Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Multisensory coding of self-motion and its contribution to navigation

Nature Reviews Neuroscience volume 26, pages 715–732 (2025)Cite this article

Subjects

Abstract

Mobile organisms integrate multimodal self-motion signals — including motor commands, vestibular inputs, optic flow and proprioceptive feedback — to accurately perceive their heading and speed of traversal. These instantaneous cues are processed, via continuous temporal integration and progressive spatial transformations, to facilitate path-integration-based navigation. Recent cutting-edge neurophysiological recordings in animal models have revealed several ubiquitous cross-modal algorithms that contribute to this processing: vestibular–visual convergence to enhance self-motion perception, predictive coding integration to enable optimal dynamic state estimates, landmark-referenced error correction‌ to mitigate path-integration drift and facilitate cognitive spatial map construction, and egocentric-to-allocentric conversion‌ via integration with proprioceptive cues from the eyes, head, body or limbs. Thus, multisensory coding plays an important role in self-motion perception and self-localization during navigational behaviour.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on SpringerLink
  • Instant access to the full article PDF.

USD 39.95

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Self-motion perception contributes to path integration-based navigation.
Fig. 2: Convergence of vestibular and optic flow signals in the primate sensory cortices.
Fig. 3: Spatiotemporal congruency of vestibular and visual self-motion signals in the primate brain.
Fig. 4: Spatial reference transformations of self-motion signals.

Similar content being viewed by others

References

  1. Campbell, M. G. & Giocomo, L. M. Self-motion processing in visual and entorhinal cortices: inputs, integration, and implications for position coding. J. Neurophysiol. 120, 2091–2106 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  2. Mittelstaedt, M. L. & Mittelstaedt, H. Homing by path integration in a mammal. Naturwissenschaften 67, 566–567 (1980).

    Article  Google Scholar 

  3. Senkowski, D. & Engel, A. K. Multi-timescale neural dynamics for multisensory integration. Nat. Rev. Neurosci. 25, 625–642 (2024).

    Article  CAS  PubMed  Google Scholar 

  4. Stein, B. E. M, M. A. Multisensory Integration: The Merging of the Senses (MIT Press, 1993).

  5. Parise, C. V. & Ernst, M. O. Correlation detection as a general mechanism for multisensory integration. Nat. Commun. 7, 11543 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Whittington, J. C. R., McCaffary, D., Bakermans, J. J. W. & Behrens, T. E. J. How to build a cognitive map. Nat. Neurosci. 25, 1257–1272 (2022).

    Article  CAS  PubMed  Google Scholar 

  7. Grabherr, L., Nicoucar, K., Mast, F. W. & Merfeld, D. M. Vestibular thresholds for yaw rotation about an Earth-vertical axis as a function of frequency. Exp. Brain Res. 186, 677–681 (2008).

    Article  PubMed  Google Scholar 

  8. MacNeilage, P. R., Turner, A. H. & Angelaki, D. E. Canal–otolith interactions and detection thresholds of linear and angular components during curved-path self-motion. J. Neurophysiol. 104, 765–773 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  9. Valko, Y., Lewis, R. F., Priesol, A. J. & Merfeld, D. M. Vestibular labyrinth contributions to human whole-body motion discrimination. J. Neurosci. 32, 13537–13542 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Gu, Y., DeAngelis, G. C. & Angelaki, D. E. A functional link between area MSTd and heading perception based on vestibular signals. Nat. Neurosci. 10, 1038–1047 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Liu, S., Dickman, J. D., Newlands, S. D., DeAngelis, G. C. & Angelaki, D. E. Reduced choice-related activity and correlated noise accompany perceptual deficits following unilateral vestibular lesion. Proc. Natl Acad. Sci. USA 110, 17999–18004 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Cullen, K. E. & Taube, J. S. Our sense of direction: progress, controversies and challenges. Nat. Neurosci. 20, 1465–1473 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Liu, S., Gu, Y., DeAngelis, G. C. & Angelaki, D. E. Choice-related activity and correlated noise in subcortical vestibular neurons. Nat. Neurosci. 16, 89–97 (2013).

    Article  PubMed  Google Scholar 

  14. Liu, S., Yakusheva, T., Deangelis, G. C. & Angelaki, D. E. Direction discrimination thresholds of vestibular and cerebellar nuclei neurons. J. Neurosci. 30, 439–448 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  15. Yakusheva, T. A., Blazquez, P. M., Chen, A. & Angelaki, D. E. Spatiotemporal properties of optic flow and vestibular tuning in the cerebellar nodulus and uvula. J. Neurosci. 33, 15145–151603 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Chen, A., DeAngelis, G. C. & Angelaki, D. E. Macaque parieto-insular vestibular cortex: responses to self-motion and optic flow. J. Neurosci. 30, 3022–3042 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Chen, A., Zeng, F., DeAngelis, G. C. & Angelaki, D. E. Dynamics of heading and choice-related signals in the parieto-insular vestibular cortex of macaque monkeys. J. Neurosci. 41, 3254–3265 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Liu, B., Tian, Q. & Gu, Y. Robust vestibular self-motion signals in macaque posterior cingulate region. eLife 10, e64569 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Bremmer, F., Kubischik, M., Pekel, M., Lappe, M. & Hoffmann, K. P. Linear vestibular self-motion signals in monkey medial superior temporal area. Ann. N. Y. Acad. Sci. 871, 272–281 (1999).

    Article  CAS  PubMed  Google Scholar 

  20. Duffy, C. J. MST neurons respond to optic flow and translational movement. J. Neurophysiol. 80, 1816–1827 (1998).

    Article  CAS  PubMed  Google Scholar 

  21. Gu, Y., Watkins, P. V., Angelaki, D. E. & DeAngelis, G. C. Visual and nonvisual contributions to three-dimensional heading selectivity in the medial superior temporal area. J. Neurosci. 26, 73–85 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Sasaki, R., Angelaki, D. E. & DeAngelis, G. C. Processing of object motion and self-motion in the lateral subdivision of the medial superior temporal area in macaques. J. Neurophysiol. 121, 1207–1221 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  23. Bremmer, F., Klam, F., Duhamel, J. R., Ben Hamed, S. & Graf, W. Visual–vestibular interactive responses in the macaque ventral intraparietal area (VIP). Eur. J. Neurosci. 16, 1569–1586 (2002).

    Article  PubMed  Google Scholar 

  24. Chen, A., DeAngelis, G. C. & Angelaki, D. E. Representation of vestibular and visual cues to self-motion in ventral intraparietal cortex. J. Neurosci. 31, 12036–12052 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Chen, A., Deangelis, G. C. & Angelaki, D. E. Functional specializations of the ventral intraparietal area for multisensory heading discrimination. J. Neurosci. 33, 3567–3581 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Avila, E., Lakshminarasimhan, K. J., DeAngelis, G. C. & Angelaki, D. E. Visual and vestibular selectivity for self-motion in macaque posterior parietal area 7a. Cereb. Cortex 29, 3932–3947 (2019).

