The hippocampus and spatial constraints on mental imagery

Frontiers in Human Neuroscience

Volumn , Issue MAY 2012, 2012, Pages 1-12

  Bird, Chris M ^a,b   Bisby, James A ^b,c   Burgess, Neil ^b,c  

^a UNIVERSITY OF SUSSEX   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Boundary vector cell; Computational model; Construction; FMRI; Place cell

Indexed keywords

BEHAVIORAL RESEARCH; DEPTH PERCEPTION; DISEASE ASSOCIATION; HIPPOCAMPUS; HUMAN; IMAGERY; IMAGINATION; INFORMATION RETRIEVAL; LIMBIC CORTEX; MEMORY CONSOLIDATION; MEMORY DISORDER; MENTAL PERFORMANCE; NEUROIMAGING; NEURONAVIGATION; NEUROPSYCHOLOGY; NONHUMAN; PARIETAL CORTEX; POSTTRAUMATIC STRESS DISORDER; PSYCHOTRAUMA; RETROSPLENIAL CORTEX; REVIEW; SENSORY ANALYSIS; SPATIAL MEMORY; VIRTUAL REALITY;

EID: 84864104547     PISSN: 16625161     EISSN: 16625161     Source Type: Journal    
DOI: 10.3389/fnhum.2012.00142     Document Type: Review

References (113)

1. Abrahams, S., Pickering, A., Polkey, C. E., and Morris, R. G. (1997). Spatial memory deficits in patients with unilateral damage to the right hippocampal formation. Neuropsychologia 35, 11-24.
2. Addis, D. R., Wong, A. T., and Schacter, D. L. (2007). Remembering the past and imagining the future: common and distinct neural substrates during event construction and elaboration. Neuropsychologia 45, 1363-1377.
3. Aggleton, J. P., and Brown, M. W. (1999). Episodic memory, amnesia, and the hippocampal-anterior thalamic axis. Behav. Brain Sci. 22, 425-490.
4. Anagnostaras, S. G., Maren, S., and Fanselow, M. S. (1999). Temporally graded retrograde amnesia of contextual fear after hippocampal damage in rats: within-subjects examination. J. Neurosci. 19, 1106-1114.
5. Anderson, M. C., Ochsner, K. N., Kuhl, B., Cooper, J., Robertson, E., Gabrieli, S. W., Glover, G. H., and Gabrieli, J. D. (2004). Neural systems underlying the suppression of unwanted memories. Science 303, 232-235.
6. Barry, C., Hayman, R., Burgess, N., and Jeffery, K. J. (2007). Experience-dependent rescaling of entorhinal grids. Nat. Neurosci. 10, 682-684.
7. Becker, S., and Burgess, N. (2001). A model of spatial recall, mental imagery and neglect. Neural Inf. Process. Syst. 13, 96-102.
8. Bird, C. M., Capponi, C., King, J. A., Doeller, C. F., and Burgess, N. (2010). Establishing the boundaries: the hippocampal contribution to imagining scenes. J. Neurosci. 30, 11688-11695.
9. Bisby, J. A., Brewin, C. R., Leitz, J. R., and Valerie, C. H. (2009). Acute effects of alcohol on the development of intrusive memories. Psychopharmacology (Berl.) 204, 655-666.
10. Bisby, J. A., King, J. A., Brewin, C. R., Burgess, N., and Curran, H. V. (2010). Acute effects of alcohol on intrusive memory development and viewpoint dependence in spatial memory support a dual representation model. Biol. Psychiatry 68, 280-286.
11. Boccara, C. N., Sargolini, F., Thoresen, V. H., Solstad, T., Witter, M. P., Moser, E. I., and Moser, M. B. (2010). Grid cells in presubiculum and parasubiculum. Nat. Neurosci. 13, 987-994.
12. Bohbot, V. D., Jech, R., Ruzicka, E., Nadel, L., Kalina, M., Stepankova, K., and Bures, J. (2002). Rat spatial memory tasks adapted for humans: characterization in subjects with intact brain and subjects with selective medial temporal lobe thermal lesions. Physiol. Res. 1 (Suppl. 51), S49-S65.
