Environmental anchoring of head direction in a computational model of retrosplenial cortex

Journal of Neuroscience

Volumn 36, Issue 46, 2016, Pages 11601-11618

  Bicanski, Andrej ^a,b   Burgess, Neil ^a,b  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Attractor networks; Head direction cells; Papez circuit; Parallax; Place cells; Retrosplenial cortex

Indexed keywords

ARTICLE; BIOINFORMATICS; BRAIN DAMAGE; BRAIN MAPPING; BRAIN NERVE CELL; HIPPOCAMPUS; HUMAN; MATHEMATICAL MODEL; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NERVE CONDUCTION; NEUROFEEDBACK; NONHUMAN; PRIORITY JOURNAL; RETROSPLENIAL CORTEX; TUNING CURVE; ANIMAL; BIOLOGICAL MODEL; BRAIN CORTEX; COMPUTER SIMULATION; DEPTH PERCEPTION; ECOSYSTEM; HEAD; HEAD MOVEMENT; ORIENTATION; PHYSIOLOGY; SENSORY FEEDBACK; SPATIAL BEHAVIOR; SPATIAL ORIENTATION;

ANIMALS; CEREBRAL CORTEX; COMPUTER SIMULATION; ECOSYSTEM; FEEDBACK, SENSORY; HEAD; HEAD MOVEMENTS; HUMANS; MODELS, NEUROLOGICAL; ORIENTATION; SPACE PERCEPTION; SPATIAL BEHAVIOR; SPATIAL NAVIGATION;

EID: 84996593885     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0516-16.2016     Document Type: Article

References (93)

