1932

Abstract

Many animals use an internal sense of direction to guide their movements through the world. Neurons selective to head direction are thought to support this directional sense and have been found in a diverse range of species, from insects to primates, highlighting their evolutionary importance. Across species, most head-direction networks share four key properties: a unique representation of direction at all times, persistent activity in the absence of movement, integration of angular velocity to update the representation, and the use of directional cues to correct drift. The dynamics of theorized network structures called ring attractors elegantly account for these properties, but their relationship to brain circuits is unclear. Here, we review experiments in rodents and flies that offer insights into potential neural implementations of ring attractor networks. We suggest that a theory-guided search across model systems for biological mechanisms that enable such dynamics would uncover general principles underlying head-direction circuit function.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-neuro-072116-031516
2020-07-08
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/neuro/43/1/annurev-neuro-072116-031516.html?itemId=/content/journals/10.1146/annurev-neuro-072116-031516&mimeType=html&fmt=ahah

Literature Cited

  1. Allen GV, Hopkins DA. 1988. Mamillary body in the rat: a cytoarchitectonic, Golgi, and ultrastructural study. J. Comp. Neurol. 275:39–64
    [Google Scholar]
  2. Allen GV, Hopkins DA. 1989. Mamillary body in the rat: topography and synaptology of projections from the subicular complex, prefrontal cortex, and midbrain tegmentum. J. Comp. Neurol. 286:311–36
    [Google Scholar]
  3. Amari SI. 1977. Dynamics of pattern formation in lateral-inhibition type neural fields. Biol. Cybern. 27:77–87
    [Google Scholar]
  4. Andrade IV, Riebli N, Nguyen B-CM, Omoto JJ, Cardona A, Hartenstein V 2019. Developmentally arrested precursors of pontine neurons establish an embryonic blueprint of the Drosophila central complex. Curr. Biol. 29:412–25.e3
    [Google Scholar]
  5. Bassett JP, Taube JS. 2001. Neural correlates for angular head velocity in the rat dorsal tegmental nucleus. J. Neurosci. 21:5740–51
    [Google Scholar]
  6. Bassett JP, Wills TJ, Cacucci F 2018. Self-organized attractor dynamics in the developing head direction circuit. Curr. Biol. 28:609–15.e3
    [Google Scholar]
  7. Ben-Yishai R, Bar-Or RL, Sompolinsky H 1995. Theory of orientation tuning in visual cortex. PNAS 92:3844–48
    [Google Scholar]
  8. Bender JA, Pollack AJ, Ritzmann RE 2010. Neural activity in the central complex of the insect brain is linked to locomotor changes. Curr. Biol. 20:921–26
    [Google Scholar]
  9. Bjerknes TL, Langston RF, Kruge IU, Moser EI, Moser MB 2015. Coherence among head direction cells before eye opening in rat pups. Curr. Biol. 25:103–8
    [Google Scholar]
  10. Blair HT. 1996. Simulation of a thalamocortical circuit for computing directional heading in the rat. Advances in Neural Information Processing Systems 8 DS Touretzky, MC Mozer 152–58 San Diego, CA: NeurIPS
    [Google Scholar]
  11. Blair HT, Cho J, Sharp PE 1998. Role of the lateral mammillary nucleus in the rat head direction circuit: a combined single unit recording and lesion study. Neuron 21:1387–97
    [Google Scholar]
  12. Blair HT, Lipscomb BW, Sharp PE 1997. Anticipatory time intervals of head-direction cells in the anterior thalamus of the rat: implications for path integration in the head-direction circuit. J. Neurophysiol. 78:145–59
    [Google Scholar]
  13. Blair HT, Sharp PE. 1995. Anticipatory head direction signals in anterior thalamus: evidence for a thalamocortical circuit that integrates angular head motion to compute head direction. J. Neurosci. 15:6260–70
    [Google Scholar]
