Contributions of medial temporal lobe and striatal memory systems to learning and retrieving overlapping spatial memories

Cerebral Cortex

Volumn 24, Issue 7, 2014, Pages 1906-1922

  Brown, Thackery I ^a,b   Stern, Chantal E ^a,b  

^a BOSTON UNIVERSITY   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

caudate; fMRI; hippocampus; navigation; parahippocampal

Indexed keywords

ADULT; ARTICLE; ASSOCIATION; BEHAVIOR; BRAIN REGION; CAUDATE NUCLEUS; CLINICAL ARTICLE; CORPUS STRIATUM; ECHO PLANAR IMAGING; FEMALE; FOLLOW UP; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HIPPOCAMPUS; HUMAN; LEARNING; LEARNING CURVE; MALE; MAZE TEST; MEDIAL CAUDATE; MEDIAL TEMPORAL LOBE; NUCLEAR MAGNETIC RESONANCE SCANNER; NUCLEUS ACCUMBENS; PARAHIPPOCAMPAL CORTEX; PRIORITY JOURNAL; RECOGNITION; RESPONSE TIME; RETROSPLENIAL CORTEX; SPATIAL MEMORY; TASK PERFORMANCE; TEMPORAL LOBE; TRAINING; VIRTUAL REALITY; ADOLESCENT; ANALYSIS OF VARIANCE; BLOOD; BRAIN MAPPING; COMPUTER INTERFACE; IMAGE PROCESSING; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; RECALL; VASCULARIZATION; YOUNG ADULT;

OXYGEN;

ADOLESCENT; ANALYSIS OF VARIANCE; BRAIN MAPPING; CORPUS STRIATUM; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MAZE LEARNING; MENTAL RECALL; OXYGEN; SPATIAL MEMORY; TEMPORAL LOBE; USER-COMPUTER INTERFACE; YOUNG ADULT;

EID: 84902492050     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bht041     Document Type: Article

References (65)