13. Bostock, E., Muller, R. U., and Kubie, J. L. (1991). Experience-dependent modifications of hippocampal place cell firing. Hippocampus 1, 193-205.
14. Brewin, C. R., Gregory, J. D., Lipton, M., and Burgess, N. (2010). Intrusive images in psychological disorders: characteristics, neural mechanisms, and treatment implications. Psychol. Rev. 117, 210-232.
15. Burgess, N., Becker, S., King, J. A., and O'Keefe, J. (2001). Memory for events and their spatial context: models and experiments. Philos. Trans. R. Soc. Lond. B Biol. Sci. 356, 1493-1503.
16. Burgess, N., Donnett, J. G., Jeffery, K. J., and O'Keefe, J. (1997). Robotic and neuronal simulation of the hippocampus and rat navigation. Philos. Trans. R. Soc. Lond. B Biol. Sci. 352, 1535-1543.
17. Burgess, N., Maguire, E. A., and O'Keefe, J. (2002). The human hippocampus and spatial and episodic memory. Neuron 35, 625-641.
18. Byrne, P., Becker, S., and Burgess, N. (2007). Remembering the past and imagining the future: a neural model of spatial memory and imagery. Psychol. Rev. 114, 340-375.
19. Cahill, L., and McGaugh, J. L. (1998). Mechanisms of emotional arousal and lasting declarative memory. Trends Neurosci. 21, 294-299.
20. Cohen, N. J., Ryan, J., Hunt, C., Romine, L., Wszalek, T., and Nash, C. (1999). Hippocampal system and declarative (relational) memory: summarizing the data from functional neuroimaging studies. Hippocampus 9, 83-98.
21. Cohen, N. J., and Squire, L. R. (1980). Preserved learning and retention of pattern-analyzing skill in amnesia: dissociation of know how and knowing that. Science 210, 207-210.
22. Cohen, N. J., and Eichenbaum, H. (1993). Memory, Amnesisa and the Hippocampal System. Cambridge, MA: MIT Press.
23. Craig, A. D. (2002). How do you feel? Interoception: the sense of the physiological condition of the body. Nat. Rev. Neurosci. 3, 655-666.
24. Craig, A. D. (2009). How do you feel-now? The anterior insula and human awareness. Nat. Rev. Neurosci. 10, 59-70.
25. Cressant, A., Muller, R. U., and Poucet, B. (1997). Failure of centrally placed objects to control the firing fields of hippocampal place cells. J. Neurosci. 17, 2531-2542.
26. Critchley, H. D., Wiens, S., Rotshtein, P., Ohman, A., and Dolan, R. J. (2004). Neural systems supporting interoceptive awareness. Nat. Neurosci. 7, 189-195.
27. Curran, H. V., and Hildebrandt, M. (1999). Dissociative effects of alcohol on recollective experience. Conscious. Cogn. 8, 497-509.
28. Davachi, L., and Wagner, A. D. (2002). Hippocampal contributions to episodic encoding: insights from relational and item-based learning. J. Neurophysiol. 88, 982-990.
29. Doeller, C. F., and Burgess, N. (2008). Distinct error correcting and incidental learning of location relative to landmarks and boundaries. Proc. Natl. Acad. Sci. U.S.A. 105, 5909-5914.
30. Doeller, C. F., Barry, C., and Burgess, N. (2010). Evidence for grid cells in a human memory network. Nature 463, 657-661.
31. Doeller, C. F., King, J. A., and Burgess, N. (2008). Parallel striatal and hip-pocampal systems for landmarks and boundaries in spatial memory. Proc. Natl. Acad. Sci. U.S.A. 105, 5915-5920.
32. Dombeck, D. A., Harvey, C. D., Tian, L., Looger, L. L., and Tank, D. W. (2010). Functional imaging of hip-pocampal place cells at cellular resolution during virtual navigation. Nat. Neurosci. 13, 1433-1440.