  14. Blair HT, Sharp PE. 1996. Visual and vestibular influences on head-direction cells in the anterior thalamus of the rat. Behav. Neurosci. 110:643–60
    [Google Scholar]
  15. Boccara CN, Sargolini F, Thoresen VH, Solstad T, Witter MP et al. 2010. Grid cells in pre- and parasubiculum. Nat. Neurosci. 13:987–94
    [Google Scholar]
  16. Boucheny C, Brunel N, Arleo A 2005. A continuous attractor network model without recurrent excitation: maintenance and integration in the head direction cell system. J. Comput. Neurosci. 18:205–27
    [Google Scholar]
  17. Boyan GS, Reichert H. 2011. Mechanisms for complexity in the brain: generating the insect central complex. Trends Neurosci 34:247–57
    [Google Scholar]
  18. Brockmann A, Basu P, Shakeel M, Murata S, Murashima N et al. 2018. Sugar intake elicits intelligent searching behavior in flies and honey bees. Front. Behav. Neurosci. 12:280
    [Google Scholar]
  19. Butler WN, Smith KS, van der Meer MAA, Taube JS 2017. The head-direction signal plays a functional role as a neural compass during navigation. Curr. Biol. 27:2406
    [Google Scholar]
  20. Butler WN, Taube JS. 2017. Oscillatory synchrony between head direction cells recorded bilaterally in the anterodorsal thalamic nuclei. J. Neurophysiol. 117:1847–52
    [Google Scholar]
  21. Cartwright BA, Collett TS. 1983. Landmark learning in bees: experiments and models. J. Comp. Physiol. 151:521–43
    [Google Scholar]
  22. Chaudhuri R, Gerçek B, Pandey B, Peyrache A, Fiete I 2019. The intrinsic attractor manifold and population dynamics of a canonical cognitive circuit across waking and sleep. Nat. Neurosci. 22:1512–20
    [Google Scholar]
  23. Chen LL, Lin LH, Barnes CA, McNaughton BL 1994. Head-direction cells in the rat posterior cortex. II. Contributions of visual and ideothetic information to the directional firing. Exp. Brain Res. 101:24–34
    [Google Scholar]
  24. Clark BJ, Taube JS. 2012. Vestibular and attractor network basis of the head direction cell signal in subcortical circuits. Front. Neural Circuits 6:7
    [Google Scholar]
  25. Collett M. 2010. How desert ants use a visual landmark for guidance along a habitual route. PNAS 107:11638–43
    [Google Scholar]
  26. Collett M, Chittka L, Collett TS 2013. Spatial memory in insect navigation. Curr. Biol. 23:R789–800
    [Google Scholar]
  27. Collett TS. 2019. Path integration: how details of the honeybee waggle dance and the foraging strategies of desert ants might help in understanding its mechanisms. J. Exp. Biol. 222:jeb205187
    [Google Scholar]
  28. Collett TS, Graham P. 2004. Animal navigation: path integration, visual landmarks and cognitive maps. Curr. Biol. 14:R475–77
    [Google Scholar]
  29. Compte A, Brunel N, Goldman-Rakic PS, Wang XJ 2000. Synaptic mechanisms and network dynamics underlying spatial working memory in a cortical network model. Cereb. Cortex 10:910–23
    [Google Scholar]
  30. Cope AJ, Sabo C, Vasilaki E, Barron AB, Marshall JA 2017. A computational model of the integration of landmarks and motion in the insect central complex. PLOS ONE 12:e0172325
    [Google Scholar]
  31. Corfas RA, Sharma T, Dickinson MH 2019. Diverse food-sensing neurons trigger idiothetic local search in Drosophila. Curr. Biol 29:1660–68.e4
    [Google Scholar]
  32. Cullen KE, Taube JS. 2017. Our sense of direction: progress, controversies and challenges. Nat. Neurosci. 20:1465–73
    [Google Scholar]
  33. Dumont JR, Taube JS. 2015. The neural correlates of navigation beyond the hippocampus. Prog. Brain Res. 219:83–102
    [Google Scholar]
  34. Dus M, Ai M, Suh GSB 2013. Taste-independent nutrient selection is mediated by a brain-specific Na+/solute co-transporter in Drosophila. Nat. . Neurosci 16:526–28
    [Google Scholar]
  35. el Jundi B, Baird E, Byrne MJ, Dacke M 2019. The brain behind straight-line orientation in dung beetles. J. Exp. Biol. 222:jeb192450
