Head Direction Cells: From Generation to Integration

Abstract

To maintain spatial orientation and guide navigation, an animal must have knowledge of its location and displacement of distance and direction from that location. Cells within the hippocampal formation and connected structures are spatially correlated to location and direction. Specifically, head direction (HD) cells discharge as a function of the directional heading of an animal, independent of their location or behavior. HD cells are found in many brain regions, but the classic circuit involved in generating, updating, and controlling their responses originates in the dorsal tegmental nucleus and projects serially to the lateral mammillary nucleus, anterior thalamic nuclei, and post- and parasubiculum and terminates in the entorhinal cortex. The HD signal is generated by self-movement cues, with the vestibular system playing a critical role. However, HD cells become strongly controlled by environmental cues, particularly visual landmarks. HD cells provide a continuous signal that an animal will use to guide its behavior and maintain orientation. Information provided by HD cells may be critical for generating the grid cell, but not for the place cell signal. Collectively, information from HD, place, and grid cells provide a complete representation of the animal’s orientation in space.

References

  1. Aguirre GK, D’Esposito M (1999) Topographical disorientation: a synthesis and taxonomy. Brain 122:1613–1628PubMedGoogle Scholar
  2. Allen GV, Hopkins DA (1989) Mammillary body in the rat: topography and synaptology of projections from the subicular complex, prefrontal cortex, and midbrain tegmentum. J Comp Neurol 286:311–336PubMedGoogle Scholar
  3. Alonso A, Garcia-Austt E (1987) Neuronal sources of theta rhythm in the entorhinal cortex of the rat. I. Laminar distribution of theta field potentials. Exp Brain Res 67:493–501PubMedGoogle Scholar
  4. Baker R, Berthoz A (1975) Is the prepositus hypoglossi nucleus the sources of another vestibule-ocular pathway? Brain Res 86:121–127PubMedGoogle Scholar
  5. Barry C, Burgess N (2007) Learning in a geometric model of place cell firing. Hippocampus 17:786–800PubMedGoogle Scholar
  6. Bassett JP, Taube JS (2001) Neural correlates for angular head velocity in the rat dorsal tegmental nucleus. J Neurosci 21:5740–5751PubMedGoogle Scholar
  7. 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 27:7564–7577PubMedGoogle Scholar
  8. Bett D, Wood ER, Dudchenko PA (2012) The postsubiculum is necessary for spatial alternation but not for homing by path integration. Behav Neurosci 126:237–248PubMedGoogle Scholar
  9. Biazoli CE, Goto M, Campos AM, Canteras NS (2006) The supragenual nucleus: a putative relay station for ascending vestibular signs to head direction cells. Brain Res 1094:138–148PubMedGoogle Scholar
  10. 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 21:1387–1397PubMedGoogle Scholar
  11. Blair HT, Cho J, Sharp PE (1999) The anterior thalamic head-direction signal is abolished by bilateral but not unilateral lesions of the lateral mammillary nucleus. J Neurosci 19:6673–6683PubMedGoogle Scholar
  12. Blanks RHI, Volkind R, Precht W, Baker R (1977) Responses of cat prepositus hypoglossi neurons to horizontal angular acceleration. Neuroscience 2:391–403PubMedGoogle Scholar
  13. Boccara CN, Sargolini F, Thoresen VH, Solstad T, Witter MP, Moser EI, Moser M-B (2010) Grid cells in pre- and parasubiculum. Nat Neurosci 13:987–994PubMedGoogle Scholar