    Article  PubMed  Google Scholar 

  27. Chen, A., DeAngelis, G. C. & Angelaki, D. E. Convergence of vestibular and visual self-motion signals in an area of the posterior sylvian fissure. J. Neurosci. 31, 11617–11627 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Gu, Y., Cheng, Z., Yang, L., DeAngelis, G. C. & Angelaki, D. E. Multisensory convergence of visual and vestibular heading cues in the pursuit area of the frontal eye field. Cereb. Cortex 26, 3785–3801 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  29. Zhao, B., Zhang, Y. & Chen, A. Encoding of vestibular and optic flow cues to self-motion in the posterior superior temporal polysensory area. J. Physiol. 599, 3937–3954 (2021).

    Article  CAS  PubMed  Google Scholar 

  30. Lappe, M., Bremmer, F., Pekel, M., Thiele, A. & Hoffmann, K. P. Optic flow processing in monkey STS: a theoretical and experimental approach. J. Neurosci. 16, 6265–6285 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Gu, Y., Fetsch, C. R., Adeyemo, B., Deangelis, G. C. & Angelaki, D. E. Decoding of MSTd population activity accounts for variations in the precision of heading perception. Neuron 66, 596–609 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Crowell, J. A. & Banks, M. S. Perceiving heading with different retinal regions and types of optic flow. Percept. Psychophys. 53, 325–337 (1993).

    Article  CAS  PubMed  Google Scholar 

  33. Chen, A., Gu, Y., Liu, S., DeAngelis, G. C. & Angelaki, D. E. Evidence for a causal contribution of macaque vestibular, but not intraparietal, cortex to heading perception. J. Neurosci. 36, 3789–3798 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Gu, Y., Deangelis, G. C. & Angelaki, D. E. Causal links between dorsal medial superior temporal area neurons and multisensory heading perception. J. Neurosci. 32, 2299–2313 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Schneider, A. D., Jamali, M., Carriot, J., Chacron, M. J. & Cullen, K. E. The increased sensitivity of irregular peripheral canal and otolith vestibular afferents optimizes their encoding of natural stimuli. J. Neurosci. 35, 5522–5536 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Goldberg, J. M. et al. The Vestibular System: A Sixth Sense (Oxford Univ. Press, 2012).

  37. Cullen, K. E. Vestibular processing during natural self-motion: implications for perception and action. Nat. Rev. Neurosci. 20, 346–363 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Angelaki, D. E. & Dickman, J. D. Spatiotemporal processing of linear acceleration: primary afferent and central vestibular neuron responses. J. Neurophysiol. 84, 2113–2132 (2000).

    Article  CAS  PubMed  Google Scholar 

  39. Laurens, J. et al. Transformation of spatiotemporal dynamics in the macaque vestibular system from otolith afferents to cortex. eLife 6, e20787 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  40. Gu, Y. Vestibular signals in primate cortex for self-motion perception. Curr. Opin. Neurobiol. 52, 10–17 (2018).

    Article  CAS  PubMed  Google Scholar 

  41. Hou, H., Zheng, Q., Zhao, Y., Pouget, A. & Gu, Y. Neural correlates of optimal multisensory decision making under time-varying reliabilities with an invariant linear probabilistic population code. Neuron 104, 1010–1021.e1010 (2019).

    Article  CAS  PubMed  Google Scholar 

  42. Zheng, Q., Zhou, L. & Gu, Y. Temporal synchrony effects of optic flow and vestibular inputs on multisensory heading perception. Cell Rep. 37, 109999 (2021).

    Article  CAS  PubMed  Google Scholar 

  43. Zeng, Z., Zhang, C., Xu, Y., He, H. & Gu, Y. Distinct population code and critical roles of the primate caudate nucleus in multisensory decision making. Nat. Commun. 16, 5253 (2025).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Drugowitsch, J., DeAngelis, G. C., Klier, E. M., Angelaki, D. E. & Pouget, A. Optimal multisensory decision-making in a reaction-time task. eLife 3, e03005 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  45. Cheng, Z. & Gu, Y. Distributed representation of curvilinear self-motion in the macaque parietal cortex. Cell Rep. 15, 1013–1023 (2016).

    Article  CAS  PubMed  Google Scholar 

  46. Carriot, J., Jamali, M., Brooks, J. X. & Cullen, K. E. Integration of canal and otolith inputs by central vestibular neurons is subadditive for both active and passive self-motion: implication for perception. J. Neurosci. 35, 3555–3565 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Newlands, S. D., Abbatematteo, B., Wei, M., Carney, L. H. & Luan, H. Convergence of linear acceleration and yaw rotation signals on non-eye movement neurons in the vestibular nucleus of macaques. J. Neurophysiol. 119, 73–83 (2018).

    Article  PubMed  Google Scholar 

  48. Massot, C., Chacron, M. J. & Cullen, K. E. Information transmission and detection thresholds in the vestibular nuclei: single neurons vs. population encoding. J. Neurophysiol. 105, 1798–1814 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  49. Sadeghi, S. G., Chacron, M. J., Taylor, M. C. & Cullen, K. E. Neural variability, detection thresholds, and information transmission in the vestibular system. J. Neurosci. 27, 771–781 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Haburcakova, C., Lewis, R. F. & Merfeld, D. M. Frequency dependence of vestibuloocular reflex thresholds. J. Neurophysiol. 107, 973–983 (2012).

    Article  PubMed  Google Scholar 

  51. Gibson, J. J. The Perception of the Visual World (Houghton Mifflin, 1950).

  52. Warren, W. H. The dynamics of perception and action. Psychol. Rev. 113, 358–389 (2006).

    Article  PubMed  Google Scholar 

  53. Matthis, J. S., Muller, K. S., Bonnen, K. L. & Hayhoe, M. M. Retinal optic flow during natural locomotion. PLoS Comput. Biol. 18, e1009575 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Burlingham, C. S. & Heeger, D. J. Heading perception depends on time-varying evolution of optic flow. Proc. Natl Acad. Sci. USA 117, 33161–33169 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Lappe, M., Bremmer, F. & van den Berg, A. V. Perception of self-motion from visual flow. Trends Cogn. Sci. 3, 329–336 (1999).

    Article  CAS  PubMed  Google Scholar 

  56. Li, L., Sweet, B. T. & Stone, L. S. Humans can perceive heading without visual path information. J. Vis. 6, 874–881 (2006).

    Article  PubMed  Google Scholar 

  57. Banks, M. S., Ehrlich, S. M., Backus, B. T. & Crowell, J. A. Estimating heading during real and simulated eye movements. Vis. Res. 36, 431–443 (1996).

    Article  CAS  PubMed  Google Scholar 

  58. Dash, S., Baliga, V. B., Lapsansky, A. B., Wylie, D. R. & Altshuler, D. L. Encoding of global visual motion in the avian pretectum shifts from a bias for temporal-to-nasal selectivity to omnidirectional excitation across speeds. eNeuro 11, ENEURO.0301-24.2024 (2024).