    [Google Scholar]
  36. el Jundi B, Pfeiffer K, Heinze S, Homberg U 2014. Integration of polarization and chromatic cues in the insect sky compass. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 200:575–89
    [Google Scholar]
  37. el Jundi B, Warrant EJ, Byrne MJ, Khaldy L, Baird E et al. 2015. Neural coding underlying the cue preference for celestial orientation. PNAS 112:11395–400
    [Google Scholar]
  38. Finkelstein A, Derdikman D, Rubin A, Foerster JN, Las L, Ulanovsky N 2015. Three-dimensional head-direction coding in the bat brain. Nature 517:159–64
    [Google Scholar]
  39. Finkelstein A, Las L, Ulanovsky N 2016. 3-D maps and compasses in the brain. Annu. Rev. Neurosci. 39:171–96
    [Google Scholar]
  40. Finkelstein A, Rouault H, Romani S, Ulanovsky N 2019. Dynamic control of cortical head-direction signal by angular velocity. bioRxiv 730374 https://doi.org/10.1101/730374
    [Crossref]
  41. Fisher YE, Lu J, D'Alessandro I, Wilson RI 2019. Sensorimotor experience remaps visual input to a heading-direction network. Nature 576:121–25
    [Google Scholar]
  42. Franconville R, Beron C, Jayaraman V 2018. Building a functional connectome of the Drosophila central complex. eLife 7:e37017
    [Google Scholar]
  43. Giraldo YM, Leitch KJ, Ros IG, Warren TL, Weir PT, Dickinson MH 2018. Sun navigation requires compass neurons in Drosophila. Curr. Biol 28:172845–52.e4
    [Google Scholar]
  44. Goodridge JP, Dudchenko PA, Worboys KA, Golob EJ, Taube JS 1998. Cue control and head direction cells. Behav. Neurosci. 112:749–61
    [Google Scholar]
  45. Goodridge JP, Taube JS. 1995. Preferential use of the landmark navigational system by head direction cells in rats. Behav. Neurosci. 109:49–61
    [Google Scholar]
  46. Goodridge JP, Taube JS. 1997. Interaction between the postsubiculum and anterior thalamus in the generation of head direction cell activity. J. Neurosci. 17:9315–30
    [Google Scholar]
  47. Goodridge JP, Touretzky DS. 2000. Modeling attractor deformation in the rodent head-direction system. J. Neurophysiol. 83:3402–10
    [Google Scholar]
  48. Green J, Adachi A, Shah KK, Hirokawa JD, Magani PS, Maimon G 2017. A neural circuit architecture for angular integration in Drosophila. . Nature 546:101–6
    [Google Scholar]
  49. Green J, Maimon G. 2018. Building a heading signal from anatomically defined neuron types in the Drosophila central complex. Curr. Opin. Neurobiol. 52:156–64
    [Google Scholar]
  50. Green J, Vijayan V, Mussells Pires P, Adachi A, Maimon G 2019. A neural heading estimate is compared with an internal goal to guide oriented navigation. Nat. Neurosci. 22:1460–68
    [Google Scholar]
  51. Grieves RM, Jeffery KJ. 2017. The representation of space in the brain. Behav. Process. 135:113–31
    [Google Scholar]
  52. Guo P, Ritzmann RE. 2013. Neural activity in the central complex of the cockroach brain is linked to turning behaviors. J. Exp. Biol. 216:992–1002
    [Google Scholar]
  53. Haberkern H, Basnak MA, Ahanonu B, Schauder D, Cohen JD et al. 2019. Visually guided behavior and optogenetically induced learning in head-fixed flies exploring a virtual landscape. Curr. Biol. 29:1647–59.e8
    [Google Scholar]
  54. Hanesch U, Fischbach KF, Heisenberg M 1989. Neuronal architecture of the central complex in Drosophila melanogaster. . Cell Tissue Res 257:343–66
    [Google Scholar]
  55. Hargreaves EL, Yoganarasimha D, Knierim JJ 2007. Cohesiveness of spatial and directional representations recorded from neural ensembles in the anterior thalamus, parasubiculum, medial entorhinal cortex, and hippocampus. Hippocampus 17:826–41
    [Google Scholar]
  56. Hartmann G, Wehner R. 1995. The ant's path integration system: a neural architecture. Biol. Cybern. 73:483–97
    [Google Scholar]
