1932

Abstract

Many animals can navigate toward a goal they cannot see based on an internal representation of that goal in the brain's spatial maps. These maps are organized around networks with stable fixed-point dynamics (attractors), anchored to landmarks, and reciprocally connected to motor control. This review summarizes recent progress in understanding these networks, focusing on studies in arthropods. One factor driving recent progress is the availability of the connectome; however, it is increasingly clear that navigation depends on ongoing synaptic plasticity in these networks. Functional synapses appear to be continually reselected from the set of anatomical potential synapses based on the interaction of Hebbian learning rules, sensory feedback, attractor dynamics, and neuromodulation. This can explain how the brain's maps of space are rapidly updated; it may also explain how the brain can initialize goals as stable fixed points for navigation.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-neuro-110920-032645
2023-07-10
2024-04-21
Loading full text...

Full text loading...

/deliver/fulltext/neuro/46/1/annurev-neuro-110920-032645.html?itemId=/content/journals/10.1146/annurev-neuro-110920-032645&mimeType=html&fmt=ahah

Literature Cited

  1. Ajabi Z, Keinath AT, Wei X-X, Brandon MP. 2021. Population dynamics of the thalamic head direction system during drift and reorientation. bioRxiv 2021.08.30.458266. https://doi.org/10.1101/2021.08.30.458266
    [Crossref]
  2. Arendse MC, Kruyswijk CJ. 1981. Orientation of Talitrus saltator to magnetic fields. Neth. J. Sea Res. 15:23–32
    [Google Scholar]
  3. Barter JW, Li S, Lu D, Bartholomew RA, Rossi MA et al. 2015. Beyond reward prediction errors: the role of dopamine in movement kinematics. Front. Integr. Neurosci. 9:39
    [Google Scholar]
  4. Barth FG, Seyfarth E-A. 1971. Slit sense organs and kinesthetic orientation. Z. Vergl. Physiol. 74:326–28
    [Google Scholar]
  5. Bates AS, Janssens J, Jefferis GS, Aerts S. 2019. Neuronal cell types in the fly: single-cell anatomy meets single-cell genomics. Curr. Opin. Neurobiol. 56:125–34
    [Google Scholar]
  6. Beetz MJ, Kraus C, Franzke M, Dreyer D, Strube-Bloss MF et al. 2021. Flight-induced compass representation in the monarch butterfly heading network. Curr. Biol. 32:338–49.e5
    [Google Scholar]
  7. Behbahani AH, Palmer EH, Corfas RA, Dickinson MH. 2021. Drosophila re-zero their path integrator at the center of a fictive food patch. Curr. Biol. 31:4534–46.e5
    [Google Scholar]
  8. Bell WJ, Kramer E. 1979. Search and anemotactic orientation of cockroaches. J. Insect Physiol. 25:631–40
    [Google Scholar]
  9. Bicanski A, Burgess N. 2020. Neuronal vector coding in spatial cognition. Nat. Rev. Neurosci. 21:453–70
    [Google Scholar]
  10. Böhm H. 1995. Dynamic properties of orientation to turbulent air current by walking carrion beetles. J. Exp. Biol. 198:1995–2005
    [Google Scholar]
  11. Böhm H, Heinzel H-G, Scharstein H, Wendler G. 1991. The course control system of beetles walking in an air-current field. J. Comp. Physiol. A 169:671–83
    [Google Scholar]
  12. Boles LC, Lohmann KJ. 2003. True navigation and magnetic maps in spiny lobsters. Nature 421:60–63
    [Google Scholar]
  13. 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]
  14. Buehlmann C, Wozniak B, Goulard R, Webb B, Graham P, Niven JE 2020. Mushroom bodies are required for learned visual navigation, but not for innate visual behavior, in ants. Curr. Biol. 30:3438–43.e2
