Spatial navigation and the central complex: Sensory acquisition, orientation, and motor control

Frontiers in Behavioral Neuroscience

Volumn 11, Issue , 2017, Pages

  Varga, Adrienn G ^a   Kathman, Nicholas D ^a   Martin, Joshua P ^b   Guo, Peiyuan ^a   Ritzmann, Roy E ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Colby College   (United States)

Author keywords

Central complex; Head direction cells; Motor activity; Population code; Reflex; Spatial navigation

Indexed keywords

ANIMAL EXPERIMENT; BRAIN REGION; HEAD; INSECT; MOTOR ACTIVITY; MOTOR CONTROL; NERVE CELL; NONHUMAN; REFLEX; SENSORY STIMULATION; SPATIAL ORIENTATION;

EID: 85010841162     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2017.00004     Document Type: Review

References (110)

1. Ache, J. M., Haupt, S., and Dürr,V. (2015). A direct descending pathway informing locomotor networks about tactile sensor movement. J. Neurosci. 35, 4081-4091. doi: 10.1523/JNEUR0SCI.3350-14.2015
2. Akay, T., Bässler, U., Gerharz, P., and Büschges, A. (2001). The role of sensory signals from the insect coxa-trochanteral joint in controlling motor activity of the femur-tibia joint. J. Neurophysiol. 85, 594-604.
3. Akay, T., Haehn, S., Schmitz, J., and Büschges, A. (2004). Signals from load sensors underlie interjoint coordination during stepping movements of the stick insect leg. J. Neurophysiol. 92, 42-51. doi: 10.1152/jn.01271.2003
4. Akay, T., Ludwar, B. C., Goritz, M. L., Schmitz, J., and Büschges, A. (2007). Segment specificity of load signal processing depends on walking direction in the stick insect leg muscle control system. J. Neurosci. 27, 3285-3294. doi: 10.1523/JNEUR0SCI.5202-06.2007
5. Barry, C., Lever, C., Hayman, R., Hartley, T., Burton, S., O'Keefe, J., et al. (2006). The boundary vector cell model of place cell firing and spatial memory. Rev. Neurosci. 17,71-97. doi: 10.1515/REVNEUR0.2006.17.1-2.71
6. Bech, M., Homberg, U., and Pfeiffer, K. (2014). Receptive fields of locust brain neurons are matched to polarization patterns of the sky. Curr. Biol. 24, 2124-2129. doi: 10.1016/j.cub.2014.07.045
7. Bender, J. A., Pollack, A. J., and Ritzmann, R. E. (2010). Neural activity in the central complex of the insect brain is linked to locomotor changes. Curr. Biol. 20, 921-926. doi: 10.1016/j.cub.2010.03.054
8. Bender, J. A., Simpson, E. M., Tietz, B. R., Daltorio, K. A., Quinn, R. D., and Ritzmann, R. E. (2011). Kinematic and behavioral evidence for a distinction between trotting and ambling gaits in the cockroach Blaberus discoidalis. J. Exp. Biol. 214, 2057-2064. doi: 10.1242/jeb.056481
9. Bläesing, B., and Cruse, H. (2004). Mechanisms of stick insect locomotion in a gap-crossing paradigm. J. Comp. Physiol. A. Neuroethol. Sens. Neural. Behav. Physiol. 190, 173-183. doi: 10.1007/s00359-003-0482-3
10. Bockhorst, T., and Homberg, U. (2015). Amplitude and dynamics of polarization- plane signaling in the central complex of the locust brain. J. Neurophsyiol. 113, 3291-3311. doi: 10.1152/jn.00742.2014
11. Bonnevie, T., Dunn, B., Fyhn, M., Hafting, T., Derdikman, D., Kubie, J. L., et al. (2013). Grid cells require excitatory drive from the hippocampus. Nat. Neurosci. 16, 309-317. doi: 10.1038/nn.3311
12. Boyan, G. S., and Liu, Y. (2016). Development of the neurochemical architecture of the central complex. Front. Behav. Neurosci. 10:167. doi: 10.3389/fnbeh.2016.00167