  57. Hayakawa T, Zyo K. 1989. Retrograde double-labeling study of the marnmillothalamic and the mammillotegmental projections in the rat. J. Comp. Neurol. 284:1–11
    [Google Scholar]
  58. Hayakawa T, Zyo K. 1990. Fine structure of the lateral mammillary projection to the dorsal tegmental nucleus of Gudden in the rat. J. Comp. Neurol. 298:224–36
    [Google Scholar]
  59. Heinze S, Homberg U. 2007. Maplike representation of celestial E-vector orientations in the brain of an insect. Science 315:995–97
    [Google Scholar]
  60. Heinze S, Homberg U. 2008. Neuroarchitecture of the central complex of the desert locust: intrinsic and columnar neurons. J. Comp. Neurol. 511:454–78
    [Google Scholar]
  61. Heinze S, Reppert SM. 2011. Sun compass integration of skylight cues in migratory monarch butterflies. Neuron 69:345–58
    [Google Scholar]
  62. Honkanen A, Adden A, Freitas JD, Heinze S 2019. The insect central complex and the neural basis of navigational strategies. J. Exp. Biol. 222:jeb188854
    [Google Scholar]
  63. Itskov V, Hansel D, Tsodyks M 2011. Short-term facilitation may stabilize parametric working memory trace. Front. Comput. Neurosci. 5:40
    [Google Scholar]
  64. Jacob PY, Casali G, Spieser L, Page H, Overington D, Jeffery K 2017. An independent, landmark-dominated head-direction signal in dysgranular retrosplenial cortex. Nat. Neurosci. 20:173–75
    [Google Scholar]
  65. Jayakumar RP, Madhav MS, Savelli F, Blair HT, Cowan NJ, Knierim JJ 2019. Recalibration of path integration in hippocampal place cells. Nature 566:533–37
    [Google Scholar]
  66. Kennedy JS. 1945. Observations on the mass migration of desert locust hoppers. Ecol. Entomol. 95:247–62
    [Google Scholar]
  67. Kim IS, Dickinson MH. 2017. Idiothetic path integration in the fruit fly Drosophila melanogaster. Curr. Biol 27:2227–38.e3
    [Google Scholar]
  68. Kim SS, Hermundstad AM, Romani S, Abbott LF, Jayaraman V 2019. Generation of stable heading representations in diverse visual scenes. Nature 576:126–31
    [Google Scholar]
  69. Kim SS, Rouault H, Druckmann S, Jayaraman V 2017. Ring attractor dynamics in the Drosophila central brain. Science 356:849–53
    [Google Scholar]
  70. Knierim JJ, Kudrimoti HS, McNaughton BL 1995. Place cells, head direction cells, and the learning of landmark stability. J. Neurosci. 15:1648–59
    [Google Scholar]
  71. Knierim JJ, Kudrimoti HS, McNaughton BL 1998. Interactions between idiothetic cues and external landmarks in the control of place cells and head direction cells. J. Neurophysiol. 80:425–46
    [Google Scholar]
  72. Knierim JJ, Zhang K. 2012. Attractor dynamics of spatially correlated neural activity in the limbic system. Annu. Rev. Neurosci. 35:267–85
    [Google Scholar]
  73. Krogh A. 1929. The progress of physiology. Science 70:200–4
    [Google Scholar]
  74. Kuntz S, Poeck B, Strauss R 2017. Visual working memory requires permissive and instructive NO/cGMP signaling at presynapses in the Drosophila central brain. Curr. Biol. 27:613–23
    [Google Scholar]
  75. Laurens J, Angelaki DE. 2018. The brain compass: a perspective on how self-motion updates the head direction cell attractor. Neuron 97:275–89
    [Google Scholar]
  76. Laurens J, Kim B, Dickman JD, Angelaki DE 2016. Gravity orientation tuning in macaque anterior thalamus. Nat. Neurosci. 19:1566–68
    [Google Scholar]
  77. Lin CY, Chuang CC, Hua TE, Chen CC, Dickson BJ et al. 2013. A comprehensive wiring diagram of the protocerebral bridge for visual information processing in the Drosophila brain. Cell Rep 3:1739–53
    [Google Scholar]
  78. Liu S, Liu QL, Tabuchi M, Wu MN 2016. Sleep drive is encoded by neural plastic changes in a dedicated circuit. Cell 165:1347–60
    [Google Scholar]
  79. Martin JP, Guo P, Mu L, Harley CM, Ritzmann RE 2015. Central-complex control of movement in the freely walking cockroach. Curr. Biol. 25:2795–803
    [Google Scholar]