    [Google Scholar]
  15. Burak Y, Fiete IR. 2009. Accurate path integration in continuous attractor network models of grid cells. PLOS Comput. Biol. 5:e1000291
    [Google Scholar]
  16. Cheng K, Narendra A, Wehner R. 2005. Behavioral ecology of odometric memories in desert ants: acquisition, retention, and integration. Behav. Ecol. 17:227–35
    [Google Scholar]
  17. Cheng K, Shettleworth SJ, Huttenlocher J, Rieser JJ. 2007. Bayesian integration of spatial information. Psychol. Bull. 133:625–37
    [Google Scholar]
  18. Cohn R, Morantte I, Ruta V. 2015. Coordinated and compartmentalized neuromodulation shapes sensory processing in Drosophila. Cell 163:1742–55
    [Google Scholar]
  19. Collett M, Collett TS. 2018. How does the insect central complex use mushroom body output for steering?. Curr. Biol. 28:R733–34
    [Google Scholar]
  20. 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]
  21. Collett TS, Zeil J. 2018. Insect learning flights and walks. Curr. Biol. 28:R984–88
    [Google Scholar]
  22. 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]
  23. 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]
  24. Currier TA, Matheson AM, Nagel KI. 2020. Encoding and control of orientation to airflow by a set of Drosophila fan-shaped body neurons. eLife 9:e61510
    [Google Scholar]
  25. Dacke M, Baird E, Byrne M, Scholtz CH, Warrant EJ. 2013. Dung beetles use the Milky Way for orientation. Curr. Biol. 23:298–300
    [Google Scholar]
  26. Dacke M, Baird E, el Jundi B, Warrant EJ, Byrne M. 2021. How dung beetles steer straight. Annu. Rev. Entomol. 66:243–56
    [Google Scholar]
  27. Dacke M, Bell ATA, Foster JJ, Baird EJ, Strube-Bloss MF et al. 2019. Multimodal cue integration in the dung beetle compass. PNAS 116:14248–53
    [Google Scholar]
  28. Dacke M, Byrne MJ, Scholtz CH, Warrant EJ. 2004. Lunar orientation in a beetle. Proc. Biol. Sci. 271:361–65
    [Google Scholar]
  29. Dacke M, Srinivasan MV. 2008. Two odometers in honeybees?. J. Exp. Biol. 211:3281–86
    [Google Scholar]
  30. Dan C, Kappagantula R, Hulse BK, Jayaraman V, Hermundstad AM. 2022. Flexible control of behavioral variability mediated by an internal representation of head direction. bioRxiv 2021.08.18.456004. https://doi.org/10.1101/2021.08.18.456004
    [Crossref]
  31. de Croon GCHE, Dupeyroux JJG, Fuller SB, Marshall JAR. 2022. Insect-inspired AI for autonomous robots. Sci. Robot. 7:eab16334
    [Google Scholar]
  32. Dickinson MH. 2014. Death Valley, Drosophila, and the Devonian toolkit. Annu. Rev. Entomol. 59:51–72
    [Google Scholar]
  33. Dubowy C, Sehgal A. 2017. Circadian rhythms and sleep in Drosophila melanogaster. Genetics 205:1373–97
    [Google Scholar]
  34. el Jundi B, Foster JJ, Byrne MJ, Baird E, Dacke M. 2015a. Spectral information as an orientation cue in dung beetles. Biol. Lett. 11:20150656
    [Google Scholar]
  35. el Jundi B, Foster JJ, Khaldy L, Byrne MJ, Dacke M, Baird E 2016. A snapshot-based mechanism for celestial orientation. Curr. Biol. 26:1456–62
    [Google Scholar]
  36. el Jundi B, Warrant EJ, Byrne MJ, Khaldy L, Baird E et al. 2015b. Neural coding underlying the cue preference for celestial orientation. PNAS 112:11395–400
    [Google Scholar]
  37. Engelhard B, Finkelstein J, Cox J, Fleming W, Jang HJ et al. 2019. Specialized coding of sensory, motor and cognitive variables in VTA dopamine neurons. Nature 570:509–13