  14. Brandon MP, Bogaard AR, Libby CP, Connerney KG, Hasselmo ME (2011) Reduction of theta rhythm dissociates grid cell spatial periodicity from directional tuning. Science 332:595–599PubMedCentralPubMedGoogle Scholar
  15. Burak Y, Fiete IR (2009) Accurate path integration in continuous attractor network models of grid cells. PLoS Comput Biol 5:e1000291PubMedCentralPubMedGoogle Scholar
  16. Burgess N, O’Keefe J (2011) Models of place and grid cell firing and theta rhythmicity. Curr Opin Neurobiol 21:734–744PubMedCentralPubMedGoogle Scholar
  17. Burgess N, Barry C, O’Keefe J (2007) An oscillatory interference model of grid cell firing. Hippocampus 17:801–812PubMedCentralPubMedGoogle Scholar
  18. Butler WN, Taube JS (2012) The nucleus prepositus contributes to head direction cell stability in rats. Soc Neurosci Abstr 920:13Google Scholar
  19. 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 23:9719–9731PubMedGoogle Scholar
  20. Chen LL, Lin LH, Barnes CA, McNaughton BL (1994a) Head-direction cells in the rat posterior cortex. II. Contributions of visual and ideothetic information to the directional firing. Exp Brain Res 191:24–34Google Scholar
  21. Chen LL, Lin LH, Green EJ, Barnes CA, McNaughton BL (1994b) Head direction cells in the rat posterior cortex. I. Anatomical distribution and behavioral modulation. Exp Brain Res 191:8–23Google Scholar
  22. Cheng K (1986) A purely geometric module in the rat’s spatial representation. Cognition 23:149–178PubMedGoogle Scholar
  23. Cho J, Sharp PE (2001) Head direction, place, and movement correlates for cells in the rat retrosplenial cortex. Behav Neurosci 115:3–25PubMedGoogle Scholar
  24. Clark BJ, Taube JS (2011) Intact landmark control and angular path integration by head direction cells in the anterodorsal thalamus after lesions of the medial entorhinal cortex. Hippocampus 21:767–782PubMedGoogle Scholar
  25. Clark BJ, Sarma A, Taube JS (2009) Head direction cell instability in the anterior dorsal thalamus after lesions of the interpeduncular nucleus. J Neurosci 29:493–507PubMedCentralPubMedGoogle Scholar
  26. 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 30:5289–5302PubMedCentralPubMedGoogle Scholar
  27. Clark BJ, Valerio S, Taube JS (2011) Disrupted grid and head direction cell signal in the entorhinal cortex and parasubiculum after lesions of the head direction system. Soc Neurosci Abstr 729:11Google Scholar
  28. Clark BJ, Brown JE, Taube JS (2012) Head direction cell activity in the anterodorsal thalamus requires intact supragenual nuclei. J Neurophysiol 108:2767–2784PubMedCentralPubMedGoogle Scholar
  29. Contestabile A, Flumerfelt BA (1981) Afferent connections of the interpeduncular nucleus and the topographic organization of the habenulo-interpeduncular pathway: an HRP study in the rat. J Comp Neurol 196:253–270PubMedGoogle Scholar
  30. Derdikman D, Moser EI (2014) Spatial maps in the entorhinal cortex and adjacent structures. In: Derdikman D, Knierim JJ (eds) Space, time and memory in the hippocampal formation. Springer, HeidelbergGoogle Scholar
  31. Dudchenko PA, Taube JS (1997) Correlation between head direction cell activity and spatial behavior on a radial arm maze. Behav Neurosci 111:3–19PubMedGoogle Scholar
  32. Eilam D, Golani I (1989) Home base behavior of rats (Rattus norvegicus) exploring a novel environment. Behav Brain Res 34:199–211PubMedGoogle Scholar