13. Bush, D., Barry, C., and Burgess, N. (2014). What do grid cells contribute to place cell firing? Trends Neurosci. 37, 136-145. doi: 10.1016/j.tins.2013.12.003
14. Bush, D., Barry, C., Manson, D., and Burgess, N. (2015). Using grid cells for navigation. Neuron 87, 507-520. doi: 10.1016/j.neuron.2015.07.006
15. Canonge, S., Sempo, G., Jeanson, R., Detrain, C., and Deneubourg, J. L. (2009). Self-amplification as a source of interindividual variability: shelter selection in cockroaches. J. InsectPhysiol. 55, 976-982. doi: 10.1016/j.jinsphys.2009.06.011
16. Capaldi, E. A., Robinson, G. E. and Fahrbach, S. E. (1999). Neuroethology of spatial learning: the birds and the bees. Annu. Rev. Psychol. 50, 651-682. doi: 10.1146/annurev.psych.50.1.651
17. Collett, M. (2012). How navigational guidance systems are combined in a desert ant. Curr. Biol. 22, 927-932. doi: 10.1016/j.cub.2012.03.049
18. Daltorio, K. A., Tietz, B. R., Bender, J. A., Webster, V. A., Szczecinski, N. S., Branicky, M. S., et al. (2013). A model of exploration and goal- searching in the cockroach, Blaberus discoidalis. Adapt. Behav. 21, 404-420. doi: 10.1177/1059712313491615
19. Devaud, J.-M., Blunk, A., Podufall, J., Giurfa, M., and Grünewald, B. (2007). Using local anaesthetics to block neuronal activity and map specific learning tasks to the mushroom bodies of an insect brain. Eur. J. Neurosci. 26, 3193-3206. doi: 10.1111/j.1460-9568.2007.05904.x
20. Dordek, Y., Soudry, D., Meir, R., and Derdikman, D. (2016). Extracting grid cell characteristics from place cell inputs using non-negative principal component analysis. Elife 5:e10094. doi: 10.7554/eLife.10094
21. Dürr, V., and Ebeling, W. (2005). The behavioural transition from straight to curve walking: kinetics of leg movement parameters and the initiation of turning. J. Exp. Biol. 208, 2237-2252. doi: 10.1242/jeb.01637
22. Dürr, V., König, Y., and Kittmann, R. (2001). The antennal motor system of the stick insect Carausius morosus: anatomy and antennal movement pattern duringwalking. J. Comp. Phsiol.A. 187, 131-144. doi: 10.1007/s003590100183
23. el Jundi, B., Pfeiffer, K., Heinze, S., and Homberg, U. (2014). Integration of polarization and chromatic cues in the insect sky compass. J. Comp. Physiol. A. Neuroethol. Sens. Neural. Behav. Physiol. 200, 575-589. doi: 10.1007/s00359-014-0890-6
24. el Jundi, B., Warrant, E. J., Byrne, M. J., Khaldy, L., Baird, E., Smolka, J., et al. (2015). Neural coding underlying the cue preference for celestial orientation. Proc. Natl. Acad. Sci. U.S.A. 112, 11395-11400. doi: 10.1073/pnas.1501272112
25. Feng, A. Y. T., and Himsworth, C. G. (2014). The secret life of the city rat: a review of the ecology of urban Norway and black rats (Rattus norvegicus and Rattus rattus). UrbanEcosyst. 17,149-162. doi: 10.1007/s11252-013-0305-4
26. Finkelstein, A., Derdikman, D., Rubin, A., Foerster, J. N., Las, L., and Ulanovsky, N. (2011). Three-dimensional head-direction coding in the bat brain. Nature 517, 159-164. doi: 10.1038/nature14031
27. Georgopoulos, A. P. (1995). Current issues in directional motor control. Trends Neurosci. 18, 506-510.doi: 10.1016/0166-2236(95)92775-l
28. Georgopoulos, A. P., Kettner, R. E., and Schwartz, A. B. (1988). Primate motor cortex and free arm movements to visual targets in three- dimensional space. II. Coding of the direction of movement by a neuronal population. J. Neurosci. 8, 2928-2937.
