Neural Representations Supporting Spatial Navigation and Memory

  • Joel E. Brown
  • Jeffrey S. Taube


Neural representations of spatial information are substrates for behaviors that range from simple limb movements and basic locomotion to sophisticated navigation through complex environments. The processing of different types of spatial information, including the storage and recall of related neural representations, is integral to the ability to navigate through and interact with the external environment. Finding food, shelter, and potential mates requires an animal to develop an understanding of the spatial relationships between itself and numerous objects and goals within its environment. Two forms of information necessary for spatial navigation are the knowledge of one’s location within an environment and directional heading, or orientation. This information is represented by neural activity distributed over several nuclei within the limbic system and neocortex. Furthermore, the ability to integrate, store, and recall these representations is essential for long-term survival strategies. This chapter discusses the neural representations of spatial location and orientation and how they can contribute to a spatial memory system.


Entorhinal Cortex Place Cell Head Direction Spatial Navigation Head Direction Cell 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Alyan S, McNaughton BL (1999) Hippocampectomized rats are capable of homing by path integration. Hippocampus 113:19–31Google Scholar
  2. Anderson MI, Jeffery KJ (2003) Heterogeneous modulation of place cell firing by changes in context. J Neurosci 23:8827–8835PubMedGoogle Scholar
  3. Barnes CA, McNaughton BL, Mizumori SJ, Leonard BW, Lin LH (1990) Comparison of spatial and temporal characteristics of neuronal activity in sequential stages of hippocampal processing. Prog Brain Res 83:287–300PubMedCrossRefGoogle Scholar
  4. Bassett JP, Taube JS (2001) Neural correlates for angular head velocity in the rat dorsal tegmental nucleus. J Neurosci 21:5740–5751PubMedGoogle Scholar
  5. Bassett JP, Tullman ML, Taube JS (2007) Lesions of the tegmento-mammilliary circuit in the head direction system disrupts the direction signal in the anterior thamus. J Neurosci (in press)Google Scholar
  6. Bassett JP, Zugaro MB, Muir GM, Golob EJ, Muller RU, Taube JS (2005) Passive movements of the head do not abolish anticipatory firing properties of head direction cells. J Neurophysiol 93:1304–1316PubMedCrossRefGoogle Scholar
  7. Battaglia FP, Sutherland GR, McNaughton BL (2004) Local sensory cues and place cell directionality: additional evidence of prospective coding in the hippocampus. J Neurosci 24:4541–4550PubMedCrossRefGoogle Scholar
  8. Biazoli CE Jr, Goto M, Campos AM, Canteras NS (2006) The supragenual nucleus: a putative relay station for ascending vestibular signs to head direction cells. Brain Res 1094:138–148PubMedCrossRefGoogle Scholar
  9. 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 15:6260–6270PubMedGoogle Scholar
  10. Blair HT, Sharp PE (1996) Visual and vestibular influences on head-direction cells in the anterior thalamus of the rat. Behav Neurosci 110:643–660PubMedCrossRefGoogle Scholar
  11. Blair HT, Cho J, Sharp PE (1998) Role of the lateral mammillary nucleus in the rat head direction circuit: a combined single-unit recording and lesion study. Neuron 21:1387–1397PubMedCrossRefGoogle Scholar
  12. Bower MR, Euston DR, McNaughton BL (2005) Sequential-context-dependent hippocampal activity is not necessary to learn sequences with repeated elements. J Neurosci 25:1313–1323PubMedCrossRefGoogle Scholar
  13. Brazhnik ES, Muller RU, Fox SE (2003) Muscarinic blockade slows and degrades the location-specific firing of hippocampal pyramidal cells. J Neurosci 23:611–621PubMedGoogle Scholar
  14. Breese CR, Hampson RE, Deadwyler SA (1989) Hippocampal place cells: stereotypy and plasticity. J Neurosci 9:1097–1111PubMedGoogle Scholar
  15. Brown JE, Skaggs WE (2002) Concordant and discordant coding of spatial location in populations of hippocampal CA1 pyramidal cells. J Neurophysiol 88: 1605–1613.PubMedGoogle Scholar
  16. Brown JE, Yates BJ, Taube JS (2002) Does the vestibular system contribute to head direction cell activity in the rat? Physiol Behav 77:743–748PubMedCrossRefGoogle Scholar
  17. Brown JE, Card JP, Yates BJ (2005a) Polysynaptic pathways from the vestibular nuclei to the lateral mammillary nucleus in the rat: substrates for vestibular input to head direction cells. Exp Brain Res 161:47–61PubMedCrossRefGoogle Scholar