33. Duff, M. C., and Brown-Schmidt, S. (2012). The hippocampus and the flexible use and processing of language. Front. Hum. Neurosci. 6:69. doi:10.3389/fnhum.2012.00069
34. Eacott, M. J., and Gaffan, E. A. (2005). The roles of perirhinal cortex, postrhinal cortex, and the fornix in memory for objects, contexts, and events in the rat. Q. J. Exp. Psychol. B 58, 202-217.
35. Eichenbaum, H., Yonelinas, A. P., and Ranganath, C. (2007). The medial temporal lobe and recognition memory. Annu. Rev. Neurosci. 30, 123-152.
36. Eichenbaum, H., and Cohen, N. J. (2001). From Conditioning to Conscious Recollection: Memory Systems of the Brain. Oxford: Oxford University Press.
37. Ekstrom, A. D., Kahana, M. J., Caplan, J. B., Fields, T. A., Isham, E. A., Newman, E. L., and Fried, I. (2003). Cellular networks underlying human spatial navigation. Nature 425, 184-188.
38. Fenton, A. A., and Muller, R. U. (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, 3182-3187.
39. Fyhn, M., Hafting, T., Treves, A., Moser, M. B., and Moser, E. I. (2007). Hippocampal remapping and grid realignment in entorhinal cortex. Nature 446, 190-194.
40. Galletti, C., Battaglini, P. P., and Fattori, P. (1995). Eye position influence on the parieto-occipital area PO (V6) of the macaque monkey. Eur. J. Neurosci. 7, 2486-2501.
41. Hafting, T., Fyhn, M., Molden, S., Moser, M. B., and Moser, E. I. (2005). Microstructure of a spatial map in the entorhinal cortex. Nature 436, 801-806.
42. Hannula, D. E., and Greene, A. (2012). The hippocampus re-evaluated in automatic and unconscious expressions of memory: at a tipping point? Front. Hum. Neurosci. 6:80. doi:10.3389/fnhum.2012.00080
43. Hartley, T., Bird, C. M., Chan, D., Cipolotti, L., Husain, M., Vargha-Khadem, F., and Burgess, N. (2007). The hippocampus is required for short-term topographical memory in humans. Hippocampus 17, 34-48.
44. Hartley, T., Burgess, N., Lever, C., Cacucci, F., and O'Keefe, J. (2000). Modeling place fields in terms of the cortical inputs to the hippocampus. Hippocampus 10, 369-379.
45. Hartley, T., Trinkler, I., and Burgess, N. (2004). Geometric determinants of human spatial memory. Cognition 94, 39-75.
46. Hassabis, D., Kumaran, D., and Maguire, E. A. (2007a). Using imagination to understand the neural basis of episodic memory. J. Neurosci. 27, 14365-14374.
47. Hassabis, D., Kumaran, D., Vann, S. D., and Maguire, E. A. (2007b). Patients with hippocampal amnesia cannot imagine new experiences. Proc. Natl. Acad. Sci. U.S.A. 104, 1726-1731.
48. Hayman, R., Verriotis, M. A., Jovalekic, A., Fenton, A. A., and Jeffery, K. J. (2011). Anisotropic encoding of three-dimensional space by place cells and grid cells. Nat. Neurosci. 14, 1182-1188.
49. Hirsch, R. (1974). The hippocampus and contextual retrieval of information from memory: a theory. Behav. Biol. 12, 421-444.
50. Holmes, E. A., and Bourne, C. (2008). Inducing and modulating intrusive emotional memories: a review of the trauma film paradigm. Acta Psychol. (Amst.) 127, 553-566.
51. Huxter, J., Burgess, N., and O'Keefe, J. (2003). Independent rate and temporal coding in hippocampal pyramidal cells. Nature 425, 828-832.
52. Jacobs, W. J., and Nadel, L. (1985). Stress-induced recovery of fears and phobias. Psychol. Rev. 92, 512-531.
53. Jeffery, K. J., Anderson, M. I., Hayman, R., and Chakraborty, S. (2004). A proposed architecture for the neural representation of spatial context. Neurosci. Biobehav. Rev. 28, 201-218.
