1932

Abstract

Despite increasing evidence of its involvement in several key functions of the cerebral cortex, the vestibular sense rarely enters our consciousness. Indeed, the extent to which these internal signals are incorporated within cortical sensory representation and how they might be relied upon for sensory-driven decision-making, during, for example, spatial navigation, is yet to be understood. Recent novel experimental approaches in rodents have probed both the physiological and behavioral significance of vestibular signals and indicate that their widespread integration with vision improves both the cortical representation and perceptual accuracy of self-motion and orientation. Here, we summarize these recent findings with a focus on cortical circuits involved in visual perception and spatial navigation and highlight the major remaining knowledge gaps. We suggest that vestibulo-visual integration reflects a process of constant updating regarding the status of self-motion, and access to such information by the cortex is used for sensory perception and predictions that may be implemented for rapid, navigation-related decision-making.

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2023-07-10
2024-04-22
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Literature Cited

  1. Agster KL, Burwell RD. 2013. Hippocampal and subicular efferents and afferents of the perirhinal, postrhinal, and entorhinal cortices of the rat. Behav. Brain Res. 254:50–64
    [Google Scholar]
  2. Alexander AS, Tung JC, Chapman GW, Conner AM, Shelley LE et al. 2022. Adaptive integration of self-motion and goals in posterior parietal cortex. Cell Rep. 38:110504
    [Google Scholar]
  3. Arenz A, Silver RA, Schaefer AT, Margrie TW. 2008. The contribution of single synapses to sensory representation in vivo. Science 321:977–80
    [Google Scholar]
  4. Arleo A, Dejean C, Allegraud P, Khamassi M, Zugaro MB, Wiener SI. 2013. Optic flow stimuli update anterodorsal thalamus head direction neuronal activity in rats. J. Neurosci. 33:16790–95
    [Google Scholar]
  5. Auger SD, Maguire EA. 2013. Assessing the mechanism of response in the retrosplenial cortex of good and poor navigators. Cortex 49:2904–13
    [Google Scholar]
  6. Auger SD, Mullally SL, Maguire EA. 2012. Retrosplenial cortex codes for permanent landmarks. PLOS ONE 7:e43620
    [Google Scholar]
  7. Bassett JP, Taube JS. 2001. Neural correlates for angular head velocity in the rat dorsal tegmental nucleus. J. Neurosci. 21:5740–51
    [Google Scholar]
  8. Bassett JP, Tullman ML, Taube JS. 2007. Lesions of the tegmentomammillary circuit in the head direction system disrupt the head direction signal in the anterior thalamus. J. Neurosci. 27:7564–77
    [Google Scholar]
  9. Baumann O, Mattingley JB. 2010. Medial parietal cortex encodes perceived heading direction in humans. J. Neurosci. 30:12897–901
    [Google Scholar]
  10. Ben-Yishay E, Krivoruchko K, Ron S, Ulanovsky N, Derdikman D, Gutfreund Y 2021. Directional tuning in the hippocampal formation of birds. Curr. Biol. 31:2592–602.e4
    [Google Scholar]
  11. Bense S, Stephan T, Yousry TA, Brandt T, Dieterich M. 2001. Multisensory cortical signal increases and decreases during vestibular galvanic stimulation (fMRI). J. Neurophysiol. 85:886–99
    [Google Scholar]
  12. Best C, Lange E, Buchholz HG, Schreckenberger M, Reuss S, Dieterich M. 2014. Left hemispheric dominance of vestibular processing indicates lateralization of cortical functions in rats. Brain Struct. Funct. 219:2141–58
    [Google Scholar]
  13. 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]
  14. 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]
  15. 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]
  16. Bohne P, Schwarz MK, Herlitze S, Mark MD. 2019. A new projection from the deep cerebellar nuclei to the hippocampus via the ventrolateral and laterodorsal thalamus in mice. Front. Neural Circuits 13:51
    [Google Scholar]
  17. Bouvier G, Sanzeni A, Brunel N, Scanziani M. 2022. Inter- and intra-hemispheric sources of vestibular signals to V1 Abstract presented at the Federation of European Neuroscience Societies (FENS) Forum Paris: July 9–13