    [Google Scholar]
  38. 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]
  39. Fisher YE, Marquis M, D'Alessandro I, Wilson RI 2022. Dopamine promotes head direction plasticity during orienting movements. Nature 612:316–22
    [Google Scholar]
  40. Fleischmann PN, Grob R, Müller VL, Wehner R, Rössler W. 2018. The geomagnetic field is a compass cue in Cataglyphis ant navigation. Curr. Biol. 28:1440–44.e2
    [Google Scholar]
  41. Franconville R, Beron C, Jayaraman V. 2018. Building a functional connectome of the Drosophila central complex. eLife 7:e37017
    [Google Scholar]
  42. Frémaux N, Gerstner W. 2015. Neuromodulated spike-timing-dependent plasticity, and theory of three-factor learning rules. Front. Neural Circuits 9:85
    [Google Scholar]
  43. Geurten BRH, Jähde P, Corthals K, Göpfert MC. 2014. Saccadic body turns in walking Drosophila. Front. Behav. Neurosci. 8:365
    [Google Scholar]
  44. Giraldo YM, Leitch KJ, Ros IG, Warren TL, Weir PT, Dickinson MH 2018. Sun navigation requires compass neurons in Drosophila. Curr. Biol. 28:2845–52.e4
    [Google Scholar]
  45. Goulard R, Buehlmann C, Niven JE, Graham P, Webb B 2021. A unified mechanism for innate and learned visual landmark guidance in the insect central complex. PLOS Comput. Biol. 17:e1009383
    [Google Scholar]
  46. 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]
  47. 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]
  48. Grover D, Chen J-Y, Xie J, Li J, Changeux J-P, Greenspan RJ. 2022. Differential mechanisms underlie trace and delay conditioning in Drosophila. Nature 603:302–8
    [Google Scholar]
  49. Haberkern H, Chitnis SS, Hubbard PM, Goulet T, Hermundstad AM, Jayaraman V. 2022. Maintaining a stable head direction representation in naturalistic visual environments. bioRxiv 2022.05.17.492284. https://doi.org/10.1101/2022.05.17.492284
    [Crossref]
  50. Handler A, Graham TGW, Cohn R, Morantte I, Siliciano AF et al. 2019. Distinct dopamine receptor pathways underlie the temporal sensitivity of associative learning. Cell 178:60–75.e19
    [Google Scholar]
  51. Hardcastle BJ, Omoto JJ, Kandimalla P, Nguyen B-CM, Keleş MF et al. 2021. A visual pathway for skylight polarization processing in Drosophila. eLife 10:e63225
    [Google Scholar]
  52. Heinze S, Homberg U. 2007. Maplike representation of celestial E-vector orientations in the brain of an insect. Science 315:995–97
    [Google Scholar]
  53. Heinze S, Homberg U. 2009. Linking the input to the output: new sets of neurons complement the polarization vision network in the locust central complex. J. Neurosci. 29:4911–21
    [Google Scholar]
  54. Heinze S, Narendra A, Cheung A. 2018. Principles of insect path integration. Curr. Biol. 28:R1043–58
    [Google Scholar]
  55. Heinze S, Reppert SM. 2011. Sun compass integration of skylight cues in migratory monarch butterflies. Neuron 69:345–58
    [Google Scholar]
  56. Heinzel H-G, Böhm H. 1989. The wind-orientation of walking carrion beetles. J. Comp. Physiol. A 164:775–86
    [Google Scholar]
  57. Hige T, Aso Y, Rubin GM, Turner GC. 2015. Plasticity-driven individualization of olfactory coding in mushroom body output neurons. Nature 526:258–62
    [Google Scholar]
  58. Homberg U. 2004. In search of the sky compass in the insect brain. Naturwissenschaften 91:199–208
    [Google Scholar]