29. Geva-Sagiv, M., Las, L., Yovel, Y., and Ulanovsky, N. (2015). Spatial cognition in bats and rats: from sensory acquisition to multiscale maps and navigation. Nat. Rev. Neurosci. 16, 94-108. doi: 10.1038/nrn3888
30. Goodridge, J. P., Dudchenko, P. A., Worboys, K. A., Golob, E. J., and Taube, J. S. (1998). Cue control and head direction cells. Behav. Neurosci. 112, 749-761. doi: 10.1037/0735-7044.112.4.749
31. Guo, P., Pollack, A. J., Varga, A. G., Martin, J. P., and Ritzmann, R. E. (2014). Extracellular wire tetrode recording in brain of freely walking insects. J. Vis. Exp. 86:e51337. doi: 10.3791/51337
32. Guo, P., and Ritzmann, R. E. (2013). Neural activity in the central complex of the cockroach brain is linked to turning behaviors. J. Exp. Biol. 216, 992-1002. doi: 10.1242/jeb.080473
33. Hafting, T., Fyhn, M., Molden, S., Moser, M.-B., and Moser, E. I. (2005). Microstructure of a spatial map in the entorhinal cortex. Nature 436, 801-806. doi: 10.1038/nature03721
34. Harley, C. M., English, B. A., and Ritzmann, R. E. (2009). Characterization of obstacle negotiation behaviors in the cockroach, Blaberus discoidalis. J. Exp. Biol. 212, 1463-1476. doi: 10.1242/jeb.028381
35. Harley, C. M., and Ritzmann, R. E. (2010). Electrolytic lesions within central complex neuropils of the cockroach brain affect negotiation of barriers. J. Exp. Biol. 213, 2851-2864. doi: 10.1242/jeb.042499
36. Hartley, T., Lever, C., Burgess, N., and O'Keefe, J. (2014). Space in the brain: how the hippocampal formation supports spatial cognition. Philos. Trans. R. Soc. B. 369:20120510. doi: 10.1098/rstb.2012.0510
37. Heinze, S., Gotthardt, S., and Homberg, U. (2009). Transformation of polarized light information in the central complex of the locust. J. Neuorosci. 29, 11783-11793. doi: 10.1523/JNEUR0SCI.1870-09.2009
38. Heinze, S., and Homberg, U. (2007). Maplike representation of celestial E-vector orientations in the brain of an insect. Science 315, 995-997. doi: 10.1126/science.1135531
39. Heinze, S., and Homberg, U. (2008). Neuroarchitecture of the central complex of the desert locust: Intrinsic and columnar neurons. J. Comp. Neurol. 511, 454-478. doi: 10.1002/cne.21842
40. Heinze, S., and Reppert, S. M. (2011). Sun compass integration of Skylight cues in migratory monarch butterflies. Neuron 69, 345-358. doi: 10.1016/j.neuron.2010.12.025
41. Heisenberg, M. (2003). Mushroom body memoir: from maps to models. Nat. Rev. Neurosci. 4, 266-275. doi: 10.1038/nrn1074
42. Hellekes, K., Blincow, E., Hoffmann, J., and Büschges, A. (2012). Control of reflex reversal in stick insect walking: effects of intersegmental signals, changes in direction, and optomotor-induced turning. J. Neurophysiol. 107, 239-249. doi: 10.1152/jn.00718.2011
43. Holling, C. S. (1966). The functional response of invertebrate predators to prey density. Mem. Entomol. Soc. Can. 98, 5-86. doi: 10.4039/entm9848fv
44. Homberg, U., Heinze, S., Pfeiffer, K., Kinoshita, M., and el Jundi, B. (2011). Central neural coding of sky polarization in insects. Philos. Trans. R. Soc. Lond. B. 366, 680-687. doi: 10.1098/rstb.2010.0199
45. Huber, F. (1960). Untersuchungen über die funktion des zentralnervensystems und insbesondere des gehirns bei der fortbewegung und lauterzeugung der grillen. Zeit. Vergleich. Physiol. 44, 60-132. doi: 10.1007/BF00297863