  18. Brown JE, Lamia MV, Taube JS (2005b) Head direction cell responses in a novel 14-choice T-maze. Program No. 198.15. 2005 Abstract Viewer/Itinerary Planner, Society for Neuroscience, Washington, DC (online)Google Scholar
  19. Brun VH, Otnass MK, Molden S, Steffenach HA, Witter MP, Moser MB, Moser EI (2002) Place cells and place recognition maintained by direct entorhinal-hippocampal circuitry. Science 296:2243–2246PubMedCrossRefGoogle Scholar
  20. Burgess N, Maguire EA, O’Keefe J (2002) The human hippocampus and spatial and episodic memory. Neuron 35:625–641PubMedCrossRefGoogle Scholar
  21. Burwell RD, Hafeman DM (2003) Positional firing properties of postrhinal cortex neurons. Neuroscience 119:577–588PubMedCrossRefGoogle Scholar
  22. Buzsaki G (2004) Large-scale recordings of neuronal ensembles. Nat Neurosci 7:446–451PubMedCrossRefGoogle Scholar
  23. Buzsaki G (2005) Theta rhythm of navigation: link between path integration and landmark navigation, episodic and semantic memory. Hippocampus 15:827–840PubMedCrossRefGoogle Scholar
  24. Cacucci F, Lever C, Wills TJ, Burgess N, O’Keefe J (2004) Theta-modulated place-bydirection cells in the hippocampal formation in the rat. J Neurosci 24:8265–8277PubMedCrossRefGoogle Scholar
  25. Calton JL, Taube JS (2001) Head direction cell activity following bilateral lesions of posterior parietal cortex. Soc Neurosci Abstr 27:537.30Google Scholar
  26. Calton JL, Taube JS (2005) Degradation of head direction cell activity during inverted locomotion. J Neurosci 25:2420–2428PubMedCrossRefGoogle Scholar
  27. 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
  28. 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 101:8–23PubMedCrossRefGoogle Scholar
  29. Cho J, Sharp PE (2001) Head direction, place, and movement correlates for cells in the rat retrosplenial cortex. Behav Neurosci 115:3–25PubMedCrossRefGoogle Scholar
  30. Colby CL, Duhamel JR (1996) Spatial representations for action in parietal cortex. Brain Res Cognit Brain Res 5:105–115CrossRefGoogle Scholar
  31. Cooper BG, Mizumori SY (2001) Temporary inactivation of the retrosplenial cortex causes a transient reorganization of spatial coding in the hippocampus. J Neurosci 21:3986–4001PubMedGoogle Scholar
  32. Dragoi G, Buzsaki G (2006) Temporal encoding of place sequences by hippocampal cell assemblies. Neuron 50:145–157PubMedCrossRefGoogle Scholar
  33. Dudchenko PA, Taube JS (1997) Correlation between head direction cell activity and spatial behavior on a radial arm maze. Behav Neurosci 111:3–19PubMedCrossRefGoogle Scholar
  34. Eichenbaum H, Dudchenko PA, Wood E, Shapiro M, Tanila H (1999) The hippocampus, memory, and place cells: is it spatial memory or memory space? Neuron 23:209–226PubMedCrossRefGoogle Scholar
  35. Ekstrom AD, Kahana MJ, Caplan JB, Field TA, Isham EA, Newman EL, Fried I (2003) Cellular networks underlying human spatial navigation. Nature (Lond) 425:184–188PubMedCrossRefGoogle Scholar
  36. Fenton AA, Muller RU (1998) Place cell discharge is extremely variable during individual passes of the rat through the firing field. Proc Natl Acad Sci U S A 95:3182–3187PubMedCrossRefGoogle Scholar
  37. Ferbinteanu J, Shapiro MK (2003) Prospective and retrospective memory coding in the hippocampus. Neuron 40:1227–1239PubMedCrossRefGoogle Scholar
  38. Fortin NJ, Agster KL, Eichenbaum (2002) Critical role of the hippocampus in memory for sequences of events. Nat Neurosci 5:458–462PubMedGoogle Scholar
  39. Foster DJ, Wilson MA (2006) Reverse replay of behavioral sequences in hippocampal place cells during the awake state. Nature (Lond) 440:680–683PubMedCrossRefGoogle Scholar
  40. Frank LM, Brown EN, Wilson M (2000) Trajectory encoding in the hippocampus and entorhinal cortex. Neuron 27:169–178PubMedCrossRefGoogle Scholar
  41. Frohardt RJ, Basset 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 130:135–149CrossRefGoogle Scholar
  42. Fyhn M, Molden S, Willter MP, Moser EI, Moser MB (2004) Spatial representations in the entorhinal cortex. Science 305:1258–1264PubMedCrossRefGoogle Scholar
  43. Gallistel CR (1990) The organization of learning. MIT Press, CambridgeGoogle Scholar
  44. Golob EJ, Taube JS (1997) Head direction cells and episodic spatial information in rats without a hippocampus. Proc Natl Acad Sci U S A 94:7645–7650PubMedCrossRefGoogle Scholar