  18. Bouvier G, Senzai Y, Scanziani M. 2020. Head movements control the activity of primary visual cortex in a luminance-dependent manner. Neuron 108:500–11.e5
    [Google Scholar]
  19. Bremmer F, Kubischik M, Pekel M, Lappe M, Hoffmann KP. 1999. Linear vestibular self-motion signals in monkey medial superior temporal area. Ann. N. Y. Acad. Sci. 871:272–81
    [Google Scholar]
  20. Brennan EK, Jedrasiak-Cape I, Kailasa S, Rice SP, Sudhakar SK, Ahmed OJ. 2021. Thalamus and claustrum control parallel layer 1 circuits in retrosplenial cortex. eLife 10:e62207
    [Google Scholar]
  21. Brown APY, Cossell L, Strom M, Tyson AL, Velez-Fort M, Margrie TW. 2021. Analysis of segmentation ontology reveals the similarities and differences in connectivity onto L2/3 neurons in mouse V1. Sci. Rep. 11:4983
    [Google Scholar]
  22. Bush D, Burgess N. 2014. A hybrid oscillatory interference/continuous attractor network model of grid cell firing. J. Neurosci. 34:5065–79
    [Google Scholar]
  23. Butler JS, Smith ST, Campos JL, Bulthoff HH. 2010. Bayesian integration of visual and vestibular signals for heading. J. Vis. 10:23
    [Google Scholar]
  24. 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]
  25. Calton JL, Stackman RW, Goodridge JP, Archey WB, Dudchenko PA, Taube JS. 2003. Hippocampal place cell instability after lesions of the head direction cell network. J. Neurosci. 23:9719–31
    [Google Scholar]
  26. Campagner D, Vale R, Tan YL, Iordanidou P, Arocas OP et al. 2023. A cortico-collicular circuit for orienting to shelter during escape. Nature 613:111–19
    [Google Scholar]
  27. Carriot J, Jamali M, Chacron MJ, Cullen KE. 2017. The statistics of the vestibular input experienced during natural self-motion differ between rodents and primates. J. Physiol. 595:2751–66
    [Google Scholar]
  28. Carvalho MM, Tanke N, Kropff E, Witter MP, Moser MB, Moser EI. 2020. A brainstem locomotor circuit drives the activity of speed cells in the medial entorhinal cortex. Cell Rep. 32:108123
    [Google Scholar]
  29. Chabrol FP, Arenz A, Wiechert MT, Margrie TW, DiGregorio DA. 2015. Synaptic diversity enables temporal coding of coincident multisensory inputs in single neurons. Nat. Neurosci. 18:718–27
    [Google Scholar]
  30. Chaplin TA, Margrie TW. 2020. Cortical circuits for integration of self-motion and visual-motion signals. Curr. Opin. Neurobiol. 60:122–28
    [Google Scholar]
  31. Chen A, DeAngelis GC, Angelaki DE. 2011. Convergence of vestibular and visual self-motion signals in an area of the posterior sylvian fissure. J. Neurosci. 31:11617–27
    [Google Scholar]
  32. Chen G, Manson D, Cacucci F, Wills TJ. 2016. Absence of visual input results in the disruption of grid cell firing in the mouse. Curr. Biol. 26:2335–42
    [Google Scholar]
  33. Chen LL, Lin LH, Green EJ, Barnes CA, McNaughton BL. 1994. Head-direction cells in the rat posterior cortex. I. anatomical distribution and behavioral modulation. Exp. Brain Res. 101:8–23
    [Google Scholar]
  34. Cho J, Sharp PE. 2001. Head direction, place, and movement correlates for cells in the rat retrosplenial cortex. Behav. Neurosci. 115:3–25
    [Google Scholar]
  35. Clark BJ, Bassett JP, Wang SS, Taube JS. 2010. Impaired head direction cell representation in the anterodorsal thalamus after lesions of the retrosplenial cortex. J. Neurosci. 30:5289–302
    [Google Scholar]
  36. Crapse TB, Sommer MA. 2008. Corollary discharge across the animal kingdom. Nat. Rev. Neurosci. 9:587–600
    [Google Scholar]
  37. Cullen KE. 2019. Vestibular processing during natural self-motion: implications for perception and action. Nat. Rev. Neurosci. 20:346–63
    [Google Scholar]
  38. Cullen KE, Taube JS. 2017. Our sense of direction: progress, controversies and challenges. Nat. Neurosci. 20:1465–73
    [Google Scholar]
  39. Dannenberg H, Kelley C, Hoyland A, Monaghan CK, Hasselmo ME. 2019. The firing rate speed code of entorhinal speed cells differs across behaviorally relevant time scales and does not depend on medial septum inputs. J. Neurosci. 39:3434–53
    [Google Scholar]
  40. Dannenberg H, Lazaro H, Nambiar P, Hoyland A, Hasselmo ME. 2020. Effects of visual inputs on neural dynamics for coding of location and running speed in medial entorhinal cortex. eLife 9:e62500