  80. McNaughton BL, Chen LL, Markus EJ 1991. “Dead reckoning,” landmark learning, and the sense of direction: a neurophysiological and computational hypothesis. J. Cogn. Neurosci. 3:190–202
    [Google Scholar]
  81. Mittelstaedt ML, Mittelstaedt H. 1980. Homing by path integration in a mammal. Naturwissenschaften 67:566–67
    [Google Scholar]
  82. Mouritsen H. 2018. Long-distance navigation and magnetoreception in migratory animals. Nature 558:50–59
    [Google Scholar]
  83. Muir GM, Brown JE, Carey JP, Hirvonen TP, Della Santina CC et al. 2009. Disruption of the head direction cell signal after occlusion of the semicircular canals in the freely moving chinchilla. J. Neurosci. 29:14521–33
    [Google Scholar]
  84. Muller M, Wehner R. 1988. Path integration in desert ants. Cataglyphis fortis. PNAS 85:5287–90
    [Google Scholar]
  85. Murata S, Brockmann A, Tanimura T 2017. Pharyngeal stimulation with sugar triggers local searching behavior in Drosophila. J. Exp. Biol 220:3231–37
    [Google Scholar]
  86. Neuser K, Triphan T, Mronz M, Poeck B, Strauss R 2008. Analysis of a spatial orientation memory in Drosophila. . Nature 453:1244–47
    [Google Scholar]
  87. Ocko SA, Hardcastle K, Giocomo LM, Ganguli S 2018. Emergent elasticity in the neural code for space. PNAS 115:E11798–806
    [Google Scholar]
  88. Ofstad TA, Zuker CS, Reiser MB 2011. Visual place learning in Drosophila melanogaster. . Nature 474:204–7
    [Google Scholar]
  89. O'Keefe J, Nadel L. 1978. The Hippocampus as a Cognitive Map New York: Oxford Univ. Press
  90. Omoto JJ, Keles MF, Nguyen BM, Bolanos C, Lovick JK et al. 2017. Visual input to the Drosophila central complex by developmentally and functionally distinct neuronal populations. Curr. Biol. 27:1098–110
    [Google Scholar]
  91. Page HJI, Jeffery KJ. 2018. Landmark-based updating of the head direction system by retrosplenial cortex: a computational model. Front. Cell Neurosci. 12:191
    [Google Scholar]
  92. Page HJI, Walters D, Stringer SM 2018a. A speed-accurate self-sustaining head direction cell path integration model without recurrent excitation. Network 29:37–69
    [Google Scholar]
  93. Page HJI, Wilson JJ, Jeffery KJ 2018b. A dual-axis rotation rule for updating the head direction cell reference frame during movement in three dimensions. J. Neurophysiol. 119:192–208
    [Google Scholar]
  94. Peyrache A, Lacroix MM, Petersen PC, Buzsaki G 2015. Internally organized mechanisms of the head direction sense. Nat. Neurosci. 18:569–75
    [Google Scholar]
  95. Pfeiffer K, Homberg U. 2014. Organization and functional roles of the central complex in the insect brain. Annu. Rev. Entomol. 59:165–84
    [Google Scholar]
  96. Power ME. 1943. The brain of Drosophila melanogaster. J. Morphol 72:517–59
    [Google Scholar]
  97. Ranck JB Jr 1984. Head-direction cells in the deep cell layers of dorsal presubiculum in freely moving rats. Soc. Neurosci. Abstr. 10:599
    [Google Scholar]
  98. Raudies F, Brandon MP, Chapman GW, Hasselmo ME 2015. Head direction is coded more strongly than movement direction in a population of entorhinal neurons. Brain Res 1621:355–67
    [Google Scholar]
  99. Redish AD, Elga AN, Touretzky DS 1996. A coupled attractor model of the rodent head direction system. Net. Comput. Neural Syst. 7:671–85
    [Google Scholar]
  100. Renart A, Song PC, Wang XJ 2003. Robust spatial working memory through homeostatic synaptic scaling in heterogeneous cortical networks. Neuron 38:473–85
    [Google Scholar]
  101. Reppert SM, Gegear RJ, Merlin C 2010. Navigational mechanisms of migrating monarch butterflies. Trends Neurosci 33:399–406
    [Google Scholar]
  102. Reppert SM, Zhu HS, White RH 2004. Polarized light helps monarch butterflies navigate. Curr. Biol. 14:155–58
    [Google Scholar]