  45. Golob EJ, Taube JS (1999) Head direction cells in rats with hippocampal or overlying neocortical lesions: evidence for impaired angular path integration. J Neurosci 19:7198–7211PubMedGoogle Scholar
  46. Golob EJ, Wolk DA, Taube JS (1998) Recordings of postsubiculum head direction cells following lesions of the laterodorsal thalamic nucleus. Brain Res 780:9–19PubMedCrossRefGoogle Scholar
  47. 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 115:285–304PubMedCrossRefGoogle Scholar
  48. Goodridge JP, Taube JS (1995) Preferential use of the landmark navigational system by head direction cells. Behav Neurosci 109:49–61PubMedCrossRefGoogle Scholar
  49. Goodridge JP, Taube JS (1997) Interaction between postsubiculum and anterior thalamus in the generation of head direction cell activity. J Neurosci 17:9315–9330PubMedGoogle Scholar
  50. Goodridge JP, Touretzky DS (2000) Modeling attractor deformation in the rodent headdirection system. J Neurophysiol 83:3402–3410PubMedGoogle Scholar
  51. Goodridge JP, Dudchenko PA, Worboys KA, Golob EJ, Taube JS (1998) Cue control and head direction cells. Behav Neurosci 112:749–761PubMedCrossRefGoogle Scholar
  52. Guzowski JF, Timlin JA, Roysam B, McNaughton BL, Worley PF, Barnes CA (2005) Mapping behaviorally relevant neural circuits with immediate-early gene expression. Curr Opin Neurobiol 15:599–560PubMedCrossRefGoogle Scholar
  53. Hafting T, Fyhn M, Molden S, Moser MB, Moser EI (2005) Microstructure of a spatial map in the entorhinal cortex. Nature (Lond) 436:801–806PubMedCrossRefGoogle Scholar
  54. Hahnloser RHR (2003) Emergence of neural integration in the head-direction system by visual supervision. Neuroscience 120:877–891PubMedCrossRefGoogle Scholar
  55. Hampson RE, Simeral JD, Deadwyler SA (2002) “Keeping on track”: firing of hippocampal neurons during delayed-nonmatch-to-sample performance. J Neurosci 22: RC198PubMedGoogle Scholar
  56. Hargreaves EL, Rao G, Lee I, Knierim JJ (2005) Major dissociation between medial and lateral entorhinal input to dorsal hippocampus. Science 308:1792–1794PubMedCrossRefGoogle Scholar
  57. Harris KD, Henze DA, Hirase H, Leinekugel X, Dragoi G, Czurko A, Buzsaki G (2002) Spike train dynamics predicts theta-related phase precession in hippocampal pyramidal cells. Nature (Lond) 417:738–741PubMedCrossRefGoogle Scholar
  58. Hetherington PA, Shapiro ML (1997) Hippocampal place fields are altered by the removal of single visual cues in a distance-dependent manner. Behav Neurosci 111:20–34PubMedCrossRefGoogle Scholar
  59. Hok V, Save E, Lenck-Santini PP, Poucet B (2005) Coding for spatial goals in the prelimbic/infralimbic area of the rat frontal cortex. Proc Natl Acad Sci U S A 102:4602–4607PubMedCrossRefGoogle Scholar
  60. Hollup SA, Molden S, Donnett JG, Moser MB, Moser EI (2001) Accumulation of hippocampal place fields at the goal location in an annular watermaze task. J Neurosci 21:1635–1644PubMedGoogle Scholar
  61. Hori E, Tabuchi E, Matsumura N, Tamura R, Eifuku S, Endo S, Nishijo H, Ono T (2003) Representation of place by monkey hippocampal neurons in real and virtual translocation. Hippocampus 13:190–196PubMedCrossRefGoogle Scholar
  62. Hori E, Nishio Y, Kazui K, Umeno K, Tabuchi E, Sasaki K, Endo S, Ono T, Nishijo H (2005) Place-related neural responses in the monkey hippocampal formation in a virtual space. Hippocampus 15:991–996PubMedCrossRefGoogle Scholar
  63. Huxter J, Burgess N, O’Keefe J (2003) Independent rate and temporal coding in hippocampal pyramidal cells. Nature (Lond) 425:828–832PubMedCrossRefGoogle Scholar
  64. Jeffery KJ, Gilbert A, Burton S, Strudwick A (2003) Preserved performance in a hippocampal-dependent spatial task despite complete place cell remapping. Hippocampus 13:175–189PubMedCrossRefGoogle Scholar
  65. Jeffery KJ, Anand RL, Anderson MI (2006) A role for terrain slope in orienting hippocampal place fields. Exp Brain Res 169:218–225PubMedCrossRefGoogle Scholar
  66. Jung MW, McNaughton BL (1993) Spatial selectivity of unit activity in the hippocampal granular layer. Hippocampus 3:165–182PubMedCrossRefGoogle Scholar
  67. Kentros CG, Agnihotri NT, Streater S, Hawkins RD, Kandel ER (2004) Increased attention to spatial context increases both place field stability and spatial memory. Neuron 42:283–295PubMedCrossRefGoogle Scholar
  68. Khabbaz A, Fee MS, Tsien JZ, Tank DW (2000) A compact converging-electrode microdrive for recording head direction cells in mice. Soc Neurosci Abstr 26: rogram 367.20Google Scholar