1. Addis DR, Wong AT, Schacter DL. 2007. Remembering the past and imagining the future: Common and distinct neural substrates during even construction and elaboration. Neuropsychologia. 45:1363-1377.
2. Agster KL, Fortin NJ, Eichenbaum H. 2002. The hippocampus and disambiguation of overlapping sequences. J Neurosci. 22:5760-5768.
3. Andersson JL, Hutton C, Ashburner J, Turner R, Friston K. 2001. Modeling geometric deformations in EPI time series. Neuroimage. 13:903-919.
4. Ashburner J. 2007. A fast diffeomorphic image registration algorithm. Neuroimage. 38:95-113.
5. Bar M, Aminoff E. 2003. Cortical analysis of visual context. Neuron. 38:347-358.
6. Brown TI, Ross RS, Keller JB, Hasselmo ME, Stern CE. 2010. Which way was I going? Contextual retrieval supports the disambiguation of well learned overlapping navigational routes. J Neurosci. 30:7414-7422.
7. Brown TI, Ross RS, Tobyne SM, Stern CE. 2012. Cooperative interactions between hippocampal and striatal systems support flexible navigation. Neuroimage. 60:1316-1330.
8. Burgess N, Maguire EA, Spiers HJ, O'Keefe J. 2001. A temporoparietal and prefrontal network for retrieving the spatial context of lifelike events. Neuroimage. 14:439-453.
9. Davachi L. 2006. Item, context and relational episodic encoding in humans. Curr Opin Neurobiol. 16:693-700.
10. Davachi L, Mitchell JP, Wagner AD. 2003. Multiple routes to memory: distinct medial temporal lobe processes build item and source memories. Proc Natl Acad Sci USA. 100:2157-2162.
11. Davidson TJ, Kloosterman F, Wilson MA. 2009. Hippocampal replay of extended experience. Neuron. 63:497-507.
12. DeCoteau W, Thorn C, Gibson DJ, Courtemanche R, Mitra P, Kubota Y, Graybiel AM. 2007. Learning-related coordination of striatal and hippocampal theta rhythms during acquisition of a procedural maze task. Proc Natl Acad Sci USA. 104:5644-5649.
13. Devan BD, White NM. 1999. Parallel information processing in the dorsal striatum: Relation to hippocampal function. J Neurosci. 19:2789-2798.
14. Eichenbaum H, Sauvage M, Fortin N, Komorowski R, Lipton P. 2011. Towards a functional organization of episodic memory in the medial temporal lobe. Neurosci Biobehav Rev. 36:1597-1608.
15. Eichenbaum H, Yonelinas AP, Ranganath C. 2007. The medial temporal lobe and recognition memory. Ann Rev Neurosci. 30:123-152.
16. Ekstrom AD, Bookheimer SY. 2007. Spatial and temporal episodic memory retrieval recruit dissociable functional networks in the human brain. Learn Mem. 14:645-654.
17. Epstein R, Higgins JS. 2007. Differential parahippocampal and retrosplenial involvement in three types of visual scene recognition. Cereb Cortex. 17:1680-1693.
18. Epstein R, Kanwisher N. 1998. A cortical representation of the local visual environment. Nature. 392:598-601.
19. Epstein RA, Parker WE, Feiler AM. 2007. Where am I now? Distinct roles for parahippocampal and retrosplenial cortices in place recognition. J Neurosci. 27:6141-6149.
20. Fanselow MS, Dong HW. 2010. Are the dorsal and ventral hippocampus functionally distinct structures? Neuron. 65:7-19.
21. Ferbinteanu J, Shapiro ML. 2003. Prospective and retrospective memory coding in the hippocampus. Neuron. 40:1227-1239.
22. Foster DJ, Knierim JJ. 2011. Sequence learning and the role of the hippocampus in rodent navigation. Curr Opin Neurobiol. 22:1-7.
23. Ginther MR, Walsh DF, Ramus SJ. 2011. Hippocampal neurons encode different episodes in an overlapping sequence of odors task. J Neurosci. 31:2706-2711.
24. Graham S, Phua E, Soon CS, Oh T, Au C, Shuter B, Wang SC, Yeh IB. 2009. Role of medial cortical, hippocampal and striatal interactions during cognitive set-shifting. Neuroimage. 45:1359-1367.
25. Gupta AS, van der Meer MAA, Touretzky DS, Redish AD. 2010. Hippocampal replay is not a simple function of experience. Neuron. 65:695-705.
26. Hartley T, Maguire EA, Spiers HJ, Burgess N. 2003. The well-worn route and the path less traveled: Distinct neural bases of route following and wayfinding in humans. Neuron. 37:877-888.
27. Hassabis D, Kumaran D, Maguire EA. 2007. Using imagination to understand the neural basis of episodic memory. J Neurosci. 27:14365-14374.
28. Hasselmo ME. 2009. A model of episodic memory: mental time travel along encoded trajectories using grid cells. Neurobiol Learn Mem. 92:559-573.
29. Hasselmo ME, Eichenbaum H. 2005. Hippocampal mechanisms for the context-dependent retrieval of episodes. Neural Netw. 18:1172-1190.
30. Howard LR, Kumaran D, Olafsdottir HF, Spiers HJ. 2011. Double dissociation between hippocampal and parahippocampal responses to object-background context and scene novelty. J Neurosci. 31:5253-5261.
31. Hupbach A, Gomez R, Hardt O, Nadel L. 2007. Reconsolidation of episodic memories: A subtle reminder triggers integration of new information. Learn Mem. 14:47-53.
32. Hupbach A, Hardt O, Gomez R, Nadel L. 2008. The dynamics of memory: Context-dependent updating. Learn Mem. 15:574-579.
33. Janzen G, van Turennout M. 2004. Selective neural representation of objects relevant for navigation. Nat Neurosci. 7:673-677.