    Article  PubMed  PubMed Central  Google Scholar 

  59. Gutierrez-Ibanez, C., Wylie, D. R. & Altshuler, D. L. From the eye to the wing: neural circuits for transforming optic flow into motor output in avian flight. J. Comp. Physiol. A 209, 839–854 (2023).

    Article  Google Scholar 

  60. Meng, H. & Angelaki, D. E. Responses of ventral posterior thalamus neurons to three-dimensional vestibular and optic flow stimulation. J. Neurophysiol. 103, 817–826 (2010).

    Article  PubMed  Google Scholar 

  61. Britten, K. H. Mechanisms of self-motion perception. Annu. Rev. Neurosci. 31, 389–410 (2008).

    Article  CAS  PubMed  Google Scholar 

  62. Chowdhury, S. A., Takahashi, K., DeAngelis, G. C. & Angelaki, D. E. Does the middle temporal area carry vestibular signals related to self-motion? J. Neurosci. 29, 12020–12030 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Duffy, C. J. & Wurtz, R. H. Response of monkey MST neurons to optic flow stimuli with shifted centers of motion. J. Neurosci. 15, 5192–5208 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Bremmer, F., Kubischik, M., Pekel, M., Hoffmann, K. P. & Lappe, M. Visual selectivity for heading in monkey area MST. Exp. Brain Res. 200, 51–60 (2010).

    Article  PubMed  Google Scholar 

  65. Li, W., Lu, J., Zhu, Z. & Gu, Y. Causal contribution of optic flow signal in macaque extrastriate visual cortex for roll perception. Nat. Commun. 13, 5479 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Zhang, T. & Britten, K. H. The responses of VIP neurons are sufficiently sensitive to support heading judgments. J. Neurophysiol. 103, 1865–1873 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  67. Zhang, T., Heuer, H. W. & Britten, K. H. Parietal area VIP neuronal responses to heading stimuli are encoded in head-centered coordinates. Neuron 42, 993–1001 (2004).

    Article  CAS  PubMed  Google Scholar 

  68. Kaminiarz, A., Schlack, A., Hoffmann, K. P., Lappe, M. & Bremmer, F. Visual selectivity for heading in the macaque ventral intraparietal area. J. Neurophysiol. 112, 2470–2480 (2014).

    Article  PubMed  Google Scholar 

  69. Anderson, K. C. & Siegel, R. M. Optic flow selectivity in the anterior superior temporal polysensory area, STPa, of the behaving monkey. J. Neurosci. 19, 2681–2692 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Galletti, C., Fattori, P., Gamberini, M. & Kutz, D. F. The cortical visual area V6: brain location and visual topography. Eur. J. Neurosci. 11, 3922–3936 (1999).

    Article  CAS  PubMed  Google Scholar 

  71. Fan, R. H., Liu, S., DeAngelis, G. C. & Angelaki, D. E. Heading tuning in macaque area V6. J. Neurosci. 35, 16303–16314 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Wall, M. B. & Smith, A. T. The representation of egomotion in the human brain. Curr. Biol. 18, 191–194 (2008).

    Article  CAS  PubMed  Google Scholar 

  73. Britten, K. H. & van Wezel, R. J. Electrical microstimulation of cortical area MST biases heading perception in monkeys. Nat. Neurosci. 1, 59–63 (1998).

    Article  CAS  PubMed  Google Scholar 

  74. Yu, X. & Gu, Y. Probing sensory readout via combined choice-correlation measures and microstimulation perturbation. Neuron 100, 715–727.e715 (2018).

    Article  CAS  PubMed  Google Scholar 

  75. Schmitt, C., Baltaretu, B. R., Crawford, J. D. & Bremmer, F. A causal role of area hMST for self-motion perception in humans. Cereb. Cortex Commun. 1, tgaa042 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  76. Jeurissen, D., Shushruth, S., El-Shamayleh, Y., Horwitz, G. D. & Shadlen, M. N. Deficits in decision-making induced by parietal cortex inactivation are compensated at two timescales. Neuron 110, 1924–1931.e1925 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Duhamel, J. R., Bremmer, F., Ben Hamed, S. & Graf, W. Spatial invariance of visual receptive fields in parietal cortex neurons. Nature 389, 845–848 (1997).

    Article  CAS  PubMed  Google Scholar 

  78. Cooke, D. F., Taylor, C. S., Moore, T. & Graziano, M. S. Complex movements evoked by microstimulation of the ventral intraparietal area. Proc. Natl Acad. Sci. USA 100, 6163–6168 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Viswanathan, P. & Nieder, A. Differential impact of behavioral relevance on quantity coding in primate frontal and parietal neurons. Curr. Biol. 25, 1259–1269 (2015).

    Article  CAS  PubMed  Google Scholar 

  80. Zhang, T. & Britten, K. H. Parietal area VIP causally influences heading perception during pursuit eye movements. J. Neurosci. 31, 2569–2575 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Telford, L., Howard, I. P. & Ohmi, M. Heading judgments during active and passive self-motion. Exp. Brain Res. 104, 502–510 (1995).

    Article  CAS  PubMed  Google Scholar 

  82. Ohmi, M. Egocentric perception through interaction among many sensory systems. Brain Res. Cogn. Brain Res. 5, 87–96 (1996).

    Article  CAS  PubMed  Google Scholar 

  83. Harris, L. R., Jenkin, M. & Zikovitz, D. C. Visual and non-visual cues in the perception of linear self-motion. Exp. Brain Res. 135, 12–21 (2000).

    Article  CAS  PubMed  Google Scholar 

  84. Bertin, R. J. & Berthoz, A. Visuo-vestibular interaction in the reconstruction of travelled trajectories. Exp. Brain Res. 154, 11–21 (2004).

    Article  CAS  PubMed  Google Scholar 

  85. Butler, J. S., Smith, S. T., Campos, J. L. & Bulthoff, H. H. Bayesian integration of visual and vestibular signals for heading. J. Vis. 10, 23 (2010).

    Article  PubMed  Google Scholar 

  86. Crane, B. T. Effect of eye position during human visual-vestibular integration of heading perception. J. Neurophysiol. 118, 1609–1621 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  87. Gu, Y., Angelaki, D. E. & Deangelis, G. C. Neural correlates of multisensory cue integration in macaque MSTd. Nat. Neurosci. 11, 1201–1210 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Fetsch, C. R., Pouget, A., DeAngelis, G. C. & Angelaki, D. E. Neural correlates of reliability-based cue weighting during multisensory integration. Nat. Neurosci. 15, 146–154 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  89. Keshavarzi, S. et al. Multisensory coding of angular head velocity in the retrosplenial cortex. Neuron 110, 532–543.e539 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Fetsch, C. R., DeAngelis, G. C. & Angelaki, D. E. Bridging the gap between theories of sensory cue integration and the physiology of multisensory neurons. Nat. Rev. Neurosci. 14, 429–442 (2013).