    [Google Scholar]
  41. DeAngelis GC, Angelaki DE 2012. Visual-vestibular integration for self-motion perception. The Neural Bases of Multisensory Processes MM Murray, MT Wallace Boca Raton, FL: CRC Press
    [Google Scholar]
  42. Denney D, Adorjanti C. 1972. Orientation specificity of visual cortical neurons after head tilt. Exp. Brain Res. 14:312–17
    [Google Scholar]
  43. Dokka K, DeAngelis GC, Angelaki DE. 2015a. Multisensory integration of visual and vestibular signals improves heading discrimination in the presence of a moving object. J. Neurosci. 35:13599–607
    [Google Scholar]
  44. Dokka K, MacNeilage PR, DeAngelis GC, Angelaki DE. 2015b. Multisensory self-motion compensation during object trajectory judgments. Cereb. Cortex 25:619–30
    [Google Scholar]
  45. Dudchenko PA, Taube JS. 1997. Correlation between head direction cell activity and spatial behavior on a radial arm maze. Behav. Neurosci. 111:3–19
    [Google Scholar]
  46. Duffy CJ. 1998. MST neurons respond to optic flow and translational movement. J. Neurophysiol. 80:1816–27
    [Google Scholar]
  47. Dugue GP, Tihy M, Gourevitch B, Lena C. 2017. Cerebellar re-encoding of self-generated head movements. eLife 6:e26179
    [Google Scholar]
  48. Ericsson R, Knight R, Johanson Z. 2013. Evolution and development of the vertebrate neck. J. Anat. 222:67–78
    [Google Scholar]
  49. Fasold O, von Brevern M, Kuhberg M, Ploner CJ, Villringer A et al. 2002. Human vestibular cortex as identified with caloric stimulation in functional magnetic resonance imaging. Neuroimage 17:1384–93
    [Google Scholar]
  50. Fetsch CR, Pouget A, DeAngelis GC, Angelaki DE. 2011. Neural correlates of reliability-based cue weighting during multisensory integration. Nat. Neurosci. 15:146–54
    [Google Scholar]
  51. Fetsch CR, Turner AH, DeAngelis GC, Angelaki DE. 2009. Dynamic reweighting of visual and vestibular cues during self-motion perception. J. Neurosci. 29:15601–12
    [Google Scholar]
  52. Fetsch CR, Wang S, Gu Y, Deangelis GC, Angelaki DE. 2007. Spatial reference frames of visual, vestibular, and multimodal heading signals in the dorsal subdivision of the medial superior temporal area. J. Neurosci. 27:700–12
    [Google Scholar]
  53. 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]
  54. Fischer LF, Soto-Albors RM, Buck F, Harnett MT. 2020. Representation of visual landmarks in retrosplenial cortex. eLife 9:e51458
    [Google Scholar]
  55. Fiser A, Mahringer D, Oyibo HK, Petersen AV, Leinweber M, Keller GB. 2016. Experience-dependent spatial expectations in mouse visual cortex. Nat. Neurosci. 19:1658–64
    [Google Scholar]
  56. Fuhrmann F, Justus D, Sosulina L, Kaneko H, Beutel T et al. 2015. Locomotion, theta oscillations, and the speed-correlated firing of hippocampal neurons are controlled by a medial septal glutamatergic circuit. Neuron 86:1253–64
    [Google Scholar]
  57. Galloni AR, Ye Z, Rancz E. 2022. Dendritic domain-specific sampling of long-range axons shapes feedforward and feedback connectivity of L5 neurons. J. Neurosci. 42:3394–405
    [Google Scholar]
  58. Gerlei K, Passlack J, Hawes I, Vandrey B, Stevens H et al. 2020. Grid cells are modulated by local head direction. Nat. Commun. 11:4228
    [Google Scholar]
  59. Giocomo LM, Moser MB, Moser EI. 2011. Computational models of grid cells. Neuron 71:589–603
    [Google Scholar]
  60. Golob EJ, Stackman RW, Wong AC, Taube JS. 2001. On the behavioral significance of head direction cells: neural and behavioral dynamics during spatial memory tasks. Behav. Neurosci. 115:285–304
    [Google Scholar]
  61. Goodridge JP, Dudchenko PA, Worboys KA, Golob EJ, Taube JS. 1998. Cue control and head direction cells. Behav. Neurosci. 112:749–61
    [Google Scholar]
  62. 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]
  63. 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]
  64. Gorgiladze GI, Smirnov GD. 1967. [The effect of vestibular stimulation on the neuronal activity of the visual cortex of the cat brain]. Zh. Vyssh. Nerv. Deiat. Im. I. P. Pavlova 17:345–52 ( In Russian )
    [Google Scholar]
  65. 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]