  33. Frank LM, Brown EN, Wilson M (2000) Trajectory encoding in the hippocampus and entorhinal cortex. Neuron 27:169–178PubMedGoogle Scholar
  34. Frohardt RJ, Bassett JP, Taube JS (2006) Path integration and lesions within the head direction cell circuit: comparison between the roles of the anterodorsal thalamus and dorsal tegmental nucleus. Behav Neurosci 120:135–149PubMedGoogle Scholar
  35. Fyhn M, Molden S, Witter MP, Moser EI, Moser M-B (2004) Spatial representation in the entorhinal cortex. Science 305:1258–1264PubMedGoogle Scholar
  36. Gallistel CR (1990) The organization of learning. MIT Press, Cambridge, MAGoogle Scholar
  37. Goldberg JM, Farnandez C (1975) Vestibular mechanisms. Annu Rev Physiol 37:129–162PubMedGoogle Scholar
  38. Golob EJ, Taube JS (1997) Head direction cells and episodic spatial information in rats without a hippocampus. Proc Natl Acad Sci U S A 94:7645–7650PubMedCentralPubMedGoogle Scholar
  39. Golob EJ, Wolk DA, Taube JS (1998) Recordings of postsubiculum head direction cells following lesions of the laterodorsal thalamic nucleus. Brain Res 780:9–19PubMedGoogle Scholar
  40. Goodridge JP, Taube JS (1997) Interaction between the postsubiculum and anterior thalamus in the generation of head direction cell activity. J Neurosci 17:9315–9330PubMedGoogle Scholar
  41. Goodridge JP, Dudchenko PA, Worboys KA, Golob EJ, Taube JS (1998) Cue control and head direction cells. Behav Neurosci 112:749–761PubMedGoogle Scholar
  42. Groenewegen HJ, Ahlenius S, Haber SN, Kowall NW, Nauta WJH (1986) Cytoarchitecture, fiber connections, and some histochemical aspects of the interpeduncular nucleus in the rat. J Comp Neurol 249:65–102PubMedGoogle Scholar
  43. Hafting T, Fyhn M, Molden S, Moser M-B, Moser EI (2005) Microstructure of a spatial map in the entorhinal cortex. Nature 436:801–806PubMedGoogle Scholar
  44. Hasselmo ME, Brandon MP (2008) Linking cellular mechanisms to behavior: entorhinal persistent spiking and membrane potential oscillations may underlie path integration, grid cell firing, and episodic memory. Neural Plast 2008:658323PubMedCentralPubMedGoogle Scholar
  45. Hasselmo ME, Brandon MP (2012) A model combining oscillations and attractor dynamics for generation of grid firing. Front Neural Circuits 6:30PubMedCentralPubMedGoogle Scholar
  46. Hayakawa T, Zyo K (1984) Comparative anatomical study of the tegmentomammillary projections in some mammals: a horseradish peroxidase study. Brain Res 300:335–349PubMedGoogle Scholar
  47. Hayakawa T, Zyo K (1985) Afferent connections of Gudden’s tegmental nuclei in the rabbit. J Comp Neurol 235:169–181PubMedGoogle Scholar
  48. Iwasaki H, Kani K, Maeda T (1999) Neural connections of the pontine reticular formation, which connects reciprocally with the nucleus prepositus hypoglossi in the rat. Neuroscience 93:195–208PubMedGoogle Scholar
  49. Jeffery KJ (2011) Place cells, grid cells, attractors, and remapping. Neural Plast 2011:182602PubMedCentralPubMedGoogle Scholar
  50. Jeffery KJ, Donnett JG, Burgess N, O’Keefe JM (1997) Directional control of hippocampal place fields. Exp Brain Res 117:131–142PubMedGoogle Scholar
  51. Knierim JJ, Kudrimoti HS, McNaughton BL (1995) Place cells, head direction cells, and the learning of landmark stability. J Neurosci 15:1648–1659PubMedGoogle Scholar
  52. Knierim JJ, Kudrimoti HS, McNaughton BL (1998) Interactions between idiothetic cues and external landmarks in the control of place cells and head direction cells. J Neurophysiol 80:425–446PubMedGoogle Scholar