  59. Homberg U. 2015. Sky compass orientation in desert locusts—evidence from field and laboratory studies. Front. Behav. Neurosci. 9:346
    [Google Scholar]
  60. Honkanen A, Adden A, da Silva Freitas J, Heinze S. 2019. The insect central complex and the neural basis of navigational strategies. J. Exp. Biol. 222:Suppl. 1jeb188854
    [Google Scholar]
  61. Hughes GM, Wiersma CAG. 1960. The co-ordination of swimmeret movements in the crayfish, Procambarus clarkii (Girard). J. Exp. Biol. 37:657–70
    [Google Scholar]
  62. Hughes RN, Bakhurin KI, Petter EA, Watson GDR, Kim N et al. 2020. Ventral tegmental dopamine neurons control the impulse vector during motivated behavior. Curr. Biol. 30:2681–94.e5
    [Google Scholar]
  63. Hulse BK, Haberkern H, Franconville R, Turner-Evans DB, Takemura S-Y et al. 2021. A connectome of the Drosophila central complex reveals network motifs suitable for flexible navigation and context-dependent action selection. eLife 10:e66039
    [Google Scholar]
  64. Hulse BK, Jayaraman V. 2020. Mechanisms underlying the neural computation of head direction. Annu. Rev. Neurosci. 43:31–54
    [Google Scholar]
  65. Kamhi JF, Barron AB, Narendra A. 2020. Vertical lobes of the mushroom bodies are essential for view-based navigation in Australian Myrmecia ants. Curr. Biol. 30:3432–37.e3
    [Google Scholar]
  66. Khaldy L, Peleg O, Tocco C, Mahadevan L, Byrne M, Dacke M. 2019. The effect of step size on straight-line orientation. J. R. Soc. Interface 16:20190181
    [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, Zhang K. 2012. Attractor dynamics of spatially correlated neural activity in the limbic system. Annu. Rev. Neurosci. 35:267–85
    [Google Scholar]
  71. Krause T, Spindler L, Poeck B, Strauss R. 2019. Drosophila acquires a long-lasting body-size memory from visual feedback. Curr. Biol. 29:1833–41.e3
    [Google Scholar]
  72. Kutschireiter A, Basnak MA, Drugowitsch J. 2022. Bayesian inference in ring attractor networks. bioRxiv 2021.12.17.473253. https://doi.org/10.1101/2021.12.17.473253
    [Crossref]
  73. Labhart T, Meyer EP. 2002. Neural mechanisms in insect navigation: polarization compass and odometer. Curr. Opin. Neurobiol. 12:707–14
    [Google Scholar]
  74. Laughlin SB. 1981. A simple coding procedure enhances a neuron's information capacity. Z. Naturforsch. C 36:910–12
    [Google Scholar]
  75. Laurent G. 2002. Olfactory network dynamics and the coding of multidimensional signals. Nat. Rev. Neurosci. 3:884–95
    [Google Scholar]
  76. Li F, Lindsey JW, Marin EC, Otto N, Dreher M et al. 2020. The connectome of the adult Drosophila mushroom body provides insights into function. eLife 9:e62576
    [Google Scholar]
  77. Liang X, Ho MCW, Zhang Y, Li Y, Wu MN et al. 2019. Morning and evening circadian pacemakers independently drive premotor centers via a specific dopamine relay. Neuron 102:843–57.e4
    [Google Scholar]
  78. Litwin-Kumar A, Harris KD, Axel R, Sompolinsky H, Abbott LF 2017. Optimal degrees of synaptic connectivity. Neuron 93:1153–64.e7
    [Google Scholar]
  79. Litwin-Kumar A, Turaga SC. 2019. Constraining computational models using electron microscopy wiring diagrams. Curr. Opin. Neurobiol. 58:94–100
    [Google Scholar]
  80. Lu J, Behbehani A, Hamburg L, Westeinde EA, Dawson PM et al. 2021. Transforming representations of movement from body- to world-centric space. Nature 601:98–104
    [Google Scholar]