  69. Knierim JJ (2002) Dynamic interactions between local surface cues, distal landmarks, and intrinsic circuitry in hippocampal place cells. J Neurosci 22: 6254–6264PubMedGoogle Scholar
  70. Knierim JJ, Rao G (2003) Distal landmarks and hippocampal place cells: effects of relative translation versus rotation. Hippocampus 13:604–617PubMedCrossRefGoogle Scholar
  71. Knierim JJ, Kudrimoti HS, McNaughton BL (1995) Place cells, head direction cells, and the learning of landmark stability. J Neurosci 15:1648–1659PubMedGoogle Scholar
  72. 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
  73. Kobayashi T, Nishijo H, Fukuda M, Bures J, Ono T (1997) Task-dependent representations in rat hippocampal place neurons. J Neurophysiol 78:597–613PubMedGoogle Scholar
  74. Kobayashi T, Tran AH, Nishijo H, Ono T, Matsumoto G (2003) Contribution of hippocampal place cell activity to learning and formation of goal-directed navigation in rats. Neuroscience 117:1025–1035PubMedCrossRefGoogle Scholar
  75. Kumaran D, Maguire EA (2006) The dynamics of hippocampal activation during encoding of overlapping sequences. Neuron 49:617–629PubMedCrossRefGoogle Scholar
  76. Kyd RJ, Bilkey DK (2003) Prefrontal cortex lesions modify the spatial properties of hippocampal place cells. Cereb Cortex 13:444–451PubMedCrossRefGoogle Scholar
  77. Kyd RJ, Bilkey DK (2005) Hippocampal place cells show increased sensitivity to changes in the local environment following prefrontal cortex lesions. Cereb Cortex 15:720–731PubMedCrossRefGoogle Scholar
  78. Lee AK, Wilson MA (2002) Memory of sequential experience in the hippocampus during slow wave sleep. Neuron 36:1183–1194PubMedCrossRefGoogle Scholar
  79. Lee I, Yoganarasimha D, Rao G, Knierim JJ (2004) Comparison of population coherence of place cells in hippocampal subfields CA1 and CA3. Nature (Lond) 430:456–459PubMedCrossRefGoogle Scholar
  80. Lenck-Santini PP, Save E, Poucet B (2001a) Place-cell firing does not depend on the direction of turn in a Y-maze alternation task. Eur J Neurosci 13:1055–1058PubMedCrossRefGoogle Scholar
  81. Lenck-Santini PP, Save E, Poucet B (2001b) Evidence for a relationship between placecell firing and spatial memory performance. Hippocampus 11:377–390PubMedCrossRefGoogle Scholar
  82. Lenck-Santini PP, Muller RU, Save E, Poucet (2002) Relationship between place cell firing fields and navigational decisions by rats. J Neurosci 22:9035–9047PubMedGoogle Scholar
  83. Leutgeb S, Mizumori SJ (1999) Excitotoxic septal lesions result in spatial memory deficits and altered flexibility of hippocampal single-unit representations. J Neurosci 19:6661–6672PubMedGoogle Scholar
  84. Leutgeb S, Leutbeg JK, Moser MB, Moser EI (2005a) Place cells, spatial maps and the population code for memory. Curr Opin Neurobiol 15:738–746PubMedCrossRefGoogle Scholar
  85. Leutgeb S, Leutgeb JK, Barnes CA, Moser EI, McNaughton BL, Moser MB (2005b) Independent codes for spatial and episodic memory in hippocampal neuronal ensembles. Science 309:619–623PubMedCrossRefGoogle Scholar
  86. Leutgeb JK, Leutgeb S, Treves A, Meyer R, Barnes CA, McNaughton BL, Moser MB, Moser EI (2005c) Progressive transformation of hippocampal neuronal representations in “morphed” environments. Neuron 48:345–358PubMedCrossRefGoogle Scholar
  87. Louie K, Wilson MA (2001) Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep. Neuron 29:145–156PubMedCrossRefGoogle Scholar
  88. Ludvig N, Botero JM, Tang HM, Gohil B, Kral JG (2001) Single-cell recording from the brain of freely moving monkeys. J Neurosci Methods 106: 179–187PubMedCrossRefGoogle Scholar
  89. Ludvig N, Tang HM, Gohil BC, Botero JM (2004) Detecting location-specific neuronal firing rate increases in the hippocampus of freely-moving monkeys. Brain Res 1014:97–109PubMedCrossRefGoogle Scholar
  90. Maaswinkel H, Jarrard LE, Whishaw IQ (1999) Hippocampectomized rats are impaired in homing by path integration. Hippocampus 9:553–561PubMedCrossRefGoogle Scholar
  91. Markus EJ, Barnes CA, McNaughton BL, Gladden VL, Skaggs WE (1994) Spatial information content and reliability of hippocampal CA1 neurons: effects of visual input. Hippocampus 4:410–421PubMedCrossRefGoogle Scholar
  92. Markus EJ, Qin YL, Leonard B, Skaggs WE, McNaughton BL, Barnes CA (1995) Interactions between location and task affect the spatial and directional firing of hippocampal neurons. J Neurosci 15:7079–7094PubMedGoogle Scholar
  93. Matsumura N, Nishijo H, Tamura R, Eifuku S, Endo S, Ono T (1999) Spatial-and task-dependent neuronal responses during real and virtual translocation in the monkey hippocampal formation. J Neurosci 19:2381–2393PubMedGoogle Scholar