46. Inoue, T., and Matsura, T. (1983). Foraging strategy of a mantid, Paratenodera angustipennis S.: Mechanisms of switching tactics between ambush and active search. Oecologia 56, 264-271. doi: 10.1007/BF00379700
47. Jacobs, L., and Menzel, R. (2014). Navigation outside of the box: what the lab can learn from the field and what the field can learn from the lab. Mov. Ecol. 2:3. doi: 10.1186/2051-3933-2-3
48. Jankowski, M. M., Ronnqvist, K. C., Tsanov, M., Vann, S., Wright, N., Erichsen, J., et al. (2013). The anterior thalamus provides a subcortical circuit supporting memory and spatial navigation. Front. Syst. Neurosci. 7:45. doi: 10.3389/fnsys.2013.00045
49. Kahsai, L., and Winther, A. M. E. (2011). Chemical neuroanatomy of the Drosophila central complex: distribution of multiple neuropeptides in relation to neurotransmitters. J. Comp. Neurol. 519, 290-315. doi: 10.1002/cne.22520
50. Kamikouchi, A., Inagaki, H. K., Effertz, T., Hendrich, O., Fiala, A., Göpfert, M. C., et al. (2009). The neural basis of Drosophila gravity-sensing and hearing. Nature 458, 165-171. doi: 10.1038/nature07810
51. Kathman, N. D., Kesavan, M., and Ritzmann, R. E. (2014). Encoding wide- field motion and direction in the central complex of the cockroach Blaberus discoidalis. J. Exp. Biol. 217,4079-4090. doi: 10.1242/jeb.112391
52. Kropff, E., Carmichael, J. E., Moser, M.-B., and Moser, E. I. (2015). Speed cells in the medial entorhinal cortex. Nature 523, 419-424. doi: 10.1038/nature14622
53. Langston, R. F., Ainge, J. A., Couey, J. J., Canto, C. B., Bjerknes, T. L., Witter, M. P., et al. (2010). Development of the spatial representation system in the rat. Science 328, 1576-1580. doi: 10.1126/science.1188210
54. Lavoie, A. M., and Mizumori, S. J. Y. (1994). Spatial, movement- and reward- sensitive discharge by medial ventral striatum neurons of rats. Brain Res. 638, 157-168. doi: 10.1016/0006-8993(94)90645-9
55. Lever, C., Burton, S., Jeewajee, A., O'Keefe, J., and Burgess, N. (2009). Boundary vector cells in the subiculum of the hippocampal formation. J. Neuorsci. 29, 9771-9777. doi: 10.1523/JNEUR0SCI.1319-09.2009
56. Liu, G., Seiler, H., Wen, A., Zars, T., Ito, K., Wolf, R., et al. (2006). Distinct memory traces for two visual features in the Drosophila brain. Nature 439, 551-556. doi: 10.1038/nature04381
57. Martin, J. P., Guo, P., Mu, L., Harley, C. M., and Ritzmann, R. E. (2015). Central- complex control of movement in the freely walking cockroach. Curr. Biol. 25, 1-9. doi: 10.1016/j.cub.2015.09.044
58. Matsuo, E., Yamada, D., Ishikawa, Y., Asai, T., Ishimoto, H., and Kamikouchi, A. (2014). Identification of novel vibration- and deflection-sensitive neuronal subgroups in Johnston's organ of the fruit fly. Front. Physiol. 5:179. doi: 10.3389/fphys.2014.00179
59. Mcgeorge, A. J., and Faull, R. L. M. (1989). The organization of the projection from the cerebral cortex to the striatum in the rat. Neuroscience 29, 503-537. doi: 10.1016/0306-4522(89)90128-0
60. McNaughton, B. L., Battaglia, F. P., Jensen, O., Moser, E. I., and Moser, M. B. (2006). Path integration and the neural basis of the “cognitive map.” Nat. Rev. Neurosci. 7, 663-678. doi: 10.1038/nrn1932
61. Menzel, R. (2014). The insect mushroom body, an experience-dependent recoding device. J. Physiol. Paris 108, 84-95. doi: 10.1016/j.jphysparis.2014.07.004