54. Kim, J. J., and Diamond, D. M. (2002). The stressed hippocampus, synaptic plasticity and lost memories. Nat. Rev. Neurosci. 3, 453-462.
55. Kim, J. J., and Fanselow, M. S. (1992). Modality-specific retrograde amnesia of fear. Science 256, 675-677.
56. King, J. A., Burgess, N., Hartley, T., Vargha-Khadem, F., and O'Keefe, J. (2002). The human hippocampus and viewpoint dependence in spatial memory. Hippocampus 12, 811-820.
57. King, J. A., Trinkler, I., Hartley, T., Vargha-Khadem, F., and Burgess, N. (2004). The hippocampal role in spatial memory and the familiarity-recollection distinction: a single case study. Neuropsychology 18, 405-417.
58. Kinsbourne, M., and Wood, F. (1975). "Short-term memory and the amnesic syndrome," in Short term Memory, eds D. Deutsch, and J. A. Deutsch (New York, NY: Academic), 257-291.
59. Koenig, J., Linder, A. N., Leutgeb, J. K., and Leutgeb, S. (2011). The spatial periodicity of grid cells is not sustained during reduced theta oscillations. Science 332, 592-595.
60. LaBar, K. S., Gatenby, J. C., Gore, J. C., LeDoux, J. E., and Phelps, E. A. (1998). Human amygdala activation during conditioned fear acquisition and extinction: a mixed-trial fMRI study. Neuron 20, 937-945.
61. LeDoux, J. (1996). The Emotional Brain. New York, NY: Simon and Schuster.
62. Lee, A. C., Buckley, M. J., Pegman, S. J., Spiers, H. J., Scahill, V. R., Gaffan, D., Bussey, T. J., Davies, R. R., Kapur, N., Hodges, J. R., and Graham, K. S. (2005a). Specialisation in the medial temporal lobe for processing of objects and scenes. Hippocampus 15, 782-797.
63. Lee, A. C., Bussey, T. J., Murray, E. A., Saksida, L. M., Epstein, R. A., Kapur, N., Hodges, J. R., and Graham, K. S. (2005b). Perceptual deficits in amnesia: challenging the medial temporal lobe 'mnemonic' view. Neuropsychologia 43, 1-11.
64. Lee, A. C., Yeung, L., and Barense, M. D. (2012). The hippocampus and visual perception. Front. Hum. Neurosci. 6:91. doi:10.3389/fnhum.2012.00091
65. Leitz, J. R., Morgan, C. J., Bisby, J. A., Rendell, P. G., and Curran, H. V. (2009). Global impairment of prospective memory following acute alcohol. Psychopharmacology (Berl.) 205, 379-387.
66. Lenck-Santini, P. P., Save, E., and Poucet, B. (2001). Evidence for a relationship between place-cell spatial firing and spatial memory performance. Hippocampus 11, 377-390.
67. Lever, C., Burgess, N., Cacucci, F., Hartley, T., and O'Keefe, J. (2002). What can the hippocampal representation of environmental geometry tell us about Hebbian learning? Biol. Cybern. 87, 356-372.
68. Lever, C., Burton, S., Jeewajee, A., O'Keefe, J., and Burgess, N. (2009). Boundary vector cells in the subicu-lum of the hippocampal formation. J. Neurosci. 29, 9771-9777.
69. MacDonald, C. J., Lepage, K. Q., Eden, U. T., and Eichenbaum, H. (2011). Hippocampal "time cells" bridge the gap in memory for discontiguous events. Neuron 71, 737-749.
70. Manns, J. R., and Eichenbaum, H. (2009). A cognitive map for object memory in the hippocampus. Learn. Mem. 16, 616-624.
71. Marr, D. (1970). A theory for cerebral cortex. Proc. R. Soc. Lond B Biol. Sci. 176, 161-234.
72. Marr, D. (1971). Simple memory: a theory for archicortex. Philos. Trans. R. Soc. Lond B Biol. Sci. 262, 23-81.
73. Matthews, D. B., Simson, P. E., and Best, P. J. (1995). Acute ethanol impairs spatial memory but not stimulus/ response memory in the rat. Alcohol. Clin. Exp. Res. 19, 902-909.