  94. Maurer AP, Vanrhoads SR, Sutherland GR, Lipa P, McNaughton BL (2005) Self-motion and the origin of differential spatial scaling along the septo-temporal axis of the hippocampus. Hippocampus 15:841–852PubMedCrossRefGoogle Scholar
  95. McNaughton BL, Barnes CA, O’Keefe J (1983a) The contributions of position, direction, and velocity to single unit activity in the hippocampus of freely-moving rats. Exp Brain Res 52:41–49PubMedCrossRefGoogle Scholar
  96. McNaughton BL, O’Keefe J, Barnes CA (1983b) The stereotrode: a new technique for simultaneous isolation of several single units in the central nervous system from multiple unit records. J Neurosci Methods 8:391–397PubMedCrossRefGoogle Scholar
  97. McNaughton BL, Barnes CA, Meltzer J, Sutherland RJ (1989) Hippocampal granule cells are necessary for normal spatial learning but not for spatially-selective pyramidal cell discharge. Exp Brain Res 76:485–496PubMedCrossRefGoogle Scholar
  98. McNaughton BL, Chen LL, Markus EJ (1995a) “Dead reckoning,” landmark learning, and the sense of direction: a neurophysiological and computational hypothesis. J Cognit Neurosci 3:190–202CrossRefGoogle Scholar
  99. McNaughton BL, Knierim JJ, Wilson MA (1995b) Vector encoding and the vestibular foundations of spatial cognition: neurophysiological and computational mechanisms. In: Gazzaniga M (ed) The cognitive neurosciences. MIT Press, Cambridge, pp 585–595Google Scholar
  100. McNaughton BL, Barnes CA, Gerrard JL, Gothard K, Jung MW, Knierim HH, Kudrimoti H, Qin Y, Skaggs WE, Suster M, Weaver KL (1996) Deciphering the hippocampal polyglot: the hippocampus as a path integration system. J Exp Biol 199:173–185PubMedGoogle Scholar
  101. Miller VM, Best PJ (1980) Spatial correlates of hippocampal unit activity are altered by lesions of the fornix and entorhinal cortex. Brain Res 194:311–323PubMedCrossRefGoogle Scholar
  102. Mittelstaedt ML, Mittelstaedt H (1980) Homing by path integration in the mammal. Naturwissenschaften 67:566–567CrossRefGoogle Scholar
  103. Mizumori SJY, Williams JD (1993) Directionally selective mnemonic properties of neurons in the lateral dorsal nucleus of the thalamus in rats. J Neurosci 13:4015–4028PubMedGoogle Scholar
  104. Mizumori SY, McNaughton BL, Barnes CA, Fox KB (1989) Preserved spatial coding in hippocampal CA1 pyramidal cells during reversible suppression of CA3c output: evidence for pattern completion in hippocampus. J Neurosci 9:3915–3928PubMedGoogle Scholar
  105. Mizumori SJY, Puryear CB, Gill KM, Guazzelli A (2005) Head direction codes 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, pp 203–220Google Scholar
  106. Muir GM, Bilkey DK (2001) Instability in the place field location of hippocampal place cells after lesions centered on the perirhinal cortex. J Neurosci 21:4016–4025PubMedGoogle Scholar
  107. Muir GM, Taube JS (2002a) The neural correlates of spatial navigation and performance: do head direction and place cells guide behavior? Behav Cognit Neurosci Rev 1:297–317CrossRefGoogle Scholar
  108. Muir GM, Taube JS (2002b) Firing properties of head direction cells, place cells and theta cells in the freely moving chinchilla. Program No. 584.4. 2002 Abstract Viewer/Itinerary Planner. Society for Neuroscience, Washington, DCGoogle Scholar
  109. Muller R (1996) A quarter century of place cells. Neuron 17:813–822PubMedCrossRefGoogle Scholar
  110. Muller RU, Kubie JL (1987) The effects on changes in the environment on the spatial firing of hippocampal complex-spike cells. J Neurosci 7:1951–1968PubMedGoogle Scholar
  111. Muller RU, Kubie JL, Ranck JB Jr (1987) Spatial firing patterns of hippocampal complexspike cells in a fixed environment. J Neurosci 7:1935–1950PubMedGoogle Scholar
  112. Muller RU, Bostock E, Taube JS, Kubie JL (1994) On the directional firing properties of hippocampal place cells. J Neurosci 14:7235–7251PubMedGoogle Scholar
  113. O’Keefe (1976) Place units in the hippocampus of the freely moving rat. Exp Neurol 51:78–109PubMedCrossRefGoogle Scholar
  114. O’Keefe (1990) A computational theory of the hippocampal cognitive map. Prog Brain Res 83:301–312PubMedCrossRefGoogle Scholar
  115. O’Keefe J (1999) Do hippocampal pyramidal cells signal non-spatial as well as spatial information? Hippocampus 9:352–364PubMedCrossRefGoogle Scholar
  116. O’Keefe J, Burgess N (1996) Geometric determinants of the place fields of hippocampal neurons. Nature (Lond) 381:425–428PubMedCrossRefGoogle Scholar
