, 4152-4161 (2007).
46. Skaggs, W.E., McNaughton, B.L., Wilson, M.A., & Markus, E.J. in Advances in Neural Information Processing Systems 5 eds. Hanson, S.J., Cowan, J.D., & Giles, C.L.) 1030-1037 (Morgan Kaufman, San Mateo, California, USA, 1993).
47. Muller, R.U., Kubie, J.L., & Ranck, J.B. Jr. Spatial firing patterns of hippocampal complex-spike cells in a fixed environment. J. Neurosci. 7, 1935-1950 (1987).
48. Skaggs, W.E., McNaughton, B.L., Wilson, M.A., & Barnes, C.A. Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus 6, 149-172 (1996).
49. Alme, C.B. et al. Place cells in the hippocampus: eleven maps for eleven rooms. Proc. Natl. Acad. Sci. USA 111, 18428-18435 (2014).
50. Healy, K., McNally, L., Ruxton, G.D., Cooper, N., & Jackson, A.L. Metabolic rate and body size are linked with perception of temporal information. Anim. Behav. 86, 685-696 (2013).
51. Goldberg, J.A., Rokni, U., & Sompolinsky, H. Patterns of ongoing activity and the functional architecture of the primary visual cortex. Neuron 42, 489-500 (2004).
52. Itskov, V., Hansel, D., & Tsodyks, M. Short-term facilitation may stabilize parametric working memory trace. Front. Comput. Neurosci. 5, 40 (2011).