62. Meyer, D. J., Margiotta, J. F., and Walcott, B. (1981). The shadow response of the cockroach, Periplaneta americana. J. Neurobiol. 12, 93-96. doi: 10.1002/neu.480120109
63. Mizumori, S. J. Y., Puryear, C. B., and Martig, A. K. (2009). Basal ganglia contributions to adaptive navigation. Behav. Brain Res. 199, 32-42. doi: 10.1016/j.bbr.2008.11.014
64. Mizumori, S. J. Y., Ragozzino, K. E., and Cooper, B. G. (2000). Location and head direction representation in the dorsal striatum of rats. Psychobiology 28, 441-462. doi: 10.3758/BF03332003
65. Mizunami, M., Weibrecht, J. M., and Strausfeld, N. J. (1998). Mushroom bodies of the cockroach: their participation in place memory. J. Comp. Neurol. 402, 520-537. doi: 10.1002/(SICI)1096-9861(19981228)402:4<520::AID-CNE6>3.0.C0;2-Ky
66. Morris, G. M. (1981). Spatial localization does not require the presence of local cues. Learn. Motiv. 12, 239-260. doi: 10.1016/0023-9690(81)90020-5
67. Morris, R. G., Garrud, P., Rawlins, J. N., and O'Keefe, J. (1982). Place navigation impaired in rats with hippocampal lesions. Nature 297, 681-683. doi: 10.1038/297681a0
68. Moser, E. I., Kropff, E., and Moser, M. B. (2008). Place cells, grid cells, and the brain's spatial representation system. Annu. Rev. Neurosci. 31, 69-89 doi: 10.1146/annurev.neuro.31.061307.090723
69. Moser, E. I., Moser, M. B., and Roudi, Y. (2013). Network mechanisms of grid cells. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 369:20120511. doi: 10.1098/rstb.2012.0511
70. Mu, L., and Ritzmann, R. E. (2005). Kinematics and motor activity during tethered walking and turning in the cockroach, Blaberus discoidalis. J. Comp. Physiol. A. Neuroethol. Sens. Neural. Behav. Physiol. 191, 1037-1054. doi: 10.1007/s00359-005-0029-x
71. Mu, L., and Ritzmann, R. E. (2008). Interaction between descending input and local thoracic reflexes for joint coordination in cockroach turning: I. Descending influence on thoracic sensory reflexes. J. Comp. Physiol. A 194, 283-298. doi: 10.1007/s00359-007-0307-x
72. Neuser, K., Triphan, T., Mronz, M., Poeck, B., and Strauss, R. (2008). Analysis of a spatial orientation memory in Drosophila. Nature 453, 1244-1247. doi: 10.1038/nature07003
73. Ofstad, T. A., Zuker, C. S., and Reiser, M. B. (2011). Visual place learning in Drosophila melanogaster. Nature474, 204-207. doi: 10.1038/nature10131
74. Okada, J., and Toh, Y. (1998). Shade Response in the escape behavior of the Cockroach, Periplaneta americana. Zool. Sci. 15, 831-835. doi: 10.2108/zsj.15.831
75. Okada, J., and Toh, Y. (2000). The role of antennal hair plates in object- guided tactile orientation of the cockroach (Periplaneta americana). J. Comp. Physiol. A. Neuroethol. Sens. Neural. Behav. Physiol. 186, 849-857. doi: 10.1007/s003590000137
76. O'Keefe, J., and Dostrovsky, J. (1971). The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res. 34, 171-175. doi: 10.1016/0006-8993(71)90358-1
77. Pan, Y., Zhou, Y., Guo, C., Gong, H., Gong, Z., and Liu, L. (2009). Differential roles of the fan-shaped body and the ellipsoid body in Drosophila visual pattern memory. Learn. Mem. 16, 289-295. doi: 10.1101/lm.1331809
78. Paulsen, O., and Moser, E. I. (1998). A model of hippocampal memory encoding and rerieval: GABAergic control of synaptic plasticity. Trends Neurosci. 21, 273-278. doi: 10.1016/s0166-2236(97)01205-8