  117. O’Keefe J, Dostrovsky J (1971) The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely moving rat. Brain Res 34:171–175PubMedCrossRefGoogle Scholar
  118. O’Keefe J, Nadel L (1978) The hippocampus as a cognitive map. Clarendon Press, OxfordGoogle Scholar
  119. O’Keefe J, Recce ML (1993) Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3:317–330PubMedCrossRefGoogle Scholar
  120. O’Keefe J, Speakman A (1987) Single unit activity in the rat hippocampus during a spatial memory task. Exp Brain Res 68:1–27PubMedGoogle Scholar
  121. Ono T, Nakamura K, Hishijo H, Eifuku S (1993) Monkey hippocampal neurons related to spatial and nonspatial functions. J Neurophysiol 70:1516–1529PubMedGoogle Scholar
  122. Pavlides C, Winson J (1989) Influences of hippocampal place cell firing in the awake state on the activity of these cells during subsequent sleep episodes. J Neurosci 9:2907–2918PubMedGoogle Scholar
  123. Paz-Villagran V, Lenck-Santini PP, Save E, Poucet B (2002) Properties of place cell firing after damage to the visual cortex. Eur J Neurosci 16:771–776PubMedCrossRefGoogle Scholar
  124. Poucet B, Save E, Lenck-Santini PP (2000) Sensory and memory properties of hippocampal place cells. Rev Neurosci 11:95–111PubMedGoogle Scholar
  125. Poucet B, Lenck-Santini PP, Hok V, Save E, Banquet JP, Gaussier P, Muller RU (2004) Spatial navigation and hippocampal place cell firing: the problem of goal encoding. Rev Neurosci 15:89–107PubMedGoogle Scholar
  126. Quirk GJ, Muller RU, Kubie JL (1990) The firing of hippocampal place cells in the dark depends on the rat’s recent experience. J Neurosci 10:2008–2017PubMedGoogle Scholar
  127. Quirk GJ, Muller RU, Kubie JL, Ranck JB Jr (1992) The positional firing properties of medial entorhinal neurons: description and comparison with hippocampal place cells. J Neurosci 12:1945–1963PubMedGoogle Scholar
  128. Ranck J (1984) Head direction cells in the deep layer of dorsal presubiculum in freely moving rats. Soc Neurosci Abstr 10:599Google Scholar
  129. Redish AD (1999) Beyond the cognitive map. MIT Press, CambridgeGoogle Scholar
  130. Redish AD, Elga AN, Touretzky DS (1996) A coupled attractor model of the rodent head direction system. Network Comput Neural Syst 7:671–685CrossRefGoogle Scholar
  131. Redish AD, Battaglia FP, Chawla MK, Ekstrom AD, Gerrard JL, Lipa P, Rosenweig ES, Worley PF, Guzowski JF, McNaughton BL, Barnes CA (2001) Independence of firing correlates of anatomically proximate hippocampal pyramidal cells. J Neurosci 21:RC134PubMedGoogle Scholar
  132. Robertson RG, Rolls ET, Georges-Francois P, Panzeri S (1999) Head direction cells in the primate pre-subiculum. Hippocampus 9:206–219PubMedCrossRefGoogle Scholar
  133. Rolls ET (1999) Spatial view cells and the representation of place in the primate hippocampus. Hippocampus 9:467–480PubMedCrossRefGoogle Scholar
  134. Rolls ET, O’Mara SM (1995) View-responsive neurons in the primate hippocampal complex. Hippocampus 5:409–424PubMedCrossRefGoogle Scholar
  135. Rubin J, Terman D, Chow C (2001) Localized bumps of activity sustained by inhibition in a two-layer thalamic network. J Comp Neurosci 10:313–331CrossRefGoogle Scholar
  136. Russell NA, Horii A, Smith PF, Darlington CL, Bilkey DK (2003) Long-term effects of permanent vestibular lesions on hippocampal spatial firing. J Neurosci 23:6490–6498PubMedGoogle Scholar
  137. Sargolini F, Fyhn M, Hafting T, McNaughton BL, Witter MP, Moser MB, Moser EI (2006) Conjunctive representation of position, direction, and velocity in entorhinal cortex. Science 312:758–762PubMedCrossRefGoogle Scholar
  138. Save E, Cressant A, Thinus-Blanc C, Poucet B (1998) Spatial firing of hippocampal place cells in blind rats. J Neurosci 18:1818–1826PubMedGoogle Scholar
  139. Save E, Nerad L, Poucet B (2000) Contribution of multiple sensory information to place field stability in hippocampal place cells. Hippocampus 10:64–76PubMedCrossRefGoogle Scholar
  140. Save E, Guazzelli A, Poucet B (2001) Dissociation of the effects of bilateral lesions of the dorsal hippocampus and parietal cortex on path integration in the rat. Behav Neurosci 115:1212–1223PubMedCrossRefGoogle Scholar
  141. Scoville WB, Milner B (1957) Loss of recent memory after bilateral hippocampal lesions. J Neurol Neurosurg Psychiatry 20:11–21PubMedCrossRefGoogle Scholar
  142. Shapiro ML, Tanila H, Eichenbaum H (1997) Cues that hippocampal place cells encode: dynamic and hierarchical representation of local and distal stimuli. Hippocampus 7:624–642PubMedCrossRefGoogle Scholar