  53. Koenig J, Linder AN, Leutgeb JK, Leutgeb S (2011) The spatial periodicity of grid cells is not sustained during reduced theta oscillations. Science 332:592–595PubMedGoogle Scholar
  54. Lannou J, Cazin L, Precht W, Le Taillanter M (1984) Responses of prepositus hypoglossi neurons to optokinetic and vestibular stimulations in the rats. Brain Res 301:39–45PubMedGoogle Scholar
  55. Leigh R, Zee DS (1999) The neurology of eye movements. Oxford University Press, New York, NYGoogle Scholar
  56. Leutgeb S, Ragozzino KE, Mizumori SJ (2000) Convergence of head direction and place information in the CA1 region of hippocampus. Neuroscience 100:11–19PubMedGoogle Scholar
  57. Liu R, Chang L, Wickern G (1984) The dorsal tegmental nucleus: an axoplasmic transport study. Brain Res 310:123–132PubMedGoogle Scholar
  58. McCrea RA, Baker R (1985) Anatomical connections of the nucleus prepositus of the cat. J Comp Neurol 237:377–407PubMedGoogle Scholar
  59. McKinney M, Coyle JT, Hedreen JC (1983) Topographic analysis of the innervation of the rat neocortex and hippocampus by the basal forebrain cholinergic system. J Comp Neurol 217:103–121PubMedGoogle Scholar
  60. Mitchell SJ, Ranck JB (1980) Generation of theta rhythm in medial entorhinal cortex of freely moving rats. Brain Res 189:49–66PubMedGoogle Scholar
  61. Mitchell SJ, Rawlins JNP, Steward O, Olton DS (1982) Medial septal area lesions disrupt θ rhythm and cholinergic staining in medial entorhinal cortex and produce impaired radial arm maze behavior in rats. J Neurosci 2:292–302PubMedGoogle Scholar
  62. Mizumori SJ, Williams JD (1993) Directionally selective mnemonic properties of neurons in the lateral dorsal nucleus of the thalamus of rats. J Neurosci 13:4015–4028PubMedGoogle Scholar
  63. Mizumori SJ, Ragozzino KE, Cooper BG (2000) Location and head direction representation in the dorsal striatum of rats. Psychobiology 28:441–462Google Scholar
  64. Mizumori SJ, Puryear CB, Gill KM, Guazzelli A (2005) Head direction cells in hippocampal afferent and efferent systems: what functions do they serve? In: Wiener SI, Taube JS (eds) Head direction cells and the neural mechanisms of spatial orientation. MIT Press, Cambridge, MA, pp 203–220Google Scholar
  65. Moser EI, Moser MB (2008) A metric for space. Hippocampus 18:1142–1156PubMedGoogle Scholar
  66. Moser EI, Kropff E, Moser MB (2008) Place cells, grid cells, and the brain’s spatial representation system. Annu Rev Neurosci 31:69–89PubMedGoogle Scholar
  67. Muir GM, Taube JS (2004) Head direction cell activity and behavior in a navigation task requiring a cognitive mapping strategy. Behav Brain Res 153:249–253PubMedGoogle Scholar
  68. Muir GM, Brown JE, Carey JP, Hirvonen TP, Della Santina CC, Minor LB, Taube JS (2009) Disruption of the head direction cell signal after occlusion of the semicircular canals in the freely moving chinchilla. J Neurosci 29(46):14521–14533PubMedCentralPubMedGoogle Scholar
  69. Navratilova Z, McNaughton BL (2014) Models of path integration in the hippocampal complex. In: Derdikman D, Knierim JJ (eds) Space, time and memory in the hippocampal formation. Springer, HeidelbergGoogle Scholar
  70. O’Keefe J (1976) Place units in the hippocampus of the freely moving rat. Exp Neurol 51:78–109PubMedGoogle Scholar
  71. O’Keefe J, Dostrovsky J (1971) The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res 34:171–175PubMedGoogle Scholar