74. Mayes, A., Montaldi, D., and Migo, E. (2007). Associative memory and the medial temporal lobes. Trends Cogn. Sci. 11, 126-135.
75. McClelland, J. L., McNaughton, B. L., and O'Reilly, R. C. (1995). Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connection-ist models of learning and memory. Psychol. Rev. 102, 419-457.
76. McNaughton, B. L., Battaglia, F. P., Jensen, O., Moser, E. I., and Moser, M. B. (2006). Path integration and the neural basis of the 'cognitive map'. Nat. Rev. Neurosci. 7, 663-678.
77. Morgan, L., MacEvoy, E., Aguirre, G., and Epstein, R. (2011). Distances between real-world locations are represented in the human hippocampus. J. Neurosci. 31, 1238-1245.
78. Moscovitch, M. (1995). "Models of consciousness and memory," in The Cognitive Neurosciences, ed M. Gazzaniga (Cambridge, MA: MIT Press), 1341-1356.
79. Muller, R. U., Bostock, E., Taube, J. S., and Kubie, J. L. (1994). On the directional firing properties of hip-pocampal place cells. J. Neurosci. 14, 7235-7251.
80. Muller, R. U., Kubie, J. L., and Ranck, J. B. Jr. (1987). Spatial firing patterns of hippocampal complex-spike cells in a fixed environment. J. Neurosci. 7, 1935-1950.
81. Muller, R. U., and Kubie, J. L. (1987). The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells. J. Neurosci. 7, 1951-1968.
82. Nakazawa, K., Quirk, M. C., Chitwood, R. A., Watanabe, M., Yeckel, M. F., Sun, L. D., Kato, A., Carr, C. A., Johnston, D., Wilson, M. A., and Tonegawa, S. (2002). Requirement for hippocampal CA3 NMDA receptors in associative memory recall. Science 297, 211-218.
83. Norman, K. A., and O'Reilly, R. C. (2003). Modeling hippocampal and neocortical contributions to recognition memory: a complementary-learning-systems approach. Psychol. Rev. 110, 611-646.
84. O'Keefe, J. (1976). Place units in the hippocampus of the freely moving rat. Exp. Neurol. 51, 78-109.
85. O'Keefe, J., and Burgess, N. (1996). Geometric determinants of the place fields of hippocampal neurons. Nature 381, 425-428.
86. O'Keefe, J., and Nadel, L. (1978). The Hippocampus as a Cognitive Map. Oxford: Oxford University Press.
87. O'Keefe, J., and Speakman, A. (1987). Single unit activity in the rat hippocampus during a spatial memory task. Exp. Brain Res. 68, 1-27.
88. Olsen, R. K., Moses, S. N., Riggs, L., and Ryan, J. D. (2012). The hippocampus supports multiple cognitive processes through relational binding and comparison. Front. Hum. Neurosci. 6:146. doi:10.3389/fnhum.2012.00146
89. O'Keefe, J., and Dostrovsky, J. (1971). The hippocampus as a spatial map: preliminary evidence from unit activity in the freely moving rat. Brain Res. 34, 171-175.
90. Payne, J. D., Jackson, E. D., Hoscheidt, S., Ryan, L., Jacobs, W. J., and Nadel, L. (2007). Stress administered prior to encoding impairs neutral but enhances emotional long-term episodic memories. Learn. Mem. 14, 861-868.
91. Recce, M., and Harris, K. D. (1996). Memory for places: a navigational model in support of Marr's theory of hippocampal function. Hippocampus 6, 735-748.
92. Redish, A. D., Rosenzweig, E. S., Bohanick, J. D., McNaughton, B. L., and Barnes, C. A. (2000). Dynamics of hippocampal ensemble activity realignment: time versus space. J. Neurosci. 20, 9298-9309.
93. Rolls, E. T., and Treves, A. (1997). Neural Networks and Brain Function. Oxford: Oxford University Press.
94. Samsonovich, A., and McNaughton, B. L. (1997). Path integration and cognitive mapping in a continuous attractor network model. J. Neurosci. 17, 5900-5920.
95. Save, E., Paz-Villagran, V., Alexinsky, T., and Poucet, B. (2005). Functional interaction between the associative parietal cortex and hippocampal place cell firing in the rat. Eur. J. Neurosci. 21, 522-530.
96. Schacter, D. L., Addis, D. R. and Buckner, R. L. (2007). Remembering the past to imagine the future: the prospective brain. Nat. Rev. Neurosci. 8, 657-661.
97. Shapiro, M. L., Tanila, H., and Eichenbaum, H. (1997). Cues that hippocampal place cells encode: dynamic and hierarchical representation of local and distal stimuli. Hippocampus 7, 624-642.
98. Smith, M. L., and Milner, B. (1981). The role of the right hippocampus in the recall of spatial location. Neuropsychologia 19, 781-793.
99. Snyder, L. H., Grieve, K. L., Brotchie, P., and Andersen, R. A. (1998). Separate body- and world-referenced representations of visual space in parietal cortex. Nature 394, 887-891.
100. Solstad, T., Boccara, C. N., Kropff, E., Moser, M. B., and Moser, E. I. (2008). Representation of geometric borders in the entorhinal cortex. Science 322, 1865-1868.
101. Squire, L. R., Stark, C. E., and Clark, R. E. (2004). The medial temporal lobe. Annu. Rev. Neurosci. 27, 279-306.
102. Squire, L. R., van der Horst, A. S., McDuff, S. G. R., Frascino, J. C., Hopkins, R. O., and Mauldin, K. N. (2010). Role of the hippocampus in remembering the past and imagining the future. Proc. Natl. Acad. Sci. U.S.A. 107, 19044-19048.
103. Sutherland, R. J., and Rudy, J. W. (1989). Configural association theory: the contribution of the hippocampus to learning, memory, and amnesia. Psychobiology 17, 129-144.
104. Taube, J. S. (1998). Head direction cells and the neuropsychological basis for a sense of direction. Prog. Neurobiol. 55, 225-256.
105. Teyler, T. J., and DiScenna, P. (1986). The hippocampal memory indexing theory. Behav. Neurosci. 100, 147-154.
106. Tolman, E. C. (1948). Cognitive maps in rats and men. Psychol. Rev. 55, 189-208.
107. Tsivilis, D., Vann, S. D., Denby, C., Roberts, N., Mayes, A. R., Montaldi, D., and Aggleton, J. P. (2008). A disproportionate role for the fornix and mammillary bodies in recall versus recognition memory. Nat. Neurosci. 11, 834-842.
108. Tulving, E. (1985). Memory and consciousness. Can. Psychol. 26, 1-12.
109. Vargha-Khadem, F., Gadian, D. G., Watkins, K. E., Connelly, A., van Paesschen, W., and Mishkin, M. (1997). Differential effects of early hippocampal pathology on episodic and semantic memory. Science 277, 376-380.
110. White, A. M., Elek, T. M., Beltz, T. L., and Best, P. J. (1998). Spatial performance is more sensitive to ethanol than nonspatial performance regardless of cue proximity. Alcohol. Clin. Exp. Res. 22, 2102-2107.
111. Wills, T., Lever, C., Cacucci, F., Burgess, N., and O'Keefe, J. (2005). Attractor dynamics in the hip-pocampal representation of the local environment. Science 308, 873-876.
112. Zeithamova, D., Schlichting, M. L., and Preston, A. R. (2012). The hippocampus and inferential reasoning: building memories to navigate future decisions. Front. Hum. Neurosci. 6:70. doi:10.3389/fnhum.2012.00070
113. Zhang, K. (1996). Representation of spatial orientation by intrinsic dynamics of the head-direction cell ensemble: a theory. J. Neurosci. 16, 2112-2126.