  81. Luo SX, Axel R, Abbott LF 2010. Generating sparse and selective third-order responses in the olfactory system of the fly. PNAS 107:10713–18
    [Google Scholar]
  82. Lyu C, Abbott LF, Maimon G. 2021. Building an allocentric travelling direction signal via vector computation. Nature 601:92–97
    [Google Scholar]
  83. 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]
  84. Matheson AMM, Lanz AJ, Medina AM, Licata AM, Currier TA et al. 2022. A neural circuit for wind-guided olfactory navigation. Nat. Commun. 13:4613
    [Google Scholar]
  85. Melnattur K, Kirszenblat L, Morgan E, Militchin V, Sakran B et al. 2021. A conserved role for sleep in supporting spatial learning in Drosophila. Sleep 44:zsaa197
    [Google Scholar]
  86. Mizumori SJ, Williams JD. 1993. Directionally selective mnemonic properties of neurons in the lateral dorsal nucleus of the thalamus of rats. J. Neurosci. 13:4015–28
    [Google Scholar]
  87. Müller M, Wehner R. 2007. Wind and sky as compass cues in desert ant navigation. Naturwissenschaften 94:589–94
    [Google Scholar]
  88. Müller M, Wehner R. 2010. Path integration provides a scaffold for landmark learning in desert ants. Curr. Biol. 20:1368–71
    [Google Scholar]
  89. Mussells Pires P, Abbott LF, Maimon G 2022. Converting an allocentric goal into an egocentric steering signal. bioRxiv 2022.11.10.516026. https://doi.org/10.1101/2022.11.10.516026
    [Crossref]
  90. Narendra A. 2007. Homing strategies of the Australian desert ant Melophorus bagoti. II. Interaction of the path integrator with visual cue information. J. Exp. Biol. 210:1804–12
    [Google Scholar]
  91. Ofstad TA, Zuker CS, Reiser MB. 2011. Visual place learning in Drosophila melanogaster. Nature 474:204–7
    [Google Scholar]
  92. Okubo TS, Patella P, D'Alessandro I, Wilson RI 2020. A neural network for wind-guided compass navigation. Neuron 107:924–40.e18
    [Google Scholar]
  93. Olsen SR, Bhandawat V, Wilson RI. 2010. Divisive normalization in olfactory population codes. Neuron 66:287–99
    [Google Scholar]
  94. 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]
  95. Page HJI, Walters DM, Knight R, Piette CE, Jeffery KJ, Stringer SM. 2014. A theoretical account of cue averaging in the rodent head direction system. Philos. Trans. R. Soc. B 369:20130283
    [Google Scholar]
  96. Pegel U, Pfeiffer K, Homberg U. 2018. Integration of celestial compass cues in the central complex of the locust brain. J. Exp. Biol. 221:jeb171207
    [Google Scholar]
  97. Pfeffer SE, Wittlinger M. 2016. How to find home backwards? Navigation during rearward homing of Cataglyphis fortis desert ants. J. Exp. Biol. 219:2119–26
    [Google Scholar]
  98. Pfeiffer K, Homberg U. 2007. Coding of azimuthal directions via time-compensated combination of celestial compass cues. Curr. Biol. 17:960–65
    [Google Scholar]
  99. Pfeiffer K, Kinoshita M, Homberg U. 2005. Polarization-sensitive and light-sensitive neurons in two parallel pathways passing through the anterior optic tubercle in the locust brain. J. Neurophysiol. 94:3903–15
    [Google Scholar]
  100. Rayshubskiy A, Holtz SL, D'Alessandro I, Li AA, Vanderbeck QX et al. 2020. Neural circuit mechanisms for steering control in walking Drosophila. bioRxiv 2020.04.04.024703. https://doi.org/10.1101/2020.04.04.024703
    [Crossref]
  101. Reichardt W. 1961. Autocorrelation, a principle for evaluation of sensory information by the central nervous system. Sensory Communication WA Rosenblith 303–17. Cambridge, MA: MIT Press