    Article  CAS  PubMed  Google Scholar 

  91. Morgan, M. L., Deangelis, G. C. & Angelaki, D. E. Multisensory integration in macaque visual cortex depends on cue reliability. Neuron 59, 662–673 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Gu, Y., Angelaki, D. E. & DeAngelis, G. C. Contribution of correlated noise and selective decoding to choice probability measurements in extrastriate visual cortex. eLife 3, e02670 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  93. Hennestad, E., Witoelar, A., Chambers, A. R. & Vervaeke, K. Mapping vestibular and visual contributions to angular head velocity tuning in the cortex. Cell Rep. 37, 110134 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Sun, H. et al. Conjunctive processing of spatial border and locomotion in retrosplenial cortex during spatial navigation. J. Physiol. 602, 5017–5038 (2024).

    Article  CAS  PubMed  Google Scholar 

  95. Velez-Fort, M. et al. A circuit for integration of head- and visual-motion signals in layer 6 of mouse primary visual cortex. Neuron 98, 179–191.e176 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Zhang, W. H. et al. Complementary congruent and opposite neurons achieve concurrent multisensory integration and segregation. eLife 8, e43753 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  97. Kim, H. R., Angelaki, D. E. & DeAngelis, G. C. A neural mechanism for detecting object motion during self-motion. eLife 11, e74971 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Sasaki, R., Angelaki, D. E. & DeAngelis, G. C. Dissociation of self-motion and object motion by linear population decoding that approximates marginalization. J. Neurosci. 37, 11204–11219 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Dicke, P. W., Chakraborty, S. & Thier, P. Neuronal correlates of perceptual stability during eye movements. Eur. J. Neurosci. 27, 991–1002 (2008).

    Article  PubMed  Google Scholar 

  100. Lisberger, S. G. & Movshon, J. A. Visual motion analysis for pursuit eye movements in area MT of macaque monkeys. J. Neurosci. 19, 2224–2246 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Baden, T. et al. A synaptic mechanism for temporal filtering of visual signals. PLoS Biol. 12, e1001972 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  102. Bizley, J. K., Jones, G. P. & Town, S. M. Where are multisensory signals combined for perceptual decision-making? Curr. Opin. Neurobiol. 40, 31–37 (2016).

    Article  CAS  PubMed  Google Scholar 

  103. Kalman, R. E. A new approach to linear filtering and prediction problems. J. Basic Eng. 82, 32–45 (1960).

    Article  Google Scholar 

  104. Sperry, R. W. Neural basis of the spontaneous optokinetic response produced by visual inversion. J. Comp. Physiol. Psychol. 43, 482–489 (1950).

    Article  CAS  PubMed  Google Scholar 

  105. Young, L. R. Optimal estimator models for spatial orientation and vestibular nystagmus. Exp. Brain Res. 210, 465–476 (2011).

    Article  PubMed  Google Scholar 

  106. Laurens, J. & Angelaki, D. E. A unified internal model theory to resolve the paradox of active versus passive self-motion sensation. eLife 6, e28074 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  107. Von holst, E. & Mittelstaedt, H. The reafference principle: interaction between the central nervous system and the periphery. Naturwissenschaften 37, 464–476 (1950).

    Google Scholar 

  108. Cullen, K. E. & Minor, L. B. Semicircular canal afferents similarly encode active and passive head-on-body rotations: implications for the role of vestibular efference. J. Neurosci. 22, RC226 (2002).

    Article  PubMed  PubMed Central  Google Scholar 

  109. Jamali, M., Sadeghi, S. G. & Cullen, K. E. Response of vestibular nerve afferents innervating utricle and saccule during passive and active translations. J. Neurophysiol. 101, 141–149 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  110. Mackrous, I., Carriot, J. & Cullen, K. E. Context-independent encoding of passive and active self-motion in vestibular afferent fibers during locomotion in primates. Nat. Commun. 13, 120 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Roy, J. E. & Cullen, K. E. Dissociating self-generated from passively applied head motion: neural mechanisms in the vestibular nuclei. J. Neurosci. 24, 2102–2111 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Carriot, J., Brooks, J. X. & Cullen, K. E. Multimodal integration of self-motion cues in the vestibular system: active versus passive translations. J. Neurosci. 33, 19555–19566 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Medrea, I. & Cullen, K. E. Multisensory integration in early vestibular processing in mice: the encoding of passive vs. active motion. J. Neurophysiol. 110, 2704–2717 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  114. Marlinski, V. & McCrea, R. A. Coding of self-motion signals in ventro-posterior thalamus neurons in the alert squirrel monkey. Exp. Brain Res. 189, 463–472 (2008).

    Article  PubMed  Google Scholar 

  115. Dale, A. & Cullen, K. E. The ventral posterior lateral thalamus preferentially encodes externally applied versus active movement: implications for self-motion perception. Cereb. Cortex 29, 305–318 (2019).

    Article  PubMed  Google Scholar 

  116. Brooks, J. X. & Cullen, K. E. The primate cerebellum selectively encodes unexpected self-motion. Curr. Biol. 23, 947–955 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Klam, F. & Graf, W. Discrimination between active and passive head movements by macaque ventral and medial intraparietal cortex neurons. J. Physiol. 574, 367–386 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Zobeiri, O. A. & Cullen, K. E. Cerebellar Purkinje cells in male macaques combine sensory and motor information to predict the sensory consequences of active self-motion. Nat. Commun. 15, 4003 (2024).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Leinweber, M., Ward, D. R., Sobczak, J. M., Attinger, A. & Keller, G. B. A sensorimotor circuit in mouse cortex for visual flow predictions. Neuron 95, 1420–1432.e1425 (2017).

    Article  CAS  PubMed  Google Scholar 

  120. Zmarz, P. & Keller, G. B. Mismatch receptive fields in mouse visual cortex. Neuron 92, 766–772 (2016).

    Article  CAS  PubMed  Google Scholar 

  121. Velez-Fort, M., Cossell, L., Porta, L., Clopath, C. & Margrie, T. W. Motor and vestibular signals in the visual cortex permit the separation of self versus externally generated visual motion. Cell 188, 2175–2189.e2115 (2025).

    Article  CAS  PubMed  Google Scholar 

  122. Shinder, M. E. & Taube, J. S. Resolving the active versus passive conundrum for head direction cells. Neuroscience 270, 123–138 (2014).

    Article  CAS  PubMed  Google Scholar 

  123. Shinder, M. E. & Newlands, S. D. Sensory convergence in the parieto-insular vestibular cortex. J. Neurophysiol. 111, 2445–2464 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  124. Graham, J. A. et al. Angular head velocity cells within brainstem nuclei projecting to the head direction circuit. J. Neurosci. 43, 8403–8424 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Blair, H. T. & Sharp, P. E. Anticipatory head direction signals in anterior thalamus: evidence for a thalamocortical circuit that integrates angular head motion to compute head direction. J. Neurosci. 15, 6260–6270 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Colgin, L. L. Five decades of hippocampal place cells and EEG rhythms in behaving rats. J. Neurosci. 40, 54–60 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Song, E. Y., Kim, Y. B., Kim, Y. H. & Jung, M. W. Role of active movement in place-specific firing of hippocampal neurons. Hippocampus 15, 8–17 (2005).