  72. O’Keefe J, Nadal L (1978) The hippocampus as a cognitive map. Clarendon, OxfordGoogle Scholar
  73. Parron C, Save E (2004) Evidence for entorhinal and parietal cortices involvement in path integration in the rat. Exp Brain Res 159:349–359PubMedGoogle Scholar
  74. Quirk GJ, Muller RU, Kubie JL, Ranck JB (1992) The positional firing properties of medial entorhinal neurons: description and comparison with hippocampal place cells. J Neurosci 12:1945–1963PubMedGoogle Scholar
  75. Ranck JB (1984) Head direction cells in the deep layer of dorsal presubiculum in freely moving rats. Soc Neurosci Abstr 10:599Google Scholar
  76. Redish AD, Elga AN, Touretzky DS (1996) A coupled attractor model of the rodent head direction system. Network 7:671–685Google Scholar
  77. Sargolini F, Fyhn M, Hafting T, McNaughton BL, Witter MP, Moser M-B, Moser EI (2006) Conjunctive representation of position, direction, and velocity in entorhinal cortex. Science 312:758–762PubMedGoogle Scholar
  78. Seki M, Zyo K (1984) Anterior thalamic afferents from the mammillary body and limbic cortex in the rat. J Comp Neurol 229:242–256PubMedGoogle Scholar
  79. Shapiro ML, Tanila H, Eichenbaum H (1997) Cues that hippocampal place cells encode: dynamic and hierarchical representation of local and distal stimuli. Hippocampus 7:624–642PubMedGoogle Scholar
  80. Sharp PE, Green C (1994) Spatial correlates of firing patterns of single cells in the subiculum of the freely moving rat. J Neurosci 14:2339–2358PubMedGoogle Scholar
  81. Sharp PE, Koester K (2008) Lesions of the mammillary body region severely disrupt the cortical head direction, but not place cell signal. Hippocampus 18:766–784PubMedGoogle Scholar
  82. 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 115:571–588PubMedGoogle Scholar
  83. Sharp PE, Turner-Williams S, Tuttle S (2006) Movement-related correlates of single cell activity in the interpeduncular nucleus and habenula of the rat during a pellet-chasing task. Behav Brain Res 166:55–70PubMedGoogle Scholar
  84. Shibata H (1993) Direct projections from the anterior thalamic nuclei to the retrohippocampal region in the rat. J Comp Neurol 337:431–445PubMedGoogle Scholar
  85. Shinder ME, Taube JS (2011) Active and passive movement are encoded equally by head direction cells in the anterodorsal thalamus. J Neurophysiol 106:788–800PubMedCentralPubMedGoogle Scholar
  86. Skaggs WE, Knierim JJ, Kudrimoti HS, McNaughton BL (1995) A model of the neural basis of the rat’s sense of direction. In: Tesauro G, Touretzky DS, Leen TK (eds) Advances in neural information processing systems, vol 7. MIT Press, Cambridge, MA, pp 173–180Google Scholar
  87. Solstad T, Boccara CN, Kropff E, Moser M-B, Moser EI (2008) Representation of geometric borders in the entorhinal cortex. Science 322:1865–1868PubMedGoogle Scholar
  88. Song P, Wang X-J (2005) Angular path integration by moving “hill of activity”: a spiking neuron model without recurrent excitation of the head-direction system. J Neurosci 25:1002–1014PubMedGoogle Scholar
  89. Souman JL, Frissen I, Sreenivasa MN, Ernst MO (2009) Walking straight into circles. Curr Biol 19:1538–1542PubMedGoogle Scholar
  90. Stackman RW, Taube JS (1997) Firing properties of head direction cells in the rat anterior thalamic nucleus: dependence on vestibular input. J Neurosci 17:4349–4358PubMedCentralPubMedGoogle Scholar
  91. Stackman RW, Taube JS (1998) Firing properties of rat lateral mammillary single units: head direction, head pitch, and angular head velocity. J Neurosci 18:9020–9037PubMedCentralPubMedGoogle Scholar