  103. Ritzmann RE, Ridgel AL, Pollack AJ 2008. Multi-unit recording of antennal mechano-sensitive units in the central complex of the cockroach. Blaberus discoidalis. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 194:341–60
    [Google Scholar]
  104. Rubin J, Terman D, Chow C 2001. Localized bumps of activity sustained by inhibition in a two-layer thalamic network. J. Comput. Neurosci. 10:313–31
    [Google Scholar]
  105. Savelli F, Knierim JJ. 2019. Origin and role of path integration in the cognitive representations of the hippocampus: computational insights into open questions. J. Exp. Biol. 222:jeb188912
    [Google Scholar]
  106. Seelig JD, Jayaraman V. 2013. Feature detection and orientation tuning in the Drosophila central complex. Nature 503:262–66
    [Google Scholar]
  107. Seelig JD, Jayaraman V. 2015. Neural dynamics for landmark orientation and angular path integration. Nature 521:186–91
    [Google Scholar]
  108. Sharp PE, Blair HT, Cho J 2001a. The anatomical and computational basis of the rat head-direction cell signal. Trends Neurosci 24:289–94
    [Google Scholar]
  109. Sharp PE, Tinkelman A, Cho J 2001b. Angular velocity and head direction signals recorded from the dorsal tegmental nucleus of Gudden in the rat: implications for path integration in the head direction cell circuit. Behav. Neurosci. 115:571–88
    [Google Scholar]
  110. Shinder ME, Taube JS. 2014. Resolving the active versus passive conundrum for head direction cells. Neuroscience 270:123–38
    [Google Scholar]
  111. Shinder ME, Taube JS. 2019. Three-dimensional tuning of head direction cells in rats. J. Neurophysiol. 121:4–37
    [Google Scholar]
  112. Shiozaki HM, Kazama H. 2017. Parallel encoding of recent visual experience and self-motion during navigation in Drosophila. Nat. Neurosci 20:1395–403
    [Google Scholar]
  113. Skaggs WE, Knierim JJ, Kudrimoti HS, McNaughton BL 1995. A model of the neural basis of the rat's sense of direction. Adv. Neural. Inf. Process. Syst. 7:173–80
    [Google Scholar]
  114. Song P, Wang XJ. 2005. Angular path integration by moving “hill of activity”: a spiking neuron model without recurrent excitation of the head-direction system. J. Neurosci. 25:1002–14
    [Google Scholar]
  115. Stackman RW, Clark AS, Taube JS 2002. Hippocampal spatial representations require vestibular input. Hippocampus 12:291–303
    [Google Scholar]
  116. Stackman RW, Taube JS. 1997. Firing properties of head direction cells in the rat anterior thalamic nucleus: dependence on vestibular input. J. Neurosci. 17:4349–58
    [Google Scholar]
  117. Stackman RW, Taube JS. 1998. Firing properties of rat lateral mammillary single units: head direction, head pitch, and angular head velocity. J. Neurosci. 18:9020–37
    [Google Scholar]
  118. Stone T, Webb B, Adden A, Weddig NB, Honkanen A et al. 2017. An anatomically constrained model for path integration in the bee brain. Curr. Biol. 27:3069–85.e11
    [Google Scholar]
  119. Strausfeld NJ. 1976. Atlas of an Insect Brain Berlin: Springer-Verlag
  120. Strauss R. 2002. The central complex and the genetic dissection of locomotor behaviour. Curr. Opin. Neurobiol. 12:633–38
    [Google Scholar]
  121. Stringer SM, Rolls ET. 2006. Self-organizing path integration using a linked continuous attractor and competitive network: path integration of head direction. Network 17:419–45
    [Google Scholar]
  122. Stringer SM, Trappenberg TP, Rolls ET, de Araujo IE 2002. Self-organizing continuous attractor networks and path integration: one-dimensional models of head direction cells. Network 13:217–42
    [Google Scholar]
  123. Sturzl W, Zeil J, Boeddeker N, Hemmi JM 2016. How wasps acquire and use views for homing. Curr. Biol. 26:470–82
    [Google Scholar]
  124. Sullivan LF, Warren TL, Doe CQ 2019. Temporal identity establishes columnar neuron morphology, connectivity, and function in a Drosophila navigation circuit. eLife 8:e43482
    [Google Scholar]