    Article  PubMed  Google Scholar 

  128. Terrazas, A. et al. Self-motion and the hippocampal spatial metric. J. Neurosci. 25, 8085–8096 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Winter, S. S., Mehlman, M. L., Clark, B. J. & Taube, J. S. Passive transport disrupts grid signals in the parahippocampal cortex. Curr. Biol. 25, 2493–2502 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Shinder, M. E. & Taube, J. S. Active and passive movement are encoded equally by head direction cells in the anterodorsal thalamus. J. Neurophysiol. 106, 788–800 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  131. Shinder, M. E. & Taube, J. S. Self-motion improves head direction cell tuning. J. Neurophysiol. 111, 2479–2492 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  132. Blanco-Hernandez, E., Balsamo, G., Preston-Ferrer, P. & Burgalossi, A. Sensory and behavioral modulation of thalamic head-direction cells. Nat. Neurosci. 27, 28–33 (2024).

    Article  CAS  PubMed  Google Scholar 

  133. Lakshminarasimhan, K. J. et al. Tracking the mind’s eye: primate gaze behavior during virtual visuomotor navigation reflects belief dynamics. Neuron 106, 662–674.e665 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  134. Alefantis, P. et al. Sensory evidence accumulation using optic flow in a naturalistic navigation task. J. Neurosci. 42, 5451–5462 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. Stavropoulos, A., Lakshminarasimhan, K. J. & Angelaki, D. E. Belief embodiment through eye movements facilitates memory-guided navigation. Preprint at bioRxiv https://doi.org/10.1101/2023.08.21.554107 (2023).

  136. Zhu, S. L., Lakshminarasimhan, K. J. & Angelaki, D. E. Computational cross-species views of the hippocampal formation. Hippocampus 33, 586–599 (2023).

    Article  PubMed  PubMed Central  Google Scholar 

  137. Kaplan, R. & Friston, K. J. Planning and navigation as active inference. Biol. Cybern. 112, 323–343 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  138. Vericel, M. E., Baraduc, P., Duhamel, J. R. & Wirth, S. Organizing space through saccades and fixations between primate posterior parietal cortex and hippocampus. Nat. Commun. 15, 10448 (2024).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  139. Zhu, S., Lakshminarasimhan, K. J., Arfaei, N. & Angelaki, D. E. Eye movements reveal spatiotemporal dynamics of visually-informed planning in navigation. eLife 11, e73097 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Jacob, P. Y., Poucet, B., Liberge, M., Save, E. & Sargolini, F. Vestibular control of entorhinal cortex activity in spatial navigation. Front. Integr. Neurosci. 8, 38 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  141. Brandt, T. et al. Vestibular loss causes hippocampal atrophy and impaired spatial memory in humans. Brain 128, 2732–2741 (2005).

    Article  PubMed  Google Scholar 

  142. 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).

    Article  CAS  PubMed  Google Scholar 

  143. Laurens, J. & Angelaki, D. E. The brain compass: a perspective on how self-motion updates the head direction cell attractor. Neuron 97, 275–289 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  144. Kim, S. S., Rouault, H., Druckmann, S. & Jayaraman, V. Ring attractor dynamics in the Drosophila central brain. Science 356, 849–853 (2017).

    Article  CAS  PubMed  Google Scholar 

  145. Yoder, R. M., Clark, B. J. & Taube, J. S. Origins of landmark encoding in the brain. Trends Neurosci. 34, 561–571 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. Stackman, R. W., Clark, A. S. & Taube, J. S. Hippocampal spatial representations require vestibular input. Hippocampus 12, 291–303 (2002).

    Article  PubMed  PubMed Central  Google Scholar 

  147. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  148. Muir, G. M. et al. Disruption of the head direction cell signal after occlusion of the semicircular canals in the freely moving chinchilla. J. Neurosci. 29, 14521–14533 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  149. Valerio, S. & Taube, J. S. Head direction cell activity is absent in mice without the horizontal semicircular canals. J. Neurosci. 36, 741–754 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  150. Aghajan, Z. M. et al. Impaired spatial selectivity and intact phase precession in two-dimensional virtual reality. Nat. Neurosci. 18, 121–128 (2015).

    Article  CAS  PubMed  Google Scholar 

  151. Ravassard, P. et al. Multisensory control of hippocampal spatiotemporal selectivity. Science 340, 1342–1346 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  152. Sharp, P. E., Blair, H. T. & Cho, J. The anatomical and computational basis of the rat head-direction cell signal. Trends Neurosci. 24, 289–294 (2001).

    Article  CAS  PubMed  Google Scholar 

  153. Butler, W. N., Smith, K. S., van der Meer, M. A. A. & Taube, J. S. The head-direction signal plays a functional role as a neural compass during navigation. Curr. Biol. 27, 1259–1267 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  154. Clark, B. J., Brown, J. E. & Taube, J. S. Head direction cell activity in the anterodorsal thalamus requires intact supragenual nuclei. J. Neurophysiol. 108, 2767–2784 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  155. LaChance, P. A. & Taube, J. S. The anterior thalamus preferentially drives allocentric but not egocentric orientation tuning in postrhinal cortex. J. Neurosci. 44, e0861232024 (2024).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  156. Laurens, J. & Angelaki, D. E. A model-based reassessment of the three-dimensional tuning of head direction cells in rats. J. Neurophysiol. 122, 1274–1287 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  157. Page, H. J. I., Wilson, J. J. & Jeffery, K. J. A dual-axis rotation rule for updating the head direction cell reference frame during movement in three dimensions. J. Neurophysiol. 119, 192–208 (2018).

    Article  PubMed  Google Scholar 

  158. Angelaki, D. E. et al. A gravity-based three-dimensional compass in the mouse brain. Nat. Commun. 11, 1855 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  159. Laurens, J., Kim, B., Dickman, J. D. & Angelaki, D. E. Gravity orientation tuning in macaque anterior thalamus. Nat. Neurosci. 19, 1566–1568 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  160. Laurens, J., Meng, H. & Angelaki, D. E. Neural representation of orientation relative to gravity in the macaque cerebellum. Neuron 80, 1508–1518 (2013).

    Article  CAS  PubMed  Google Scholar 

  161. Laurens, J., Meng, H. & Angelaki, D. E. Computation of linear acceleration through an internal model in the macaque cerebellum. Nat. Neurosci. 16, 1701–1708 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  162. LaChance, P. A., Dumont, J. R., Ozel, P., Marcroft, J. L. & Taube, J. S. Commutative properties of head direction cells during locomotion in 3D: are all routes equal? J. Neurosci. 40, 3035–3051 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  163. O’Mara, S. M., Rolls, E. T., Berthoz, A. & Kesner, R. P. Neurons responding to whole-body motion in the primate hippocampus. J. Neurosci. 14, 6511–6523 (1994).