79. Paxinos, G., and Watson, C. (1996). The Rat Brain in Stereotaxic Coordinates. San Diego, CA: Academic Press. Penner, M. R., and Mizumori, S. J. Y. (2012). Neural systems analysis of decision making during goal-directed navigation. Prog. Neurobiol. 96, 96-135. doi: 10.1016/j.pneurobio.2011.08.010
80. Pfeiffer, K., and Homberg, U. (2014). Organization and functional roles of the central complex in the insect brain. Annu. Rev. Entomol. 59, 165-184. doi: 10.1146/annurev-ento-011613-162031
81. Reppert, S. M., Gegear, R. J., and Merlin, C. (2010). Navigational mechanisms of migrating monarch butterflies. Trends Neurosci. 33, 399-406. doi: 10.1016/j.tins.2010.04.004
82. Reppert, S. M., Guerra, P. A., and Merlin, C. (2016). Neurobiology of monarch butterfly migration. Annu. Rev. Entomol. 61, 25-42. doi: 10.1146/annurev-ento-010814-020855
83. Ritzmann, R. E., Harley, C. M., Daltorio, K. A., Tietz, B. R., Pollack, A. J., Bender, J. A., et al. (2012). Deciding which way to go: how do insects alter movements to negotiate barriers? Front. Neurosci. 6:97. doi: 10.3389/fnins.2012.00097
84. Ritzmann, R. E., Ridgel, A. L., and Pollack, A. J. (2008). Multi-unit recording of antennal mechanosensitive units in the central complex of the cockroach, Blaberus discoidalis. J. Comp. Physiol. A. Neuroethol. Sens. Neural. Behav. Physiol. 194, 341-360. doi: 10.1007/s00359-007-0310-2
85. Rosner, R., and Homberg, U. (2013). Widespread sensitivityto looming stimuli and small moving objects in the central complex of an insect brain. J. Neurosci. 33, 8122-8133. doi: 10.1523/JNEUR0SCI.5390-12.2013
86. Roth, L. M., and Willis, E. R. (1960). The biotic associations of cockroaches. Smithson Misc. Collect. 141, 1-470.
87. Rowland, D. C., Roudi, Y., Moser, M.-B., and Moser, E. I. (2016). Ten years of grid cells. Ann. Rev. Neurosci. 39, 19-40. doi: 10.1146/annurev-neuro-070815-013824
88. Rubin, A., Yartsev, M. M., and Ulanovsky, N. (2014). Encoding of head direction by hippocampal place cells in bats. J. Neuorsci. 34, 1067-1080. doi: 10.1523/JNEUROSCI.5393-12.2014
89. Sakura, M., Lambrinos, D., and Labhart, T. (2008). Polarized skylight navigation in insects: model and electrophysiology of e-vector coding by neurons in the central complex. J. Neuorophysiol. 99, 667-682. doi: 10.1152/jn.00784.2007
90. Savelli, F., Yoganarasimha, D., and Knierim, J. J. (2008). Influence of boundary removal on the spatial representations of the medial entorhinal cortex Hippocampus 18, 1270-1282. doi: 10.1002/hipo.20511
91. Schiller, D., Eichenbaum, H., Buffalo, E. A., Davachi, L., Foster, D. J., Leutgeb, S., et al. (2015). Memory and space: towards an understanding of the cognitive map. J. Neuorsci. 35, 13904-13911. doi: 10.1523/JNEUR0SCI.2618-15.2015
92. Schmitzer-Torbert, N., and Redish, A. D. (2004). Neuronal activity in the rodent dorsal striatum in sequential navigation: Separation of spatial and reward responses on the multiple T task. J. Neurophysiol. 91, 2259-2272. doi: 10.1152/jn.00687.2003
93. Schwartz, A. B., Kettner, R. E., and Georgopoulos, A. P. (1988). Primate motor cortex and free arm movements to visual targets in three- dimensional space. I. Relations between single cell discharge and direction of movement. J. Neurosci. 8, 2913-2927.