    [Google Scholar]
  102. Riley JR, Reynolds DR, Smith AD, Edwards AS, Osborne JL et al. 1999. Compensation for wind drift by bumble-bees. Nature 400:126
    [Google Scholar]
  103. Ronacher BD, Wehner R. 1995. Desert ants Cataglyphis fortis use self-induced optic flow to measure distance travelled. J. Comp. Physiol. A 177:21–27
    [Google Scholar]
  104. Rumelhart DE, Hinton GE, Williams RJ. 1986. Learning representations by back-propagating errors. Nature 323:533–36
    [Google Scholar]
  105. Sakura M, Lambrinos D, Labhart T. 2008. Polarized skylight navigation in insects: model and electrophysiology of E-vector coding by neurons in the central complex. J. Neurophysiol. 99:667–82
    [Google Scholar]
  106. Samsonovich A, McNaughton BL. 1997. Path integration and cognitive mapping in a continuous attractor neural network model. J. Neurosci. 17:5900–20
    [Google Scholar]
  107. Sayre ME, Templin R, Chavez J, Kempenaers J, Heinze S. 2021. A projectome of the bumblebee central complex. eLife 10:e68911
    [Google Scholar]
  108. Schlegel P, Bates AS, Stürner T, Jagannathan SR, Drummond N et al. 2021. Information flow, cell types and stereotypy in a full olfactory connectome. eLife 10:e66018
    [Google Scholar]
  109. Schnell B, Weir PT, Roth E, Fairhall AL, Dickinson MH. 2014. Cellular mechanisms for integral feedback in visually guided behavior. PNAS 111:5700–5
    [Google Scholar]
  110. Schöne H. 1996. Optokinetic speed control and estimation of travel distance in walking honeybees. J. Comp. Physiol. A 179:587–92
    [Google Scholar]
  111. Schöne H. 2014. Spatial Orientation: The Spatial Control of Behavior in Animals and Man Princeton, NJ: Princeton Univ. Press
  112. Seelig JD, Jayaraman V. 2013. Feature detection and orientation tuning in the Drosophila central complex. Nature 503:262–66
    [Google Scholar]
  113. Seelig JD, Jayaraman V. 2015. Neural dynamics for landmark orientation and angular path integration. Nature 521:186–91
    [Google Scholar]
  114. Shiozaki HM, Ohta K, Kazama H. 2020. A multi-regional network encoding heading and steering maneuvers in Drosophila. Neuron 106:126–41.e5
    [Google Scholar]
  115. 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]
  116. Souman JL, Frissen I, Sreenivasa MN, Ernst MO. 2009. Walking straight into circles. Curr. Biol. 19:1538–42
    [Google Scholar]
  117. Srinivasan M, Zhang S, Lehrer M, Collett T. 1996. Honeybee navigation en route to the goal: visual flight control and odometry. J. Exp. Biol. 199:237–44
    [Google Scholar]
  118. Srinivasan MV, Laughlin SB, Dubs A. 1982. Predictive coding: a fresh view of inhibition in the retina. Proc. R. Soc. Lond. B Biol. Sci. 216:427–59
    [Google Scholar]
  119. Srinivasan MV, Zhang SW, Berry J, Cheng K, Zhu H. 1999. Honeybee navigation: linear perception of short distances travelled. J. Comp. Physiol. A 185:239–45
    [Google Scholar]
  120. Stevens CF. 2015. What the fly's nose tells the fly's brain. PNAS 112:9460–65
    [Google Scholar]
  121. 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]
  122. Strausfeld NJ. 2012. Arthropod Brains: Evolution, Functional Elegance, and Historical Significance Cambridge, MA: Harvard Univ. Press
  123. 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]
  124. Taube JS. 1995. Head direction cells recorded in the anterior thalamic nuclei of freely moving rats. J. Neurosci. 15:70–86
    [Google Scholar]