  143. Sharp PE (1997) Subicular cells generate similar spatial firing patterns in two geometrically and visually distinctive environments: comparison with hippocampal place cells. Behav Brain Res 85:71–92PubMedCrossRefGoogle Scholar
  144. Sharp PE, Green C (1994) Spatial correlates of firing patterns of single cells in the subiculum of the freely moving rat. J Neurosci 14:2339–2356PubMedGoogle Scholar
  145. Sharp PE, Blair HT, Cho J (2001a) The anatomical and computational basis of the rat head-direction cell signal. Trends Neurosci 24:289–294PubMedCrossRefGoogle Scholar
  146. Sharp PE, Tinkelman A, Cho J (2001b) Angular velocity and head direction signals recorded from the dorsal tegmental nucleus of Gudden in the rat: implications for path integration in the head direction cell circuit. Behav Neurosci 115:571–588PubMedCrossRefGoogle Scholar
  147. 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 7:173–180PubMedGoogle Scholar
  148. Skaggs WE, McNaughton BL (1996) Replay of neuronal firing sequences in rat hippocampus during sleep following spatial experience. Science 271:1870–1873PubMedCrossRefGoogle Scholar
  149. Smith DM, Mizumori SJ (2006) Learning-related development of context-specific neuronal responses to places and events: the hippocampal role in context processing. J Neurosci 26:3154–3163PubMedCrossRefGoogle Scholar
  150. Smith PF, Horii A, Russell N, Bilkey DK, Zheng Y, Liu P, Kerr DS, Darlington CL (2005) The effects of vestibular lesions on hippocampal function in rats. Prog Neurobiol 75:391–405PubMedCrossRefGoogle Scholar
  151. 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 25:1002–1014PubMedCrossRefGoogle Scholar
  152. Speakman A, O’Keefe J (1990) Hippocampal complex spike cells do not change their place fields if the goal is moved within a cue controlled environment. Eur J Neurosci 2:544–555PubMedCrossRefGoogle Scholar
  153. Squire LR (1992) Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol Rev 99:195–231PubMedCrossRefGoogle Scholar
  154. Stackman RW, Taube JS (1997) Firing properties of head direction cells in rat anterior thalamic neurons: dependence upon vestibular input. J Neurosci 17:4349–4358PubMedGoogle Scholar
  155. Stackman RW, Taube JS (1998) Firing properties of rat lateral mammillary nuclei single units: head direction, head pitch, and angular head velocity. J Neurosci 18:9020–9037PubMedGoogle Scholar
  156. Stackman RW, Clark AS, Taube JS (2002) Hippocampal spatial representations require vestibular input. Hippocampus 12:291–303PubMedCrossRefGoogle Scholar
  157. Stackman RW, Golob EJ, Bassett JP, Taube JS (2003) Passive transport disrupts directional path integration by rat head direction cells. J Neurophysiol 90:2862–2874PubMedCrossRefGoogle Scholar
  158. Stackman RW, Tullman ML, Taube JS (2000) Maintenance of rat head direction cell firing during locomotion in the vertical plane. J Neurophysiol 83:393–405PubMedGoogle Scholar
  159. Sun NL, Lei YL, Kim BH, Ryou JW, Ma YY, Wilson FA (2002) Neurophysiological recordings in freely moving monkeys. Methods 38:20220–20229Google Scholar
  160. Tanila H, Shapiro ML, Eichenbaum H (1997) Discordance of spatial representation in ensembles of hippocampal place cells. Hippocampus 7:613–623PubMedCrossRefGoogle Scholar
  161. Taube JS (1995a) Head direction cells recorded in the anterior thalamic nuclei of freely moving rats. J Neurosci 15:70–86PubMedGoogle Scholar
  162. Taube JS (1995b) Place cell activity recorded from the parasubiculum in freely moving rats. Hippocampus 5:569–583PubMedCrossRefGoogle Scholar
  163. Taube JS (1998) Head direction cells and the neurophysiological basis for a sense of direction. Prog Neurobiol 55:225–256PubMedCrossRefGoogle Scholar
  164. Taube JS, Bassett JP (2003) Persistent neural activity in head direction cells. Cereb Cortex 13:1162–1172PubMedCrossRefGoogle Scholar
  165. 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
  166. Taube JS, Muller RU (1998) Comparison of head direction cell activity in the postsubiculum and anterior thalamus of freely moving rats. Hippocampus 8:87–108PubMedCrossRefGoogle Scholar
  167. 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
  168. 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
  169. Taube JS, Kesslak JP, Cotman CW (1992) Lesions of the rat postsubiculum impair performance on spatial tasks. Behav Neural Biol 57:131–143PubMedCrossRefGoogle Scholar