94. Seelig, J. D., and Jayaraman, V. (2013). Feature detection and orientation tuning in the Drosophila central complex. Nature 503, 262-266. doi: 10.1038/nature12601
95. Seelig, J. D., and Jayaraman, V. (2015). Neural dynamics for landmark orientation and angular path integration. Nature 521, 186-191. doi: 10.1038/nature14446
96. Solstad, T., Boccara, C. N., Kropff, E., Moser, M.-B., and Moser, E. I. (2008). Representation of geometric borders in the entorhinal cortex. Science 322, 1865-1868. doi: 10.1126/science.1166466
97. Strausfeld, N. J., and Hirth, F. (2013). Deep homology of arthropod central complex and vertebrate basal ganglia. Science 340, 157-161. doi: 10.1126/science.1231828
98. Taube, J. S. (2007). The head direction signal: 0rigins and sensory-motor integration. Ann. Rev. Neurosci. 30, 181-207. doi: 10.1146/annurev.neuro.29.051605.112854
99. Taube, J. S., and Burton, H. L. (1995). Head direction cell activity monitored in a novel environment and during a cue conflict situation. J. Neurophysiol. 74, 1953-1971.
100. Taube, J. S., Muller, R. U., and Ranck, J. B. (1990a). Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis. J. Neurosci. 10, 420-435.
101. Taube, J. S., Muller, R. U., and Ranck, J. B. (1990b). Head-direction cells recorded from the postsubiculum in freely moving rats. II. Effects of environmental manipulations. J. Neurosci. 10, 436-447.
102. Varga, A. G., and Ritzmann, R. E. (2016). Cellular basis of head direction and contextual cues in the insect brain. Curr. Biol. 26, 1816-1828. doi: 10.1016/j.cub.2016.05.037
103. Weir, P., Schnell, B., and Dickinson, M. (2014). Central complex neurons exhibit behaviorallygated responsesto visual motion in Drosophila. J. Neurophysiol. 11, 62-71. doi: 10.1152/jn.00593.2013
104. Whitlock, J., Sutherland, R., Witter, M., Moser, M., and Moser, E. (2008). Navigating from hippocampus to parietal cortex. Proc. Natl. Acad. Sci. U.S.A. 105, 14755-14762. doi: 10.1073/pnas.0804216105
105. Wills, T. J., Cacucci, F., Burgess, N., and O'Keefe, J. (2010). Development of the hippocampal cognitive map in preweanling rats. Science 328, 1573-1576. doi: 10.1126/science.1188224
106. Winter, S. S., Clark, B. J., and Taube, J. S. (2015). Disruption of the head direction cell network impairs the parahippocampal grid cell signal. Science 347, 870-874. doi: 10.1126/science.1259591
107. Witter, M. P., and Amaral, D. G. (2004). “Hippocampal formation" in The Rat Nervous System, ed G. Paxinos (San Diego, CA: Elsevier), 635-704.
108. Yartsev, M. M., and Ulanovsky, N. (2013). Representation of threedimensional space in the hippocampus of flying bats. Science 340, 367-372. doi: 10.1126/science.1235338
109. Yoganarasimha, D., Yu, X., and Knierim, J. J. (2006). Head direction cell representations maintain internal coherence during conflicting proximal and distal cue rotations: Comparison with hippocampal place cells. J. Neurosci. 26, 622-631. doi: 10.1523/JNEUR0SCI.3885-05.2006
110. Yorozu, S., Wong, A., Fischer, B. J., Dankert, H., Kernan, M. J., Kamikouchi, A., et al. (2009). Distinct sensory representations of wind and near-field sound in the Drosophila brain. Nature 458, 201-205. doi: 10.1038/nature07843