  66. Grüsser OJ, Grüsser-Cornehls U. 1960. Mikroelektrodenuntersuchungen zur Konvergenz vestibulärer und retinaler Afferenzen an einzelnen Neuronen des optischen Cortex der Katze. Pflugers Arch. Ges. Physiol. 270:227–38
    [Google Scholar]
  67. Grüsser OJ, Grüsser-Cornehls U. 1972. Interaction of vestibular and visual inputs in the visual system. Prog. Brain Res. 37:573–83
    [Google Scholar]
  68. Grüsser OJ, Grüsser-Cornehls U, Saur G. 1959. Reaktionen einzelner Neurone im optischen Cortex der Katze nach elektrischer Polarisation des Labyrinths. Pflugers Arch. Ges. Physiol. 270:31–32
    [Google Scholar]
  69. Gu Y, Angelaki DE, Deangelis GC. 2008. Neural correlates of multisensory cue integration in macaque MSTd. Nat. Neurosci. 11:1201–10
    [Google Scholar]
  70. Guitchounts G, Lotter W, Dapello J, Cox D. 2022. Stable 3D head direction signals in the primary visual cortex. bioRxiv 2020.09.04.283762. https://doi.org/10.1101/2020.09.04.283762
    [Crossref]
  71. Guitchounts G, Masis J, Wolff SBE, Cox D. 2020. Encoding of 3D head orienting movements in the primary visual cortex. Neuron 108:512–25.e4
    [Google Scholar]
  72. Harland B, Grieves RM, Bett D, Stentiford R, Wood ER, Dudchenko PA. 2017. Lesions of the head direction cell system increase hippocampal place field repetition. Curr. Biol. 27:2706–12.e2
    [Google Scholar]
  73. Hennestad E, Witoelar A, Chambers AR, Vervaeke K. 2021. Mapping vestibular and visual contributions to angular head velocity tuning in the cortex. Cell Rep. 37:110134
    [Google Scholar]
  74. Hinman JR, Brandon MP, Climer JR, Chapman GW, Hasselmo ME. 2016. Multiple running speed signals in medial entorhinal cortex. Neuron 91:666–79
    [Google Scholar]
  75. Horn G, Hill RM. 1969. Modifications of receptive fields of cells in the visual cortex occurring spontaneously and associated with bodily tilt. Nature 221:186–88
    [Google Scholar]
  76. Horn G, Stechler G, Hill RM. 1972. Receptive fields of units in the visual cortex of the cat in the presence and absence of bodily tilt. Exp. Brain Res. 15:113–32
    [Google Scholar]
  77. Huang ZJ, Zeng H. 2013. Genetic approaches to neural circuits in the mouse. Annu. Rev. Neurosci. 36:183–215
    [Google Scholar]
  78. Hubel DH, Wiesel TN. 1968. Receptive fields and functional architecture of monkey striate cortex. J. Physiol. 195:215–43
    [Google Scholar]
  79. 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]
  80. Jacob PY, Poucet B, Liberge M, Save E, Sargolini F. 2014. Vestibular control of entorhinal cortex activity in spatial navigation. Front. Integr. Neurosci. 8:38
    [Google Scholar]
  81. Jankowski MM, Ronnqvist KC, Tsanov M, Vann SD, Wright NF et al. 2013. The anterior thalamus provides a subcortical circuit supporting memory and spatial navigation. Front. Syst. Neurosci. 7:45
    [Google Scholar]
  82. Jung R, Kornhuber HH, Da Fonseca JS. 1963. Multisensory convergence on cortical neurons neuronal effects of visual, acoustic and vestibular stimuli in the superior convolutions of the cat's cortex. Prog. Brain Res. 1:207–40
    [Google Scholar]
  83. Jurgens R, Becker W. 2006. Perception of angular displacement without landmarks: evidence for Bayesian fusion of vestibular, optokinetic, podokinesthetic, and cognitive information. Exp. Brain Res. 174:528–43
    [Google Scholar]
  84. Justus D, Dalugge D, Bothe S, Fuhrmann F, Hannes C et al. 2017. Glutamatergic synaptic integration of locomotion speed via septoentorhinal projections. Nat. Neurosci. 20:16–19
    [Google Scholar]
  85. Keller GB, Bonhoeffer T, Hubener M. 2012. Sensorimotor mismatch signals in primary visual cortex of the behaving mouse. Neuron 74:809–15
    [Google Scholar]
  86. Keller GB, Mrsic-Flogel TD. 2018. Predictive processing: a canonical cortical computation. Neuron 100:424–35
    [Google Scholar]
  87. Keshavarzi S, Bracey EF, Faville RA, Campagner D, Tyson AL et al. 2022. Multisensory coding of angular head velocity in the retrosplenial cortex. Neuron 110:532–43.e9
    [Google Scholar]
  88. Kim HR, Pitkow X, Angelaki DE, DeAngelis GC. 2016. A simple approach to ignoring irrelevant variables by population decoding based on multisensory neurons. J. Neurophysiol. 116:1449–67
    [Google Scholar]