  92. Stackman RW, Clark AS, Taube JS (2002) Hippocampal spatial representations require vestibule input. Hippocampus 12:291–303PubMedCentralPubMedGoogle Scholar
  93. Tanila H, Shapiro ML, Eichenbaum H (1997) Discordance of spatial representation in ensembles of hippocampal place cells. Hippocampus 7:613–623PubMedGoogle Scholar
  94. Taube JS (1995) Head direction cells recorded in the anterior thalamic nuclei of freely moving rats. J Neurosci 15:70–86PubMedGoogle Scholar
  95. Taube JS (2007) The head direction signal: origins and sensory-motor integration. Annu Rev Neurosci 30:181–207PubMedGoogle Scholar
  96. Taube JS, Burton HL (1995) Head direction cell activity monitored in a novel environment and during a cue conflict situation. J Neurophysiol 74:1953–1971PubMedGoogle Scholar
  97. Taube JS, Valerio S (2012) Head direction cell activity is absent in mice without horizontal semicircular canals. Soc Neurosci Abstr 265:15Google Scholar
  98. 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 10:420–435PubMedGoogle Scholar
  99. 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 10:436–447PubMedGoogle Scholar
  100. Tsanov M, Chah E, Vann SD, Reilly RB, Erichsen JT, Aggleton JP, O’Mara SM (2011) Theta-modulated head direction cells in the rat anterior thalamus. J Neurosci 31:9489–9502PubMedGoogle Scholar
  101. Uchino Y, Sasaki M, Sato H, Bai R, Kawamoto E (2005) Otolith and canal integration on single vestibular neurons in cats. Exp Brain Res 164:271–285PubMedGoogle Scholar
  102. Valerio S, Taube JS (2012) Path integration: how the head direction signal maintains and corrects spatial orientation. Nat Neurosci 15:1445–1453PubMedCentralPubMedGoogle Scholar
  103. van der Kooy D, Carter DA (1981) The organization of the efferent projections and striatal afferents of the entopeduncular nucleus and adjacent areas in the rat. Brain Res 211:15–36PubMedGoogle Scholar
  104. van der Meer MA, Richmond A, Braga RM, Wood ER, Dudchenko PA (2010) Evidence for the use of an internal sense of direction in homing. Behav Neurosci 124:164–169PubMedGoogle Scholar
  105. van Groen T, Wyss JM (1990a) The postsubicular cortex in the rat: characterization of the fourth region of the subicular cortex and its connections. Brain Res 529:165–177PubMedGoogle Scholar
  106. van Groen T, Wyss JM (1990b) The connections of the presubiculum and parasubiculum in the rat. Brain Res 518:227–243PubMedGoogle Scholar
  107. van Groen T, Wyss JM (1992) Connections of the retrosplenial dysgranular cortex in the rat. J Comp Neurol 315:200–216PubMedGoogle Scholar
  108. van Groen T, Wyss JM (1995) Projections from the anterodorsal and anteroventral nucleus of the thalamus to the limbic cortex in the rat. J Comp Neurol 358:584–604PubMedGoogle Scholar
  109. Vogt BA, Miller MW (1983) Cortical connections between rat cingulate cortex and visual, motor, and postsubicular cortices. J Comp Neurol 216:192–210PubMedGoogle Scholar
  110. Wallace DG, Hines DJ, Pellis SM, Whishaw IQ (2002) Vestibular information is required for dead reckoning in the rat. J Neurosci 22:10009–10017PubMedGoogle Scholar
  111. Wallace DG, Hamilton DA, Whishaw IQ (2006) Movement characteristics support a role for dead reckoning in organizing exploratory behavior. Anim Cogn 9:219–228PubMedGoogle Scholar