  125. Sun Y, Nern A, Franconville R, Dana H, Schreiter ER et al. 2017. Neural signatures of dynamic stimulus selection in Drosophila. Nat. Neurosci 20:1104–13
    [Google Scholar]
  126. Takeuchi Y, Allen GV, Hopkins DA 1985. Transnuclear transport and axon collateral projections of the mamillary nuclei in the rat. Brain Res. Bull. 14:453–68
    [Google Scholar]
  127. Tan HM, Bassett JP, O'Keefe J, Cacucci F, Wills TJ 2015. The development of the head direction system before eye opening in the rat. Curr. Biol. 25:479–83
    [Google Scholar]
  128. Taube JS. 1995. Head direction cells recorded in the anterior thalamic nuclei of freely moving rats. J. Neurosci. 15:70–86
    [Google Scholar]
  129. Taube JS. 2007. The head direction signal: origins and sensory-motor integration. Annu. Rev. Neurosci. 30:181–207
    [Google Scholar]
  130. Taube JS. 2011. Head direction cell firing properties and behavioural performance in 3-D space. J. Physiol. 589:835–41
    [Google Scholar]
  131. Taube JS, Bassett JP. 2003. Persistent neural activity in head direction cells. Cereb. Cortex 13:1162–72
    [Google Scholar]
  132. Taube JS, Burton HL. 1995. Head direction cell activity monitored in a novel environment and during a cue conflict situation. J. Neurophysiol. 74:1953–71
    [Google Scholar]
  133. Taube JS, Goodridge JP, Golob EJ, Dudchenko PA, Stackman RW 1996. Processing the head direction cell signal: a review and commentary. Brain Res. Bull. 40:477–84
    [Google Scholar]
  134. Taube JS, Muller RU, Ranck JB Jr 1990a. Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis. J. Neurosci. 10:420–35
    [Google Scholar]
  135. Taube JS, Muller RU, Ranck JB Jr 1990b. Head-direction cells recorded from the postsubiculum in freely moving rats. II. Effects of environmental manipulations. J. Neurosci. 10:436–47
    [Google Scholar]
  136. Tinbergen N, Kruyt W. 1938. Über die Orientierung des Bienenwolfes (Philanthus triangulum Fabr.). Z. Vgl. Physiol. 25:292–334
    [Google Scholar]
  137. Tolman EC. 1948. Cognitive maps in rats and men. Psychol. Rev. 55:189–208
    [Google Scholar]
  138. Touretzky DS, Redish AD, Wan HS 1993. Neural representation of space using sinusoidal arrays. Neural Comput 5:869–84
    [Google Scholar]
  139. Tsoar A, Nathan R, Bartan Y, Vyssotski A, Dell'Omo G, Ulanovsky N 2011. Large-scale navigational map in a mammal. PNAS 108:E718–24
    [Google Scholar]
  140. Tsodyks M, Sejnowski T. 1995. Associative memory and hippocampal place cells. Int. J. Neural Syst. 6:Suppl. 199581–86
    [Google Scholar]
  141. Turner-Evans D, Wegener S, Rouault H, Franconville R, Wolff T et al. 2017. Angular velocity integration in a fly heading circuit. eLife 6:e23496
    [Google Scholar]
  142. Turner-Evans DB, Jayaraman V. 2016. The insect central complex. Curr. Biol. 26:R453–57
    [Google Scholar]
  143. Turner-Evans DB, Jensen K, Ali S, Paterson T, Sheridan A et al. 2019. The neuroanatomical ultrastructure and function of a biological ring attractor. bioRxiv 847152 https://doi.org/10.1101/847152
    [Crossref]
  144. Valerio S, Taube JS. 2012. Path integration: how the head direction signal maintains and corrects spatial orientation. Nat. Neurosci. 15:1445–53
    [Google Scholar]
  145. Valerio S, Taube JS. 2016. Head direction cell activity is absent in mice without the horizontal semicircular canals. J. Neurosci. 36:741–54
    [Google Scholar]
  146. Varga AG, Ritzmann RE. 2016. Cellular basis of head direction and contextual cues in the insect brain. Curr. Biol. 26:1816–28
    [Google Scholar]
  147. von Frisch K. 1967. The Dance Language and Orientation of Bees Cambridge, MA: Belknap Press
  148. Warrant E, Dacke M. 2016. Visual navigation in nocturnal insects. Physiology 31:182–92
    [Google Scholar]
  149. Warren TL, Giraldo YM, Dickinson MH 2019. Celestial navigation in Drosophila. . J. Exp. Biol 222:jeb186148