  125. 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]
  126. 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]
  127. Thoen HH, Marshall J, Wolff GH, Strausfeld NJ. 2017. Insect-like organization of the stomatopod central complex: functional and phylogenetic implications. Front. Behav. Neurosci. 11:12
    [Google Scholar]
  128. Titova AV, Kau BE, Tibor S, Mach J, Thang Vo-Doan T et al. 2022. Displacement experiments provide evidence for path integration in Drosophila. bioRxiv 2022.07.22.501185. https://doi.org/10.1101/2022.07.22.501185
    [Crossref]
  129. Touretzky DS, Redish AD, Wan HS. 1993. Neural representation of space using sinusoidal arrays. Neural Comput. 5:869–84
    [Google Scholar]
  130. Turner-Evans D, Jensen KT, Ali S, Paterson T, Sheridan A et al. 2020. The neuroanatomical ultrastructure and function of a biological ring attractor. Neuron 108:145–63.e10
    [Google Scholar]
  131. 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]
  132. Ugolini A, Chiussi R. 1996. Astronomical orientation and learning in the earwig Labidura riparia. Behav. Processes 36:151–61
    [Google Scholar]
  133. Vafidis P, Owald D, D'Albis T, Kempter R. 2022. Learning accurate path integration in ring attractor models of the head direction system. eLife 11:e69841
    [Google Scholar]
  134. van Breugel F, Jewell R, Houle J 2022. Active anemosensing hypothesis: how flying insects could estimate ambient wind direction through sensory integration and active movement. J. R. Soc. Interface 19:20220258
    [Google Scholar]
  135. Vickerstaff RJ, Cheung A. 2010. Which coordinate system for modelling path integration?. J. Theor. Biol. 263:242–61
    [Google Scholar]
  136. Vickerstaff RJ, Di Paolo EA. 2005. Evolving neural models of path integration. J. Exp. Biol. 208:3349–66
    [Google Scholar]
  137. Warren TL, Giraldo YM, Dickinson MH. 2019. Celestial navigation in Drosophila. J. Exp. Biol. 222:jeb186148
    [Google Scholar]
  138. Watabe-Uchida M, Eshel N, Uchida N. 2017. Neural circuitry of reward prediction error. Annu. Rev. Neurosci. 40:373–94
    [Google Scholar]
  139. Webb B, Wystrach A. 2016. Neural mechanisms of insect navigation. Curr. Opin. Insect Sci. 15:27–39
    [Google Scholar]
  140. Westeinde EA, Kellogg E, Dawson PM, Lu J, Hamburg L et al. 2022. Transforming a head direction signal into a goal-oriented steering command. bioRxiv 2022.11.10.516039. https://doi.org/10.1101/2022.11.10.516039
    [Crossref]
  141. Wilson DM. 1961. The central nervous control of flight in a locust. J. Exp. Biol. 38:471–90
    [Google Scholar]
  142. Wittlinger M, Wehner R, Wolf H. 2007. The desert ant odometer: a stride integrator that accounts for stride length and walking speed. J. Exp. Biol. 210:198–207
    [Google Scholar]
  143. Wittmann T, Schwegler H. 1995. Path integration—a network model. Biol. Cybern. 73:569–75
    [Google Scholar]
  144. 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]
  145. 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]
  146. 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]
  147. Ziegler PE, Wehner R. 1997. Time-courses of memory decay in vector-based and landmark-based systems of navigation in desert ants, Cataglyphis fortis. J. Comp. Physiol. A 181:13–20
    [Google Scholar]
/content/journals/10.1146/annurev-neuro-110920-032645
Loading
/content/journals/10.1146/annurev-neuro-110920-032645
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