  112. Whishaw IQ, Maaswinkel H, Gonzalez CL, Kolb B (2001) Deficits in allothetic and idiothetic spatial behavior in rats with posterior cingulate cortex lesions. Behav Brain Res 118:67–76PubMedGoogle Scholar
  113. Whitlock JR, Derdikman D (2012) Head direction maps remain stable despite grid map fragmentation. Front Neural Circuits 6:1–10Google Scholar
  114. Wiener SI (1993) Spatial and behavioral correlates of striatal neurons in rats performing a self-initiated navigation task. J Neurosci 13:3802–3817PubMedGoogle Scholar
  115. Wiener SI, Taube JS (2005) Head direction cells and the neural mechanisms of spatial orientation. MIT Press, Cambridge, MAGoogle Scholar
  116. Winter SS, Wagner SJ, McMillin JL, Wallace DG (2011) Mammillothalamic tract lesions disrupt dead reckoning in the rat. Eur J Neurosci 33:371–381PubMedGoogle Scholar
  117. Winter SS, Valerio S, Taube JS (2012) Excitotoxic lesions of striatum spare head direction cell function within the anterodorsal thalamus. Soc Neurosci Abstr 920:12Google Scholar
  118. Winter SS, Koppen JR, Ebert TBN, Wallace DG (2013) Limbic system structures differentially contribute to exploratory trip organization of the rat. Hippocampus 23:139–152PubMedGoogle Scholar
  119. Woolf NJ, Eckenstein F, Butcher LL (1984) Cholinergic systems in the rat brain: I. Projections to the limbic telencephalon. Brain Res Bull 13:751–784PubMedGoogle Scholar
  120. Yoder RM, Taube JS (2008) The postsubiculum provides visual landmark control to the head direction signal at the lateral mammillary nuclei. Soc Neurosci Abstr 90:9Google Scholar
  121. Yoder RM, Taube JS (2009) Head direction cell activity in mice: robust directional signal depends on intact otolith organs. J Neurosci 29:1061–1076PubMedCentralPubMedGoogle Scholar
  122. Yoder RM, Clark BJ, Brown JE, Lamia MV, Valerio S, Shinder ME, Taube JS (2011a) Both visual and idiothetic cues contribute to head direction cell stability during navigation along complex routes. J Neurophysiol 105:2989–3001PubMedCentralPubMedGoogle Scholar
  123. Yoder RM, Clark BJ, Taube JS (2011b) Origins of landmark encoding in the brain. Trends Neurosci 34:561–571PubMedCentralPubMedGoogle Scholar
  124. Yoganarasimha D, Yu X, Knierim JJ (2006) Head direction cell representations maintain internal coherence during conflicting proximal and distal cue rotations: comparison with hippocampal place cells. J Neurosci 26:622–631PubMedCentralPubMedGoogle Scholar
  125. Zhang K (1996) Representation of spatial orientation by the intrinsic dynamics of the head-direction cell ensemble: a theory. J Neurosci 16:2112–2126PubMedGoogle Scholar
  126. Zheng Y, Darlington CL, Smith PF (2006) Impairment and recovery on a food foraging task following unilateral vestibular deafferentation in rats. Hippocampus 16:368–378PubMedGoogle Scholar
  127. Zheng Y, Goddard M, Darlington CL, Smith PF (2009) Long-term deficits on a foraging task after bilateral vestibular deafferentation in rats. Hippocampus 19:480–486PubMedGoogle Scholar
  128. Zugaro MB, Berthoz A, Wiener SI (2001) Background, but not foreground, spatial cues are taken as references for head direction responses by rat anterodorsal thalamus neurons. J Neurosci 21:RC154PubMedGoogle Scholar
  129. Zugaro MB, Arleo A, Berthoz A, Wiener SI (2003) Rapid spatial reorientation and head direction cells. J Neurosci 23:3478–3482PubMedGoogle Scholar

Copyright information

© Springer-Verlag Wien 2014

Authors and Affiliations

  1. 1.Department of Psychological and Brain SciencesDartmouth CollegeHanoverUSA

Personalised recommendations