    Article  PubMed  PubMed Central  Google Scholar 

  164. Kropff, E., Carmichael, J. E., Moser, E. I. & Moser, M. B. Frequency of theta rhythm is controlled by acceleration, but not speed, in running rats. Neuron 109, 1029–1039.e1028 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  165. Srinivasan, M., Zhang, S., Lehrer, M. & Collett, T. Honeybee navigation en route to the goal: visual flight control and odometry. J. Exp. Biol. 199, 237–244 (1996).

    Article  CAS  PubMed  Google Scholar 

  166. Esch, H. E., Zhang, S., Srinivasan, M. V. & Tautz, J. Honeybee dances communicate distances measured by optic flow. Nature 411, 581–583 (2001).

    Article  CAS  PubMed  Google Scholar 

  167. Srinivasan, M. V., Zhang, S., Altwein, M. & Tautz, J. Honeybee navigation: nature and calibration of the “odometer”. Science 287, 851–853 (2000).

    Article  CAS  PubMed  Google Scholar 

  168. Heinze, S., Narendra, A. & Cheung, A. Principles of insect path integration. Curr. Biol. 28, R1043–R1058 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  169. Pfeffer, S. E. & Wittlinger, M. Optic flow odometry operates independently of stride integration in carried ants. Science 353, 1155–1157 (2016).

    Article  CAS  PubMed  Google Scholar 

  170. Ellmore, T. M. & McNaughton, B. L. Human path integration by optic flow. Spatial Cognit. Comput. 4, 255–272 (2004).

    Article  Google Scholar 

  171. Frenz, H. & Lappe, M. Absolute travel distance from optic flow. Vis. Res. 45, 1679–1692 (2005).

    Article  PubMed  Google Scholar 

  172. Kearns, M. J., Warren, W. H., Duchon, A. P. & Tarr, M. J. Path integration from optic flow and body senses in a homing task. Perception 31, 349–374 (2002).

    Article  PubMed  Google Scholar 

  173. Petzschner, F. H. & Glasauer, S. Iterative Bayesian estimation as an explanation for range and regression effects: a study on human path integration. J. Neurosci. 31, 17220–17229 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  174. Redlick, F. P., Jenkin, M. & Harris, L. R. Humans can use optic flow to estimate distance of travel. Vis. Res. 41, 213–219 (2001).

    Article  CAS  PubMed  Google Scholar 

  175. Campbell, M. G. et al. Principles governing the integration of landmark and self-motion cues in entorhinal cortical codes for navigation. Nat. Neurosci. 21, 1096–1106 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  176. Kautzky, M. & Thurley, K. Estimation of self-motion duration and distance in rodents. R. Soc. Open Sci. 3, 160118 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  177. Thurley, K. & Ayaz, A. Virtual reality systems for rodents. Curr. Zool. 63, 109–119 (2017).

    Article  PubMed  Google Scholar 

  178. Sherrill, K. R. et al. Functional connections between optic flow areas and navigationally responsive brain regions during goal-directed navigation. Neuroimage 118, 386–396 (2015).

    Article  PubMed  Google Scholar 

  179. Arleo, A. et al. Optic flow stimuli update anterodorsal thalamus head direction neuronal activity in rats. J. Neurosci. 33, 16790–16795 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  180. 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).

    Article  CAS  PubMed  Google Scholar 

  181. Mao, D., Molina, L. A., Bonin, V. & McNaughton, B. L. Vision and locomotion combine to drive path integration sequences in mouse retrosplenial cortex. Curr. Biol. 30, 1680–1688.e1684 (2020).

    Article  CAS  PubMed  Google Scholar 

  182. Madhav, M. S. et al. Control and recalibration of path integration in place cells using optic flow. Nat. Neurosci. 27, 1599–1608 (2024).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  183. Foo, P., Warren, W. H., Duchon, A. & Tarr, M. J. Do humans integrate routes into a cognitive map? Map- versus landmark-based navigation of novel shortcuts. J. Exp. Psychol. Learn. Mem. Cogn. 31, 195–215 (2005).

    Article  PubMed  Google Scholar 

  184. Collett, M. & Collett, T. S. How do insects use path integration for their navigation? Biol. Cybern. 83, 245–259 (2000).

    Article  CAS  PubMed  Google Scholar 

  185. Sommer, S., von Beeren, C. & Wehner, R. Multiroute memories in desert ants. Proc. Natl Acad. Sci. USA 105, 317–322 (2008).

    Article  CAS  PubMed  Google Scholar 

  186. Etienne, A. S., Maurer, R., Boulens, V., Levy, A. & Rowe, T. Resetting the path integrator: a basic condition for route-based navigation. J. Exp. Biol. 207, 1491–1508 (2004).

    Article  PubMed  Google Scholar 

  187. Etienne, A. S., Maurer, R. & Seguinot, V. Path integration in mammals and its interaction with visual landmarks. J. Exp. Biol. 199, 201–209 (1996).

    Article  CAS  PubMed  Google Scholar 

  188. Tcheang, L., Bulthoff, H. H. & Burgess, N. Visual influence on path integration in darkness indicates a multimodal representation of large-scale space. Proc. Natl Acad. Sci. USA 108, 1152–1157 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  189. Nardini, M., Jones, P., Bedford, R. & Braddick, O. Development of cue integration in human navigation. Curr. Biol. 18, 689–693 (2008).

    Article  CAS  PubMed  Google Scholar 

  190. Jayakumar, R. P. et al. Recalibration of path integration in hippocampal place cells. Nature 566, 533–537 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  191. Secer, G., Knierim, J. J. & Cowan, N. J. Continuous bump attractor networks require explicit error coding for gain recalibration. Preprint at bioRxiv https://doi.org/10.1101/2024.02.12.579874 (2024).

  192. Yang, C. et al. A population code for spatial representation in the zebrafish telencephalon. Nature 634, 397–406 (2024).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  193. Noppeney, U. Perceptual inference, learning, and attention in a multisensory world. Annu. Rev. Neurosci. 44, 449–473 (2021).

    Article  CAS  PubMed  Google Scholar 

  194. Byrne, P., Becker, S. & Burgess, N. Remembering the past and imagining the future: a neural model of spatial memory and imagery. Psychol. Rev. 114, 340–375 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  195. Rolls, E. T. A theory and model of scene representations with hippocampal spatial view cells. Hippocampus 35, e70013 (2025).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  196. Andersen, R. A. & Mountcastle, V. B. The influence of the angle of gaze upon the excitability of the light-sensitive neurons of the posterior parietal cortex. J. Neurosci. 3, 532–548 (1983).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  197. Andersen, R. A., Essick, G. K. & Siegel, R. M. Encoding of spatial location by posterior parietal neurons. Science 230, 456–458 (1985).