34. Jenkins LJ, Ranganath C. 2010. Prefrontal and medial temporal lobe activity at encoding predicts temporal context memory. J Neurosci. 30:15558-15565.
35. Johnson A, Redish AD. 2007. Neural ensembles in CA3 transiently encode paths forward of the animal at a decision point. J Neurosci. 27:12176-12189.
36. Johnson A, van der Meer MAA, Redish AD. 2007. Integrating hippocampus and striatum in decision-making. Curr Opin Neurobiol. 17:692-697.
37. Kuhl BA, Shah AT, DuBrow S, Wagner AD. 2010. Resistance to forgetting associated with hippocampus-mediated reactivation during new learning. Nat Neurosci. 13:501-506.
38. Kumaran D, Maguire EA. 2006. The dynamics of hippocampal activation during encoding of overlapping sequences. Neuron. 49:617-629.
39. Lee I, Griffin AL, Zilli EA, Eichenbaum H, Hasselmo ME. 2006. Gradual translocation of spatial correlates of neuronal firing in the hippocampus toward prospective reward locations. Neuron. 51:639-650.
40. MacDonald CJ, Lepage KQ, Eden UT, Eichenbaum H. 2011. Hippocampal "time cells" bridge the gap in memory for discontiguous events. Neuron. 71:737-749.
41. Maldjian JA, Laurienti PJ, Burdette JH. 2004. Precentral gyrus discrepancy in electronic versions of the Talairach Atlas. Neuroimage. 21:450-455.
42. Maldjian JA, Laurienti PJ, Kraft RA, Burdette JH. 2003. An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage. 19:1233-1239.
43. Monchi O, Petrides M, Petre V, Worsley K, Dagher A. 2001. Wisconsin card sorting revisited: Distinct neural circuits participating in different stages of the task identified by event-related functional magnetic resonance imaging. J Neurosci. 21:7733-7741.
44. Monchi O, Petrides M, Strafella AP, Worsley KJ, Doyon J. 2006. Functional role of the basal ganglia in the planning and execution of novel actions. Ann Neurol. 59:257-264.
45. Mullally SL, Maguire EA. 2011. A new role for the parahippocampal cortex in representing space. J Neurosci. 31:7441-7449.
46. O'Craven KM, Kanwisher N. 2000. Mental imagery of faces and places activates corresponding stimulus-specific brain regions. J Cogn Neurosci. 12:1013-1023.
47. Pasupathy A, Miller EK. 2005. Different time courses of learning-related activity in the prefrontal cortex and striatum. Nature. 433:873-876.
48. Ragozzino ME, Jih J, Tzavos A. 2002. Involvement of the dorsomedial striatum in behavioral flexibility: Role of muscarinic cholinergic receptors. Brain Res. 953:205-214.
49. Ranganath C, Yonelinas AP, Cohen MX, Dy CJ, Tom SM, D'Esposito M. 2003. Dissociable correlates of recollection and familiarity within the medial temporal lobes. Neuropsychologia. 42:2-13.
50. Rosenbaum RS, Ziegler M, Winocur G, Grady CL, Moscovitch M. 2004. "I Have Often Walked Down This Street Before": fMRI studies on the hippocampus and other structures during mental navigation of an old environment. Hippocampus. 14:826-835.
51. Ross RS, Brown TI, Stern CE. 2009. The retrieval of learned sequences engages the hippocampus: Evidence from fMRI. Hippocampus. 19:790-799.
52. Ross RS, Slotnick SD. 2008. The hippocampus is preferentially associated with memory for spatial context. J Cogn Neurosci. 20:432-446.
53. Sederberg PB, Gershman SJ, Polyn SM, Norman KA. 2011. Human memory reconsolidation can be explained using the temporal context model. Psychon Bull Rev. 18:455-468.
54. Shohamy D, Wagner AD. 2008. Integrating memories in the human brain: hippocampal-midbrain encoding of overlapping events. Neuron. 60:378-389.
55. Smith DM, Mizumori SJY. 2006. Learning-related development of context-specific neuronal responses to places and events: The hippocampal role in context processing. J Neurosci. 26: 3154-3163.
56. Thorn CA, Atallah H, Howe M, Graybiel AM. 2010. Differential dynamics of activity changes in dorsolateral and dorsomedial striatal loops during learning. Neuron. 66:781-795.
57. Tronson NC, Taylor JR. 2007. Molecular mechanisms of memory reconsolidation. Nat Rev Neurosci. 8:262-275.
58. Turk-Browne NB, Simon MG, Sederberg PB. 2012. Scene representations in parahippocampal cortex depend on temporal context. J Neurosci. 32:7202-7207.
59. Turnock M, Becker S. 2008. A neural network model of hippocampal- striatal-prefrontal interactions in contextual conditioning. Brain Res. 1202:87-98.
60. Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, Mazoyer B, Joliot M. 2002. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage. 15:273-89.
61. 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. 27:623-633.
62. Xue G, Ghahremani DG, Poldrack RA. 2008. Neural substrates for reversing stimulus-outcome and stimulus-response associations. J Neurosci. 28:11196-11204.
63. Yin HH, Knowlton BJ. 2004. Contributions of striatal subregions to place and response learning. Learn Mem. 11:459-463.
64. Yin HH, Knowlton BJ. 2006. The role of the basal ganglia in habit formation. Nat Rev Neurosci. 7:464-476.
65. Zilli EA, Hasselmo ME. 2008. Modeling the role of working memory and episodic memory in behavioral tasks. Hippocampus. 18:193-209.