    [Google Scholar]
  150. Warren TL, Weir PT, Dickinson MH 2018. Flying Drosophila melanogaster maintain arbitrary but stable headings relative to the angle of polarized light. J. Exp. Biol. 221:jeb177550
    [Google Scholar]
  151. Webb B. 2019. The internal maps of insects. J. Exp. Biol. 222:jeb188094
    [Google Scholar]
  152. Wehner R, Srinivasan MV. 1981. Searching behavior of desert ants, genus Cataglyphis (Formicidae, Hymenoptera). J. Comp. Physiol. 142:315–38
    [Google Scholar]
  153. Weir PT, Dickinson MH. 2012. Flying Drosophila orient to sky polarization. Curr. Biol. 22:21–27
    [Google Scholar]
  154. Weir PT, Schnell B, Dickinson MH 2014. Central complex neurons exhibit behaviorally gated responses to visual motion in Drosophila. J. Neurophysiol 111:62–71
    [Google Scholar]
  155. Wiener SI, Taube JS. 2005. Head Direction Cells and the Neural Mechanisms of Spatial Orientation Cambridge, MA: MIT Press
  156. Wirtshafter D, Stratford TR. 1993. Evidence for GABAergic projections from the tegmental nuclei of Gudden to the mammillary body in the rat. Brain Res 630:188–94
    [Google Scholar]
  157. Wolff T, Iyer NA, Rubin GM 2015. Neuroarchitecture and neuroanatomy of the Drosophila central complex: a GAL4-based dissection of protocerebral bridge neurons and circuits. J. Comp. Neurol. 523:997–1037
    [Google Scholar]
  158. Wolff T, Rubin GM. 2018. Neuroarchitecture of the Drosophila central complex: a catalog of nodulus and asymmetrical body neurons and a revision of the protocerebral bridge catalog. J. Comp. Neurol. 526:2585–611
    [Google Scholar]
  159. Xie X, Hahnloser RH, Seung HS 2002. Double-ring network model of the head-direction system. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 66:041902
    [Google Scholar]
  160. Yoder RM, Clark BJ, Brown JE, Lamia MV, Valerio S et al. 2011. Both visual and idiothetic cues contribute to head direction cell stability during navigation along complex routes. J. Neurophysiol. 105:2989–3001
    [Google Scholar]
  161. Yoder RM, Peck JR, Taube JS 2015. Visual landmark information gains control of the head direction signal at the lateral mammillary nuclei. J. Neurosci. 35:1354–67
    [Google Scholar]
  162. Yoder RM, Taube JS. 2014. The vestibular contribution to the head direction signal and navigation. Front. Integr. Neurosci. 8:32
    [Google Scholar]
  163. Yoganarasimha D, Yu X, Knierim JJ 2006. Head direction cell representations maintain internal coherence during conflicting proximal and distal cue rotations: comparison with hippocampal place cells. J. Neurosci. 26:622–31
    [Google Scholar]
  164. Young JM, Armstrong JD. 2010a. Building the central complex in Drosophila: the generation and development of distinct neural subsets. J. Comp. Neurol. 518:1525–41
    [Google Scholar]
  165. Young JM, Armstrong JD. 2010b. Structure of the adult central complex in Drosophila: organization of distinct neuronal subsets. J. Comp. Neurol. 518:1500–24
    [Google Scholar]
  166. Zeil J. 2012. Visual homing: an insect perspective. Curr. Opin. Neurobiol. 22:285–93
    [Google Scholar]
  167. Zhang K. 1996. Representation of spatial orientation by the intrinsic dynamics of the head-direction cell ensemble: a theory. J. Neurosci. 16:2112–26
    [Google Scholar]
  168. Zugaro MB, Berthoz A, Wiener SI 2001. Background, but not foreground, spatial cues are taken as references for head direction responses by rat anterodorsal thalamus neurons. J. Neurosci. 21:RC154
    [Google Scholar]
  169. Zugaro MB, Tabuchi E, Wiener SI 2000. Influence of conflicting visual, inertial and substratal cues on head direction cell activity. Exp. Brain Res. 133:198–208
    [Google Scholar]
/content/journals/10.1146/annurev-neuro-072116-031516
Loading
/content/journals/10.1146/annurev-neuro-072116-031516
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error