  170. Taube JS, Stackman RW, Calton JL, Oman CM (2004) Rat head direction cell responses in zero-gravity parabolic flight. J Neurophysiol 92:2887–2997PubMedCrossRefGoogle Scholar
  171. Thompson LT, Best PJ (1990) Long-term stability of the place-field activity of single units recorded from the dorsal hippocampus of freely behaving rats. Brain Res 509:299–308PubMedCrossRefGoogle Scholar
  172. Tolman EC (1948) Cognitive maps in rats and men. Psychol Rev 55:189–208PubMedCrossRefGoogle Scholar
  173. Touretzky DS, Redish AD (1996) Theory of rodent navigation based on interacting representations of space. Hippocampus 6:247–270PubMedCrossRefGoogle Scholar
  174. van Groen T, Wyss JM (1990) The postsubicular cortex in the rat: characterization of the fourth region of the subicular complex and its connections. Brain Res 529:165–177PubMedCrossRefGoogle Scholar
  175. Vann SD (2005) Transient spatial deficit associated with bilateral lesions of the lateral mammillary nuclei. Eur J Neurosci 21:820–824PubMedCrossRefGoogle Scholar
  176. Vertes RP (2004) Memory consolidation in sleep: dream or reality. Neuron 44:135–148PubMedCrossRefGoogle Scholar
  177. Wang R, Spelke E (2002) Human spatial representation: insights from animals. Trends Cognit Sci 6:376–382CrossRefGoogle Scholar
  178. Whishaw IQ, Gorny B (1999) Path integration absent in scent-tracking fimbria-fornix rats: evidence for hippocampal involvement in “sense of direction” and “sense of distance” using self-movement cues. J Neurosci 19:4662–4673PubMedGoogle Scholar
  179. Whishaw IQ, Maaswinkel H (1998) Rats with fimbria-fornix lesions are impaired in path integration: a role for the hippocampus in “sense of direction.” J Neurosci 18:3050–3058PubMedGoogle Scholar
  180. 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 118:67–76PubMedCrossRefGoogle Scholar
  181. Wiener SI (1993) Spatial and behavioral correlates of striatal neurons in rats performing a self-initiated navigation task. J Neurosci 13:3802–3817PubMedGoogle Scholar
  182. Wiener SI, Paul CA, Eichenbaum H (1989) Spatial and behavioral correlates of hippocampal neuronal activity. J Neurosci 9:2737–2763PubMedGoogle Scholar
  183. Wiener SI, Arleo A, Dejean C, Boucheny C, Khamassi M, Zugaro MB (2004) Optic field flow signals update the activity of head direction cells in the rat anterodorsal thalamus. Program no. 209.2. 2004 Abstract Viewer/Itinerary Planner, Society for Neuroscience, Washington, DCGoogle Scholar
  184. Wills TJ, Lever C, Cacucci F, Burgess N, O’Keefe J (2005) Attractor dynamics in the hippocampal representation of the local environment. Science 308:873–876PubMedCrossRefGoogle Scholar
  185. Wilson MA, McNaughton BL (1993) Dynamics of the hippocampal ensemble code for space. Science 261:1055–1058PubMedCrossRefGoogle Scholar
  186. Wilson MA, McNaughton BL (1994) Reactivation of hippocampal ensemble memories during sleep. Science 265:676–679PubMedCrossRefGoogle Scholar
  187. Wilton LA, Baird AL, Muir JL, Honey RC, Aggleton JP (2001) Loss of the thalamic nuclei for “head direction” impairs performance on spatial memory tasks in rats. Behav Neurosci 115:861–869PubMedCrossRefGoogle Scholar
  188. Wood ER, Dudchenko PA, Robitsek RJ, Eichenbaum H (2000) Hippocampal neurons encode information about different types of memory episodes occurring in the same location. Neuron 27:623–633PubMedCrossRefGoogle Scholar
  189. Worden R (1992) Navigation by fragment fitting: a theory of hippocampal function. Hippocampus 2:165–187PubMedCrossRefGoogle Scholar
  190. Xie X, Hahnloser RHR, Seung HD (2002) Double-ring network model of the headdirection system. Phys Rev E Stat Nonlin Soft Matter Phys 66:041902PubMedGoogle Scholar
  191. 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 26:622–631PubMedCrossRefGoogle Scholar
  192. 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
  193. Zugaro MB, Tabuchi E, Wiener SI (2000) Influence of conflicting visual, inertial and substratal cues on head direction cell activity. Exp Brain Res 133:198–208PubMedCrossRefGoogle Scholar
  194. Zugaro MB, Berthoz A, Wiener SI (2002) Peak firing rates of rat anterodorsal thalamic head direction cells are higher during faster passive rotations. Hippocampus 12:481–486PubMedCrossRefGoogle Scholar
  195. 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 2007

Authors and Affiliations

  • Joel E. Brown
    • 1
  • Jeffrey S. Taube
    • 1
  1. 1.Department of Psychological and Brain SciencesDartmouth CollegeHanoverUSA

Personalised recommendations