  89. King WM, Lisberger SG, Fuchs AF. 1976. Responses of fibers in medial longitudinal fasciculus (MLF) of alert monkeys during horizontal and vertical conjugate eye movements evoked by vestibular or visual stimuli. J. Neurophysiol. 39:1135–49
    [Google Scholar]
  90. Klingner CM, Axer H, Brodoehl S, Witte OW. 2016. Vertigo and the processing of vestibular information: a review in the context of predictive coding. Neurosci. Biobehav. Rev. 71:379–87
    [Google Scholar]
  91. Klioutchnikov A, Wallace DJ, Frosz MH, Zeltner R, Sawinski J et al. 2020. Three-photon head-mounted microscope for imaging deep cortical layers in freely moving rats. Nat. Methods 17:509–13
    [Google Scholar]
  92. Klioutchnikov A, Wallace DJ, Sawinski J, Voit K-M, Groemping Y, Kerr JND. 2023. A three-photon head-mounted microscope for imaging all layers of visual cortex in freely moving mice. Nat. Methods 20:610–16
    [Google Scholar]
  93. Kropff E, Carmichael JE, Moser MB, Moser EI. 2015. Speed cells in the medial entorhinal cortex. Nature 523:419–24
    [Google Scholar]
  94. LaChance PA, Graham J, Shapiro BL, Morris AJ, Taube JS. 2022. Landmark-modulated directional coding in postrhinal cortex. Sci. Adv. 8:eabg8404
    [Google Scholar]
  95. 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]
  96. Leinweber M, Ward DR, Sobczak JM, Attinger A, Keller GB. 2017. A sensorimotor circuit in mouse cortex for visual flow predictions. Neuron 95:1420–32.e5
    [Google Scholar]
  97. Long X, Deng B, Young CK, Liu GL, Zhong Z et al. 2022. Sharp tuning of head direction and angular head velocity cells in the somatosensory cortex. Adv. Sci. 9:e2200020
    [Google Scholar]
  98. Lopez C, Blanke O. 2011. The thalamocortical vestibular system in animals and humans. Brain Res. Rev. 67:119–46
    [Google Scholar]
  99. Magnin M, Jeannerod M, Putkonen P. 1974. Vestibular and saccadic influences on dorsal and ventral nuclei of the lateral geniculate body. Exp. Brain Res. 21:1–18
    [Google Scholar]
  100. Magnin M, Kennedy H. 1979. Anatomical evidence of a third ascending vestibular pathway involving the ventral lateral geniculate nucleus and the intralaminar nuclei of the cat. Brain Res. 171:523–29
    [Google Scholar]
  101. Magnin M, Putkonen PT. 1978. A new vestibular thalamic area: electrophysiological study of the thalamic reticular nucleus and of the ventral lateral geniculate complex of the cat. Exp. Brain Res. 32:91–104
    [Google Scholar]
  102. Marlinski V, McCrea RA. 2008. Activity of ventroposterior thalamus neurons during rotation and translation in the horizontal plane in the alert squirrel monkey. J. Neurophysiol. 99:2533–45
    [Google Scholar]
  103. Matsuo S, Hosogai M, Nakao S. 1994. Ascending projections of posterior canal-activated excitatory and inhibitory secondary vestibular neurons to the mesodiencephalon in cats. Exp. Brain Res. 100:7–17
    [Google Scholar]
  104. McFarland WL, Teitelbaum H, Hedges EK. 1975. Relationship between hippocampal theta activity and running speed in the rat. J. Comp. Physiol. Psychol. 88:324–28
    [Google Scholar]
  105. McNaughton BL, Barnes CA, O'Keefe J. 1983. The contributions of position, direction, and velocity to single unit activity in the hippocampus of freely-moving rats. Exp. Brain Res. 52:41–49
    [Google Scholar]
  106. McNaughton BL, Battaglia FP, Jensen O, Moser EI, Moser MB. 2006. Path integration and the neural basis of the ‘cognitive map. ’. Nat. Rev. Neurosci. 7:663–78
    [Google Scholar]
  107. 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]
  108. Medrea I, Cullen KE. 2013. Multisensory integration in early vestibular processing in mice: the encoding of passive versus active motion. J. Neurophysiol. 110:2704–17
    [Google Scholar]
  109. Meng H, May PJ, Dickman JD, Angelaki DE. 2007. Vestibular signals in primate thalamus: properties and origins. J. Neurosci. 27:13590–602
    [Google Scholar]
  110. Metzler J, Spinelli DN. 1979. Tilt-constant receptive fields in the kitten visual cortex. Brain Res. 163:344–48
    [Google Scholar]
  111. Meyer AF, Poort J, O'Keefe J, Sahani M, Linden JF. 2018. A head-mounted camera system integrates detailed behavioral monitoring with multichannel electrophysiology in freely moving mice. Neuron 100:46–60.e7
    [Google Scholar]
  112. Michaiel AM, Abe ET, Niell CM. 2020. Dynamics of gaze control during prey capture in freely moving mice. eLife 9:e57458
    [Google Scholar]
  113. Miura SK, Scanziani M. 2022. Distinguishing externally from saccade-induced motion in visual cortex. Nature 610:135–42
    [Google Scholar]
  114. 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]
  115. Muir GM, Taube JS. 2004. Head direction cell activity and behavior in a navigation task requiring a cognitive mapping strategy. Behav. Brain Res. 153:249–53
    [Google Scholar]
  116. Nagata S. 1986. The vestibulothalamic connections in the rat: a morphological analysis using wheat germ agglutinin-horseradish peroxidase. Brain Res. 376:57–70
    [Google Scholar]
  117. Niell CM, Stryker MP. 2010. Modulation of visual responses by behavioral state in mouse visual cortex. Neuron 65:472–79
    [Google Scholar]
  118. Noel JP, Angelaki DE. 2022. Cognitive, systems, and computational neurosciences of the self in motion. Annu. Rev. Psychol. 73:103–29
    [Google Scholar]
  119. 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]
  120. Papaioannou JN. 1973. Effects of caloric labyrinthine stimulation on the spontaneous activity of lateral geniculate nucleus neurons in the cat. Exp. Brain Res. 17:1–9
    [Google Scholar]
  121. Parker PRL, Abe ETT, Leonard ESP, Martins DM, Niell CM. 2022a. Joint coding of visual input and eye/head position in V1 of freely moving mice. Neuron 110:3897–906.e5
    [Google Scholar]
  122. Parker PRL, Martins DM, Leonard ESP, Casey NM, Sharp SL et al. 2022b. A dynamic sequence of visual processing initiated by gaze shifts. bioRxiv 2022.08.23.504847. https://doi.org/10.1101/2022.08.23.504847
    [Crossref]
  123. Peck JR, Taube JS. 2017. The postrhinal cortex is not necessary for landmark control in rat head direction cells. Hippocampus 27:156–68
    [Google Scholar]
  124. Peréz-Escobar JA, Kornienko O, Latuske P, Kohler L, Allen K. 2016. Visual landmarks sharpen grid cell metric and confer context specificity to neurons of the medial entorhinal cortex. eLife 5:e16937
    [Google Scholar]
  125. Peyrache A, Schieferstein N, Buzsaki G. 2017. Transformation of the head-direction signal into a spatial code. Nat. Commun. 8:1752
    [Google Scholar]
  126. Prsa M, Gale S, Blanke O. 2012. Self-motion leads to mandatory cue fusion across sensory modalities. J. Neurophysiol. 108:2282–91
    [Google Scholar]
  127. Rancz EA, Franks KM, Schwarz MK, Pichler B, Schaefer AT, Margrie TW. 2011. Transfection via whole-cell recording in vivo: bridging single-cell physiology, genetics and connectomics. Nat. Neurosci. 14:527–32
    [Google Scholar]
  128. Rancz EA, Moya J, Drawitsch F, Brichta AM, Canals S, Margrie TW. 2015. Widespread vestibular activation of the rodent cortex. J. Neurosci. 35:5926–34
    [Google Scholar]
  129. Rao RP, Ballard DH. 1999. Predictive coding in the visual cortex: a functional interpretation of some extra-classical receptive-field effects. Nat. Neurosci. 2:79–87
    [Google Scholar]
  130. Rasmussen RN, Matsumoto A, Arvin S, Yonehara K 2021. Binocular integration of retinal motion information underlies optic flow processing by the cortex. Curr. Biol. 31:1165–74.e6
    [Google Scholar]
  131. Redish D, Elga AN, Touretzky DS. 1996. A coupled attractor model of the rodent head direction system. Comput. Neural Syst. 7:671–85
    [Google Scholar]
  132. Robertson RG, Rolls ET, Georges-François P, Panzeri S. 1999. Head direction cells in the primate pre-subiculum. Hippocampus 9:206–19
    [Google Scholar]
  133. Røe MB, Aasebo IEJ, Mobarhan M, Lensjo KK, Stober TM et al. 2018. Stable orientation tuning in the freely moving rat: movement-robust orientation selective neurons in the deep layers of the primary visual cortex Poster presented at the Society for Neuroscience Annual Meeting San Diego, CA: Novemb. 3–7
  134. Rummell BP, Klee JL, Sigurdsson T. 2016. Attenuation of responses to self-generated sounds in auditory cortical neurons. J. Neurosci. 36:12010–26
    [Google Scholar]
  135. Saleem AB, Diamanti EM, Fournier J, Harris KD, Carandini M. 2018. Coherent encoding of subjective spatial position in visual cortex and hippocampus. Nature 562:124–27