    Article  CAS  PubMed  Google Scholar 

  198. Chen, X., Deangelis, G. C. & Angelaki, D. E. Diverse spatial reference frames of vestibular signals in parietal cortex. Neuron 80, 1310–1321 (2013).

    Article  CAS  PubMed  Google Scholar 

  199. Martin, C. Z., Brooks, J. X. & Green, A. M. Role of rostral fastigial neurons in encoding a body-centered representation of translation in three dimensions. J. Neurosci. 38, 3584–3602 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  200. Brooks, J. X. & Cullen, K. E. Multimodal integration in rostral fastigial nucleus provides an estimate of body movement. J. Neurosci. 29, 10499–10511 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  201. Bicanski, A. & Burgess, N. A neural-level model of spatial memory and imagery. eLife 7, e33752 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  202. Alexander, A. S. & Nitz, D. A. Retrosplenial cortex maps the conjunction of internal and external spaces. Nat. Neurosci. 18, 1143–1151 (2015).

    Article  CAS  PubMed  Google Scholar 

  203. Cho, J. & Sharp, P. E. Head direction, place, and movement correlates for cells in the rat retrosplenial cortex. Behav. Neurosci. 115, 3–25 (2001).

    Article  CAS  PubMed  Google Scholar 

  204. Wang, C. et al. Egocentric coding of external items in the lateral entorhinal cortex. Science 362, 945–949 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  205. Cheng, N. et al. Egocentric processing of items in spines, dendrites, and somas in the retrosplenial cortex. Neuron 112, 646–660.e648 (2024).

    Article  CAS  PubMed  Google Scholar 

  206. Shine, J. P., Valdes-Herrera, J. P., Hegarty, M. & Wolbers, T. The human retrosplenial cortex and thalamus code head direction in a global reference frame. J. Neurosci. 36, 6371–6381 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  207. Chen, L. L., Lin, L. H., Green, E. J., Barnes, C. A. & McNaughton, B. L. Head-direction cells in the rat posterior cortex. I. Anatomical distribution and behavioral modulation. Exp. Brain Res. 101, 8–23 (1994).

    Article  CAS  PubMed  Google Scholar 

  208. Rolls, E. T. Neurons including hippocampal spatial view cells, and navigation in primates including humans. Hippocampus 31, 593–611 (2021).

    Article  PubMed  Google Scholar 

  209. McNaughton, B. L., Knierim, J. J., & Wilson, M. A. in The Cognitive Neurosciences (ed. Gazzaniga, M. S.) 585–595 (MIT Press, 1995).

  210. Mao, D. et al. Spatial modulation of hippocampal activity in freely moving macaques. Neuron 109, 3521–3534.e3526 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  211. Xu, X., Du, K. & Mao, D. Spatial dissociation between recognition and navigation in the primate hippocampus. Sci. Adv. 10, eado7392 (2024).

    Article  PubMed  PubMed Central  Google Scholar 

  212. Pouget, A. & Sejnowski, T. J. Spatial transformations in the parietal cortex using basis functions. J. Cogn. Neurosci. 9, 222–237 (1997).

    Article  CAS  PubMed  Google Scholar 

  213. Pouget, A., Deneve, S. & Duhamel, J. R. A computational perspective on the neural basis of multisensory spatial representations. Nat. Rev. Neurosci. 3, 741–747 (2002).

    Article  CAS  PubMed  Google Scholar 

  214. Sasaki, R., Anzai, A., Angelaki, D. E. & DeAngelis, G. C. Flexible coding of object motion in multiple reference frames by parietal cortex neurons. Nat. Neurosci. 23, 1004–1015 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  215. Chen, X., DeAngelis, G. C. & Angelaki, D. E. Flexible egocentric and allocentric representations of heading signals in parietal cortex. Proc. Natl Acad. Sci. USA 115, E3305–E3312 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  216. Wang, C., Chen, X. & Knierim, J. J. Egocentric and allocentric representations of space in the rodent brain. Curr. Opin. Neurobiol. 60, 12–20 (2020).

    Article  CAS  PubMed  Google Scholar 

  217. Nau, M., Julian, J. B. & Doeller, C. F. How the brain’s navigation system shapes our visual experience. Trends Cogn. Sci. 22, 810–825 (2018).

    Article  PubMed  Google Scholar 

  218. Angelaki, D. E. & Cullen, K. E. Vestibular system: the many facets of a multimodal sense. Annu. Rev. Neurosci. 31, 125–150 (2008).

    Article  CAS  PubMed  Google Scholar 

  219. Li, L. Visual perception of self-motion. Annu. Rev. Vis. Sci. 11, 20.1–20.28 (2025). In press.

    Article  Google Scholar 

  220. Nadler, J. W. et al. Joint representation of depth from motion parallax and binocular disparity cues in macaque area MT. J. Neurosci. 33, 14061–14074 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  221. Kropff, E., Carmichael, J. E., Moser, M. B. & Moser, E. I. Speed cells in the medial entorhinal cortex. Nature 523, 419–424 (2015).

    Article  CAS  PubMed  Google Scholar 

  222. Casali, G., Bush, D. & Jeffery, K. Altered neural odometry in the vertical dimension. Proc. Natl Acad. Sci. USA 116, 4631–4636 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  223. Qiu, S. et al. Whole-brain spatial organization of hippocampal single-neuron projectomes. Science 383, eadj9198 (2024).

    Article  CAS  PubMed  Google Scholar 

  224. Guldin, W. O. & Grusser, O. J. Is there a vestibular cortex? Trends Neurosci. 21, 254–259 (1998).

    Article  CAS  PubMed  Google Scholar 

  225. Felleman, D. J. & Van Essen, D. C. Distributed hierarchical processing in the primate cerebral cortex. Cereb. Cortex 1, 1–47 (1991).

    Article  CAS  PubMed  Google Scholar 

  226. Shinder, M. E. & Taube, J. S. Differentiating ascending vestibular pathways to the cortex involved in spatial cognition. J. Vestib. Res. 20, 3–23 (2010).

    Article  PubMed  Google Scholar 

  227. Ebata, S., Sugiuchi, Y., Izawa, Y., Shinomiya, K. & Shinoda, Y. Vestibular projection to the periarcuate cortex in the monkey. Neurosci. Res. 49, 55–68 (2004).

    Article  CAS  PubMed  Google Scholar 

  228. Kobayashi, Y. & Amaral, D. G. Macaque monkey retrosplenial cortex: II. Cortical afferents. J. Comp. Neurol. 466, 48–79 (2003).

    Article  PubMed  Google Scholar 

  229. Morecraft, R. J., Geula, C. & Mesulam, M. M. Architecture of connectivity within a cingulo-fronto-parietal neurocognitive network for directed attention. Arch. Neurol. 50, 279–284 (1993).

    Article  CAS  PubMed  Google Scholar 

  230. Suzuki, W. A. & Amaral, D. G. Perirhinal and parahippocampal cortices of the macaque monkey: cortical afferents. J. Comp. Neurol. 350, 497–533 (1994).