1. Alexander AS,Nitz DA (2015) Retrosplenial cortex maps the conjunction of internal and external spaces. Nat Neurosci 18:1143–1151.
2. Anzalone S,Roland J,Vogt B,Savage L (2009) Acetylcholine efflux from retrosplenial areas and hippocampal sectors during maze exploration. Behav Brain Res 201:272–278.
3. Auger SD,Maguire EA (2013) Assessing the mechanism of response in the retrosplenial cortex of good and poor navigators. Cortex 49:2904–2913.
4. Auger SD,Mullally SL,Maguire EA (2012) Retrosplenial cortex codes for permanent landmarks. PLoS One 7:e43620.
5. Ball D,Heath S,Wiles J,Wyeth G,Corke P,Milford M (2013) OpenRatS-LAM: an open source brain-based SLAM system. Auton Robot 34: 149–176.
6. Barry C,Lever C,Hayman R,Hartley T,Burton S,O’Keefe J,Jeffery K,Burgess N (2006) The boundary vector cell model of place cell firing and spatial memory. Rev Neurosci 17:71–97.
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 27:7564–7577.
8. Bi GQ,Poo MM (1998) Synaptic modifications in cultured hippocampal neurons: dependence on spike timing,synaptic strength,and postsynaptic cell type. J Neurosci 18:10464–10472.
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 15:6260–6270.
10. Blair HT,Lipscomb BW,Sharp PE (1997) Anticipatory time intervals of head direction cells in the anterior thalamus of the rat: implications for path integration in the head direction circuit. J Neurophysiol 78:145–159.
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 21:1387–1397.
12. 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 19:6673–6683.
13. Boccara CN,Sargolini F,Thoresen VH,Solstad T,Witter MP,Moser EI,Moser MB (2010) Grid cells in pre- and parasubiculum. Nat Neurosci 13:987–994.
14. Boucheny C,Brunel N,Arleo A (2005) A continuous attractor network model without recurrent excitation: maintenance and integration in the head direction cell system. J Comput Neurosci 18:205–227.
15. Burgess N,Becker S,King JA,O’Keefe J (2001a) Memory for events and their spatial context: models and experiments. Philos Trans R Soc Lond B Biol Sci 356:1493–1503.
16. Burgess N,Maguire EA,Spiers HJ,O’Keefe J (2001b) A temporoparietal and prefrontal network for retrieving the spatial context of lifelike events. Neuroimage 14:439–453.
17. Burgess N,Cacucci F,Lever C,O’Keefe J (2005) Characterizing multiple independent behavioral correlates of cell firing in freely moving animals. Hippocampus 15:149–153.
18. Byrne P,Becker S,Burgess N (2007) Remembering the past and imagining the future: a neural model of spatial memory and imagery. Psychol Rev 114:340–375.
19. Cacucci F,Lever C,Wills TJ,Burgess N,O’Keefe J (2004) Theta-modulated place-by-direction cells in the hippocampal formation in the rat. J Neurosci 24:8265–8277.
20. Campi KL,Krubitzer L (2010) Comparative studies of diurnal and nocturnal rodents: differences in lifestyle result in alterations in cortical field size and number. J Comp Neurol 518:4491–4512.
21. Carpenter F,Manson D,Jeffery K,Burgess N,Barry C (2015) Grid cells form a global representation of connected environments. Curr Biol 25: 1176–1182.
22. Cho J,Sharp PE (2001) Head direction,place,and movement correlates for cells in the rat retrosplenial cortex. Behav Neurosci 115:3–25.
23. Clark BJ,Harris MJ,Taube JS (2012) Control of anterodorsal thalamic head direction cells by environmental boundaries: comparison with conflicting distal landmarks. Hippocampus 22:172–187.
24. Cressant A,Muller RU,Poucet B (1997) Failure of centrally placed objects to control the firing fields of hippocampal place cells. J Neurosci 17: 2531–2542.
25. Dean P (1981) Visual pathways and acuity in hooded rats. Behav Brain Res 3:239–271.
26. Degris T,Sigaud O,Wiener SI,Arleo A (2004) Rapid response of head direction cells to reorienting visual cues: a computational model. Neurocomputing 58:675–682.
27. Dhindsa K,Drobinin V,King J,Hall GB,Burgess N,Becker S (2014) Examining the role of the temporo-parietal network in memory,imagery,and viewpoint transformations. Front Hum Neurosci 8:709.
28. Dudchenko PA,Zinyuk LE (2005) The formation of cognitive maps of adjacent environments: evidence from the head direction cell system. Behav Neurosci 119:1511–1523.
29. Epstein RA,Vass LK (2013) Neural systems for landmark-based wayfinding in humans. Philos Trans R Soc Lond B Biol Sci 369:20120533.
30. 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– 7650.
31. Golob EJ,Taube JS (1999) Head direction cells in rats with hippocampal or overlying neocortical lesions: evidence for impaired angular path integration. J Neurosci 19:7198–7211.
32. Goodridge JP,Taube JS (1997) Interaction between the postsubiculum and anterior thalamus in the generation of head direction cell activity. J Neurosci 17:9315–9330.
33. Goodridge JP,Touretzky DS (2000) Modeling attractor deformation in the rodent head direction system. J Neurophysiol 83:3402–3410.
34. Goodridge JP,Dudchenko PA,Worboys KA,Golob EJ,Taube JS (1998) Cue control and head direction cells. Behav Neurosci 112:749–761.
35. Guzowski JF,McNaughton BL,Barnes CA,Worley PF (1999) Environment-specific expression of the immediate-early gene Arc in hippocampal neuronal ensembles. Nat Neurosci 2:1120–1124.
36. Hahnloser RH (2003) Emergence of neural integration in the head direction system by visual supervision. Neuroscience 120:877–891.
37. Hartley T,Burgess N,Lever C,Cacucci F,O’Keefe J (2000) Modeling place fields in terms of the cortical inputs to the hippocampus. Hippocampus 10:369–379.
38. Hasselmo ME (2006) The role of acetylcholine in learning and memory. Curr Opin Neurobiol 16:710–715.
39. Jacob P-Y,Casali G,Spieser L,Page H,Overington D,Jeffery K (2016) Uncoupling of dysgranular retrosplenial “head direction” cells from the global head direction network. bioRxiv 062042. Advance online publication.
40. Knierim JJ,Kudrimoti HS,McNaughton BL (1995) Place cells,head direction cells,and the learning of landmark stability. J Neurosci 15:1648–1659.
41. Knight R,Piette CE,Page H,Walters D,Marozzi E,Nardini M,Stringer S,Jeffery KJ (2013) Weighted cue integration in the rodent head direction system. Philos Trans R Soc Lond B Biol Sci 369:20120512.
42. Lambrey S,Doeller C,Berthoz A,Burgess N (2012) Imagining being somewhere else: neural basis of changing perspective in space. Cereb Cortex 22:166–174.
43. Lever C,Wills T,Cacucci F,Burgess N,O’Keefe J (2002) Long-term plasticity in hippocampal place-cell representation of environmental geometry. Nature 416:90–94.
44. Marchette SA,Vass LK,Ryan J,Epstein RA (2014) Anchoring the neural compass: coding of local spatial reference frames in human medial parietal lobe. Nat Neurosci 17:1598–1606.
45. Milford MJ,Wiles J,Wyeth GF (2010) Solving navigational uncertainty using grid cells on robots. PLoS Comput Biol 6:e1000995.
46. Milford M,Schulz R,Prasser D,Wyeth G,Wiles J (2007) Learning spatial concepts from RatSLAM representations. Robotics Autonom Syst 55: 403–410.
47. Mizumori SJ,Williams JD (1993) Directionally selective mnemonic properties of neurons in the lateral dorsal nucleus of the thalamus of rats. J Neurosci 13:4015–4028.
48. Monaco JD,Rao G,Roth ED,Knierim JJ (2014) Attentive scanning behavior drives one-trial potentiation of hippocampal place fields. Nat Neurosci 17:725–731.
49. 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 29:14521–14533.
50. O’Keefe J,Burgess N (1996) Geometric determinants of the place fields of hippocampal neurons. Nature 381:425–428.
51. Page HJ,Walters DM,Knight R,Piette CE,Jeffery KJ,Stringer SM (2013) A theoretical account of cue averaging in the rodent head direction system. Philos Trans R Soc Lond B Biol Sci 369:20130283.
52. Paz-Villagrán V,Save E,Poucet B (2004) Independent coding of connected environments by place cells. Eur J Neurosci 20:1379–1390.
53. Pothuizen HH,Aggleton JP,Vann SD (2008) Do rats with retrosplenial cortex lesions lack direction? Eur J Neurosci 28:2486–2498.
54. Pouget A,Sejnowski TJ (1997) Spatial transformations in the parietal cortex using basis functions. J Cogn Neurosci 9:222–237.
55. Pouget A,Deneve S,Duhamel JR (2002) A computational perspective on the neural basis of multisensory spatial representations. Nat Rev Neurosci 3:741–747.
56. Ranck JB (1984) Head direction cells in the deep cell layer of dorsal presubiculum in freely moving rats. Soc Neurosci Abstr 10:176.12.
57. Redish AD,Elga AN,Touretzky DS (1996) A coupled attractor model of the rodent head direction system. Network 7:671–685.
58. Salinas E,Abbott LF (1995) Transfer of coded information from sensory to motor networks. J Neurosci 15:6461–6474.
59. 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 312:758–762.
60. Savage LM,Hall JM,Vetreno RP (2011) Anterior thalamic lesions alter both hippocampal-dependent behavior and hippocampal acetylcholine release in the rat. Learn Mem 18:751–758.
61. 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 115:571–588.
62. Shibata H (1998) Organization of projections of rat retrosplenial cortex to the anterior thalamic nuclei. Eur J Neurosci 10:3210–3219.
63. Shibata H,Honda Y,Sasaki H,Naito J (2009) Organization of intrinsic connections of the retrosplenial cortex in the rat. Anat Sci Int 84:280–292.
64. Shine JP,Valdés-Herrera JP,Hegarty M,Wolbers T (2016) The human retrosplenial cortex and thalamus code head direction in a global reference frame. J Neurosci 36:6371–6381.
65. 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 7:173–180.
66. Smith R,Self M,Cheeseman P (1990) Estimating uncertain spatial relationships in robotics. In: Autonomous robot vehicles,pp 167–193. New York: Springer.
67. Song P,Wang XJ (2005) Angular path integration by moving “Hill of Activity”: a spiking neuron model without recurrent excitation of the head direction system. J Neurosci 25:1002–1014.
68. Stackman RW,Taube JS (1997) Firing properties of head direction cells in the rat anterior thalamic nucleus: dependence on vestibular input. J Neurosci 17:4349–4358.
69. Stackman RW,Taube JS (1998) Firing properties of rat lateral mammillary single units: head direction,head pitch,and angular head velocity. J Neurosci 18:9020–9037.
70. Stratton P,Wyeth G,Wiles J (2010) Calibration of the head direction network: a role for symmetric angular head velocity cells. J Comput Neurosci 28:527–538.
71. Stringer SM,Rolls ET (2006) Self-organizing path integration using a linked continuous attractor and competitive network: path integration of head direction. Network 17:419–445.
72. Stringer SM,Trappenberg TP,Rolls ET,de Araujo IE (2002) Self-organizing continuous attractor networks and path integration: one-dimensional models of head direction cells. Network 13:217–242.
73. Sugar J,Witter MP,van Strien N,Cappaert N (2011) The retrosplenial cortex: intrinsic connectivity and connections with the (para) hippocampal region in the rat. An interactive connectome. Front Neuroinform 5:7.
74. Taube JS (1995) Place cells recorded in the parasubiculum of freely moving rats. Hippocampus 5:569–583.
75. Taube JS (2007) The head direction signal: origins and sensory-motor integration. Annu Rev Neurosci 30:181–207.
76. Taube JS,Bassett JP (2003) Persistent neural activity in head direction cells. Cereb Cortex 13:1162–1172.
77. Taube JS,Burton HL (1995) Head direction cell-activity monitored in a novel environment and during a cue conflict situation. J Neurophysiol 74:1953–1971.
78. Taube JS,Muller RU (1998) Comparisons of head direction cell activity in the postsubiculum and anterior thalamus of freely moving rats. Hippocampus 8:87–108.
79. 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 10:420–435.
80. 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 10:436–447.
81. Thompson LT,Best PJ (1989) Place cells and silent cells in the hippocampus of freely-behaving rats. J Neurosci 9:2382–2390.
82. van der Meer MA,Knierim JJ,Yoganarasimha D,Wood ER,van Rossum MC (2007) Anticipation in the rodent head direction system can be explained by an interaction of head movements and vestibular firing properties. J Neurophysiol 98:1883–1897.
83. van Groen T,Wyss JM (1990) The connections of presubiculum and parasubiculum in the rat. Brain Res 518:227–243.
84. van Groen T,Wyss JM (1992) Connections of the retrosplenial dysgranular cortex in the rat. J Comp Neurol 315:200–216.
85. Vann SD,Aggleton JP (2005) Selective dysgranular retrosplenial cortex lesions in rats disrupt allocentric performance of the radial-arm maze task. Behav Neurosci 119:1682–1686.
86. Vann SD,Kristina Wilton LA,Muir JL,Aggleton JP (2003) Testing the importance of the caudal retrosplenial cortex for spatial memory in rats. Behav Brain Res 140:107–118.
87. Vann SD,Aggleton JP,Maguire EA (2009) What does the retrosplenial cortex do? Nat Rev Neurosci 10:792–802.
88. Wilber AA,Clark BJ,Forster TC,Tatsuno M,McNaughton BL (2014) Interaction of egocentric and world-centered reference frames in the rat posterior parietal cortex. J Neurosci 34:5431–5446.
89. Xie X,Hahnloser RHR,Seung HS (2002) Double-ring network model of the head direction system. Phys Rev E 66:041902–041909.
90. Yoder RM,Taube JS (2009) Head direction cell activity in mice: robust directional signal depends on intact otolith organs. J Neurosci 29: 1061–1076.
91. Yoder RM,Peck JR,Taube JS (2015) Visual landmark information gains control of the head direction signal at the lateral mammillary nuclei. J Neurosci 35:1354–1367.
92. Yoshida M,Hasselmo ME (2009) Persistent firing supported by an intrinsic cellular mechanism in a component of the head direction system. J Neurosci 29:4945–4952.
93. Zhang K (1996) Representation of spatial orientation by the intrinsic dynamics of the head direction cell ensemble: a theory. J Neurosci 16: 2112–2126.