    [Google Scholar]
  136. Salinas E, Sejnowski TJ. 2001. Gain modulation in the central nervous system: where behavior, neurophysiology, and computation meet. Neuroscientist 7:430–40
    [Google Scholar]
  137. Sarel A, Finkelstein A, Las L, Ulanovsky N. 2017. Vectorial representation of spatial goals in the hippocampus of bats. Science 355:176–80
    [Google Scholar]
  138. Sargolini F, Fyhn M, Hafting T, McNaughton BL, Witter MP et al. 2006. Conjunctive representation of position, direction, and velocity in entorhinal cortex. Science 312:758–62
    [Google Scholar]
  139. Sasaki R, Angelaki DE, DeAngelis GC. 2017. Dissociation of self-motion and object motion by linear population decoding that approximates marginalization. J. Neurosci. 37:11204–19
    [Google Scholar]
  140. Sattler NJ, Wehr M. 2020. A head-mounted multi-camera system for electrophysiology and behavior in freely-moving mice. Front. Neurosci. 14:592417
    [Google Scholar]
  141. Schneider DM, Nelson A, Mooney R 2014. A synaptic and circuit basis for corollary discharge in the auditory cortex. Nature 513:189–94
    [Google Scholar]
  142. Seelig JD, Jayaraman V. 2015. Neural dynamics for landmark orientation and angular path integration. Nature 521:186–91
    [Google Scholar]
  143. Sharp PE, Tinkelman A, Cho J. 2001. 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]
  144. Sharp PE, Turner-Williams S. 2005. Movement-related correlates of single-cell activity in the medial mammillary nucleus of the rat during a pellet-chasing task. J. Neurophysiol. 94:1920–27
    [Google Scholar]
  145. Shinder ME, Taube JS. 2011. Active and passive movement are encoded equally by head direction cells in the anterodorsal thalamus. J. Neurophysiol. 106:788–800
    [Google Scholar]
  146. Shine JP, Valdes-Herrera JP, Hegarty M, Wolbers T. 2016. The human retrosplenial cortex and thalamus code head direction in a global reference frame. J. Neurosci. 36:6371–81
    [Google Scholar]
  147. Shiroyama T, Kayahara T, Yasui Y, Nomura J, Nakano K. 1999. Projections of the vestibular nuclei to the thalamus in the rat: a Phaseolus vulgaris leucoagglutinin study. J. Comp. Neurol. 407:318–32
    [Google Scholar]
  148. Sit KK, Goard MJ. 2022. Coregistration of heading to visual cues in retrosplenial cortex. bioRxiv 2022.03.25.485865. https://doi.org/10.1101/2022.03.25.485865
    [Crossref]
  149. 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]
  150. Spalla D, Treves A, Boccara CN. 2022. Angular and linear speed cells in the parahippocampal circuits. Nat. Commun. 13:1907
    [Google Scholar]
  151. Spiegel EA, Egyed J, Szekely EG. 1968. Cortical responses to rotation. II. Responses recorded at the onset of rotation from the second somatic sensory and posterior areas. Acta Otolaryngol. 66:261–72
    [Google Scholar]
  152. Spratling MW. 2010. Predictive coding as a model of response properties in cortical area V1. J. Neurosci. 30:3531–43
    [Google Scholar]
  153. Stackman RW, Golob EJ, Bassett JP, Taube JS. 2003. Passive transport disrupts directional path integration by rat head direction cells. J. Neurophysiol. 90:2862–74
    [Google Scholar]
  154. 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]
  155. Stahl JS. 2004. Using eye movements to assess brain function in mice. Vision Res. 44:3401–10
    [Google Scholar]
  156. Sugar J, Witter MP, van Strien NM, Cappaert NL. 2011. The retrosplenial cortex: intrinsic connectivity and connections with the (para)hippocampal region in the rat. An interactive connectome. Front. Neuroinform. 5:7
    [Google Scholar]
  157. Taube JS. 1995. Head direction cells recorded in the anterior thalamic nuclei of freely moving rats. J. Neurosci. 15:70–86
    [Google Scholar]
  158. Taube JS. 2007. The head direction signal: origins and sensory-motor integration. Ann. Rev. Neurosci. 30:181–207
    [Google Scholar]
  159. 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]
  160. 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]
  161. Thier P, Erickson RG. 1992. Responses of visual-tracking neurons from cortical area MST-I to visual, eye and head motion. Eur. J. Neurosci. 4:539–53
    [Google Scholar]
  162. Tiecks FP, Planck J, Haberl RL, Brandt T. 1996. Reduction in posterior cerebral artery blood flow velocity during caloric vestibular stimulation. J. Cereb. Blood Flow Metab. 16:1379–82
    [Google Scholar]
  163. Tomko DL, Barbaro NM, Ali FN. 1981. Effect of body tilt on receptive field orientation of simple visual cortical neurons in unanesthetized cats. Exp. Brain Res. 43:309–14
    [Google Scholar]
  164. Toyama K, Komatsu Y, Shibuki K. 1984. Integration of retinal and motor signals of eye movements in striate cortex cells of the alert cat. J. Neurophysiol. 51:649–65
    [Google Scholar]
  165. 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]
  166. Valerio S, Taube JS. 2012. Path integration: how the head direction signal maintains and corrects spatial orientation. Nat. Neurosci. 15:1445–53
    [Google Scholar]
  167. 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]
  168. van der Meer MAA, Richmond Z, Braga RM, Wood ER, Dudchenko PA. 2010. Evidence for the use of an internal sense of direction in homing. Behav. Neurosci. 124:164–69
    [Google Scholar]
  169. Vanni-Mercier G, Magnin M 1982. Single neuron activity related to natural vestibular stimulation in the cat's visual cortex. Exp. Brain Res. 45:451–55
    [Google Scholar]
  170. Velez-Fort M, Bracey EF, Keshavarzi S, Rousseau CV, Cossell L et al. 2018. A circuit for integration of head- and visual-motion signals in layer 6 of mouse primary visual cortex. Neuron 98:179–91.e6
    [Google Scholar]
  171. Velez-Fort M, Rousseau CV, Niedworok CJ, Wickersham IR, Rancz EA et al. 2014. The stimulus selectivity and connectivity of layer six principal cells reveals cortical microcircuits underlying visual processing. Neuron 83:1431–43
    [Google Scholar]
  172. Vinepinsky E, Cohen L, Perchik S, Ben-Shahar O, Donchin O, Segev R. 2020. Representation of edges, head direction, and swimming kinematics in the brain of freely-navigating fish. Sci. Rep. 10:14762
    [Google Scholar]
  173. Voigts J, Siegle JH, Pritchett DL, Moore CI. 2013. The flexDrive: an ultra-light implant for optical control and highly parallel chronic recording of neuronal ensembles in freely moving mice. Front. Syst. Neurosci. 7:8
    [Google Scholar]
  174. von Holst E, Mittelstaedt H. 1950. Das Reafferenzprinzip. Wechselwirkungen zwischen Zentralnervensystem und Peripherie. Naturwissenschaften 37:464–76
    [Google Scholar]
  175. Wallace DJ, Greenberg DS, Sawinski J, Rulla S, Notaro G, Kerr JN. 2013. Rats maintain an overhead binocular field at the expense of constant fusion. Nature 498:65–69
    [Google Scholar]
  176. Wenzel R, Bartenstein P, Dieterich M, Danek A, Weindl A et al. 1996. Deactivation of human visual cortex during involuntary ocular oscillations. A PET activation study. Brain 119:101–10
    [Google Scholar]
  177. Whitlock JR, Pfuhl G, Dagslott N, Moser MB, Moser EI. 2012. Functional split between parietal and entorhinal cortices in the rat. Neuron 73:789–802
    [Google Scholar]
  178. Wiener SI, Paul CA, Eichenbaum H. 1989. Spatial and behavioral correlates of hippocampal neuronal activity. J. Neurosci. 9:2737–63
    [Google Scholar]
  179. Winter SS, Clark BJ, Taube JS. 2015a. Disruption of the head direction cell network impairs the parahippocampal grid cell signal. Science 347:870–74
    [Google Scholar]
  180. Winter SS, Mehlman ML, Clark BJ, Taube JS. 2015b. Passive transport disrupts grid signals in the parahippocampal cortex. Curr. Biol. 25:2493–502
    [Google Scholar]
  181. Wyss JM, Van Groen T. 1992. Connections between the retrosplenial cortex and the hippocampal formation in the rat: a review. Hippocampus 2:1–11
    [Google Scholar]
  182. 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]
  183. 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]
  184. 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]
  185. Zong W, Obenhaus HA, Skytoen ER, Eneqvist H, de Jong NL et al. 2022. Large-scale two-photon calcium imaging in freely moving mice. Cell 185:1240–56.e30
    [Google Scholar]
  186. Zong W, Wu R, Li M, Hu Y, Li Y et al. 2017. Fast high-resolution miniature two-photon microscopy for brain imaging in freely behaving mice. Nat. Methods 14:713–19
    [Google Scholar]
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