    Article  CAS  PubMed  Google Scholar 

  231. Ding, S. L., Van Hoesen, G. & Rockland, K. S. Inferior parietal lobule projections to the presubiculum and neighboring ventromedial temporal cortical areas. J. Comp. Neurol. 425, 510–530 (2000).

    Article  CAS  PubMed  Google Scholar 

  232. Noel, J. P. & Angelaki, D. E. Cognitive, systems, and computational neurosciences of the self in motion. Annu. Rev. Psychol. 73, 103–129 (2022).

    Article  PubMed  Google Scholar 

  233. Lewis, J. W. & Van Essen, D. C. Corticocortical connections of visual, sensorimotor, and multimodal processing areas in the parietal lobe of the macaque monkey. J. Comp. Neurol. 428, 112–137 (2000).

    Article  CAS  PubMed  Google Scholar 

  234. Akbarian, S., Grusser, O. J. & Guldin, W. O. Thalamic connections of the vestibular cortical fields in the squirrel monkey (Saimiri sciureus). J. Comp. Neurol. 326, 423–441 (1992).

    Article  CAS  PubMed  Google Scholar 

  235. Boussaoud, D., Ungerleider, L. G. & Desimone, R. Pathways for motion analysis: cortical connections of the medial superior temporal and fundus of the superior temporal visual areas in the macaque. J. Comp. Neurol. 296, 462–495 (1990).

    Article  CAS  PubMed  Google Scholar 

  236. Baizer, J. S., Ungerleider, L. G. & Desimone, R. Organization of visual inputs to the inferior temporal and posterior parietal cortex in macaques. J. Neurosci. 11, 168–190 (1991).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  237. Lynch, J. C. & Tian, J. R. Cortico-cortical networks and cortico-subcortical loops for the higher control of eye movements. Prog. Brain Res. 151, 461–501 (2006).

    Article  CAS  PubMed  Google Scholar 

  238. Kobayashi, Y. & Amaral, D. G. Macaque monkey retrosplenial cortex: III. Cortical efferents. J. Comp. Neurol. 502, 810–833 (2007).

    Article  PubMed  Google Scholar 

  239. Clark, B. J., Simmons, C. M., Berkowitz, L. E. & Wilber, A. A. The retrosplenial–parietal network and reference frame coordination for spatial navigation. Behav. Neurosci. 132, 416–429 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  240. Salinas, E. & Sejnowski, T. J. Gain modulation in the central nervous system: where behavior, neurophysiology, and computation meet. Neuroscientist 7, 430–440 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  241. Ernst, M. O. & Banks, M. S. Humans integrate visual and haptic information in a statistically optimal fashion. Nature 415, 429–433 (2002).

    Article  CAS  PubMed  Google Scholar 

  242. Kording, K. P. et al. Causal inference in multisensory perception. PLoS ONE 2, e943 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  243. Acerbi, L., Dokka, K., Angelaki, D. E. & Ma, W. J. Bayesian comparison of explicit and implicit causal inference strategies in multisensory heading perception. PLoS Comput. Biol. 14, e1006110 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  244. Brotchie, P. R., Andersen, R. A., Snyder, L. H. & Goodman, S. J. Head position signals used by parietal neurons to encode locations of visual stimuli. Nature 375, 232–235 (1995).

    Article  CAS  PubMed  Google Scholar 

  245. Salinas, E. & Abbott, L. F. Transfer of coded information from sensory to motor networks. J. Neurosci. 15, 6461–6474 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors thank K. Du for his conscientious assistance in drafting the figures. This work was supported by grants from the National Science and Technology Innovation 2030 Major Program (no. 2022ZD0205000).

Author information

Authors and Affiliations

  1. Center for Excellence in Brain Science and Intelligence Technology, Key Laboratory of Brain Cognition and Brain-inspired Intelligence Technology, Institute of Neuroscience, International Center for Primate Brain Research, Chinese Academy of Sciences, Shanghai, China

    Dun Mao & Yong Gu

  2. University of Chinese Academy of Sciences, Beijing, China

    Dun Mao & Yong Gu

Authors
  1. Dun Mao
    View author publications

    Search author on:PubMed Google Scholar

  2. Yong Gu
    View author publications

    Search author on:PubMed Google Scholar

Contributions

The authors contributed equally to all aspects of the article.

Corresponding author

Correspondence to Yong Gu.

Ethics declarations

Competing interests

The authors declare no competing interests.

Peer review

Peer review information

Nature Reviews Neuroscience thanks Kate Jeffery and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Glossary

Cognitive map

A mental representation of explored space that allows individuals to flexibly plan routes from any starting location and head direction to goals within this map.

Conjunctive tuning

The capacity of some neurons to simultaneously encode multiple stimulus features, for example, head direction and moving speed.

Inertial motion

A tendency to maintain the current motion state of an object (for example, constant speed) until an extra force is applied that is large enough to change the state of the object (for example, by accelerating it).

Landmark cues

Physical markers in the environment, such as a lighthouse, that can be reliably used by individuals to identify their location and orientation relative to the outside world.

Otoliths

A specific part of the vestibular end organs in the inner ears of vertebrates. The otoliths are composed of calcium-based crystals and are responsible for detecting linear acceleration of the head in 3D space, including gravity.

Path integration

A neural process that relies upon and integrates self-motion cues to continuously update one’s position and head direction during locomotion in the environment under conditions without external landmark cues.

Phase-lead

A situation in which two waveforms share a similar oscillating frequency, yet one reaches its maximum value earlier than the other.

Prior

The brain’s pre-existing belief or stored knowledge learned from past experiences, which may shape current perception of incoming sensory inputs.

Rotation

‌A change in the orientation‌ of an object in space as a result of it spinning around its own axis without its rotary axis being physically displaced.

Semicircular canals

A specific part of the vestibular end organs composed of three ring-shaped organs distributed orthogonal to each other in each side of the inner ear. The semicircular canals are responsible for detecting the angular acceleration of the head in three dimensions.

Sensory–motor transformation areas

Specific brain regions that convert sensory information into planned motor commands, acting as a bridge between perception and action.

Smooth pursuit

A type of eye movement in which the eyes closely track a moving object to keep its image centred on the fovea.

Translation

Movement of an entire object in space, leading to a changed location but with maintained spatial orientation.

Vestibular organs

Specialized sensory structures located within each side of the inner ear. The vestibular organs consist of the otoliths and semicircular canals, which are responsible for detecting linear acceleration and angular acceleration of the head, respectively.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mao, D., Gu, Y. Multisensory coding of self-motion and its contribution to navigation. Nat. Rev. Neurosci. 26, 715–732 (2025). https://doi.org/10.1038/s41583-025-00970-x

Download citation

  • Accepted:

  • Published:

  • Version of record:

  • Issue date:

  • DOI: https://doi.org/10.1038/s41583-025-00970-x

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing