Attention promotes episodic encoding by stabilizing hippocampal representations

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 4, 2016, Pages E420-E429

  Aly, Mariam ^a   Turk Browne, Nicholas B ^a  

^a PRINCETON UNIVERSITY   (United States)

Author keywords

Hippocampal subfields; Long term memory; Medial temporal lobe; Representational stability; Selective attention

Indexed keywords

ADULT; ARTICLE; ATTENTION; ELECTROENCEPHALOGRAM; EPISODIC MEMORY; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HIPPOCAMPUS; HUMAN; HUMAN EXPERIMENT; MALE; MEDIAL TEMPORAL LOBE; MEMORY TEST; NEUROMODULATION; NORMAL HUMAN; PAINTING; PRIORITY JOURNAL; TASK PERFORMANCE; ART; ASSOCIATION; BRAIN CORTEX; EYE FIXATION; MOTIVATION; NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE IMAGING; PATTERN RECOGNITION; PHYSIOLOGY; SACCADIC EYE MOVEMENT; SHORT TERM MEMORY; VISION; YOUNG ADULT;

ADULT; ART; ATTENTION; CEREBRAL CORTEX; CUES; FEMALE; FIXATION, OCULAR; GOALS; HIPPOCAMPUS; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MEMORY, EPISODIC; MEMORY, SHORT-TERM; NEUROIMAGING; PATTERN RECOGNITION, VISUAL; SACCADES; VISUAL PERCEPTION; YOUNG ADULT;

EID: 84955466987     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1518931113     Document Type: Article

References (60)

1. Chun MM, Golomb JD, Turk-Browne NB (2011) A taxonomy of external and internal attention. Annu Rev Psychol 62:73-101.
2. Maunsell JHR, Treue S (2006) Feature-based attention in visual cortex. Trends Neurosci 29(6):317-322.
3. Chun MM, Turk-Browne NB (2007) Interactions between attention and memory. Curr Opin Neurobiol 17(2):177-184.
4. Carr VA, Engel SA, Knowlton BJ (2013) Top-down modulation of hippocampal encoding activity as measured by high-resolution functional MRI. Neuropsychologia 51(10):1829-1837.
5. Davachi L, Wagner AD (2002) Hippocampal contributions to episodic encoding: Insights from relational and item-based learning. J Neurophysiol 88(2):982-990.
6. Kensinger EA, Clarke RJ, Corkin S (2003) What neural correlates underlie successful encoding and retrieval? A functional magnetic resonance imaging study using a divided attention paradigm. J Neurosci 23(6):2407-2415.
7. Uncapher MR, Rugg MD (2009) Selecting for memory? The influence of selective attention on the mnemonic binding of contextual information. J Neurosci 29(25):8270-8279.
8. Desimone R, Duncan J (1995) Neural mechanisms of selective visual attention. Annu Rev Neurosci 18:193-222.
9. Gilbert CD, Li W (2013) Top-down influences on visual processing. Nat Rev Neurosci 14(5):350-363.
10. Aly M, Turk-Browne NB (2015) Attention stabilizes representations in the human hippocampus. Cereb Cortex, 10.1093/cercor/bhv041.
11. Dudukovic NM, Preston AR, Archie JJ, Glover GH, Wagner AD (2011) High-resolution fMRI reveals match enhancement and attentional modulation in the human medial temporal lobe. J Cogn Neurosci 23(3):670-682.
12. O'Craven KM, Downing PE, Kanwisher N (1999) fMRI evidence for objects as the units of attentional selection. Nature 401(6753):584-587.
13. Muzzio IA, Kentros C, Kandel E (2009) What is remembered? Role of attention on the encoding and retrieval of hippocampal representations. J Physiol 587(Pt 12):2837-2854.
14. Rowland DC, Kentros CG (2008) Potential anatomical basis for attentional modulation of hippocampal neurons. Ann N Y Acad Sci 1129:213-224.
15. Jackson J, Redish AD (2007) Network dynamics of hippocampal cell-assemblies resemble multiple spatial maps within single tasks. Hippocampus 17(12):1209-1229.
16. Kelemen E, Fenton AA (2010) Dynamic grouping of hippocampal neural activity during cognitive control of two spatial frames. PLoS Biol 8(6):e1000403.
17. Fenton AA, et al. (2010) Attention-like modulation of hippocampus place cell discharge. J Neurosci 30(13):4613-4625.
18. 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(2):283-295.
19. Muzzio IA, et al. (2009) Attention enhances the retrieval and stability of visuospatial and olfactory representations in the dorsal hippocampus. PLoS Biol 7(6):e1000140.
20. Holdstock JS, et al. (2002) Under what conditions is recognition spared relative to recall after selective hippocampal damage in humans? Hippocampus 12(3):341-351.
21. Norman KA, O'Reilly RC (2003) Modeling hippocampal and neocortical contributions to recognition memory: A complementary-learning-systems approach. Psychol Rev 110(4):611-646.
22. Kim G, Lewis-Peacock JA, Norman KA, Turk-Browne NB (2014) Pruning of memories by context-based prediction error. Proc Natl Acad Sci USA 111(24):8997-9002.
23. Wagner AD, et al. (1998) Building memories: Remembering and forgetting of verbal experiences as predicted by brain activity. Science 281(5380):1188-1191.
24. Eldridge LL, Engel SA, Zeineh MM, Bookheimer SY, Knowlton BJ (2005) A dissociation of encoding and retrieval processes in the human hippocampus. J Neurosci 25(13): 3280-3286.
25. Suthana NA, et al. (2015) High-resolution 7-Tesla fMRI of human hippocampal subfields during associative learning. J Cogn Neurosci 27(6):1194-1206.
26. Zeineh MM, Engel SA, Thompson PM, Bookheimer SY (2003) Dynamics of the hippocampus during encoding and retrieval of face-name pairs. Science 299(5606): 577-580.
27. Wolosin SM, Zeithamova D, Preston AR (2013) Distributed hippocampal patterns that discriminate reward context are associated with enhanced associative binding. J Exp Psychol Gen 142(4):1264-1276.
28. Duncan K, Ketz N, Inati SJ, Davachi L (2012) Evidence for area CA1 as a match/mismatch detector: A high-resolution fMRI study of the human hippocampus. Hippocampus 22(3): 389-398.
29. Elfman KW, Aly M, Yonelinas AP (2014) Neurocomputational account of memory and perception: Thresholded and graded signals in the hippocampus. Hippocampus 24(12):1672-1686.
30. Hasselmo ME, Wyble BP (1997) Free recall and recognition in a network model of the hippocampus: Simulating effects of scopolamine on human memory function. Behav Brain Res 89(1-2):1-34.
31. Carr VA, Rissman J, Wagner AD (2010) Imaging the human medial temporal lobe with high-resolution fMRI. Neuron 65(3):298-308.
32. Yassa MA, Stark CEL (2011) Pattern separation in the hippocampus. Trends Neurosci 34(10):515-525.
33. Bonnici HM, et al. (2012) Multi-voxel pattern analysis in human hippocampal subfields. Front Hum Neurosci 6:Article 290.
34. Chadwick MJ, Bonnici HM, Maguire EA (2014) CA3 size predicts the precision of memory recall. Proc Natl Acad Sci USA 111(29):10720-10725.
35. Diana RA, Yonelinas AP, Ranganath C (2007) Imaging recollection and familiarity in the medial temporal lobe: A three-component model. Trends Cogn Sci 11(9):379-386.
36. Yonelinas AP, Aly M, Wang W-C, Koen JD (2010) Recollection and familiarity: Examining controversial assumptions and new directions. Hippocampus 20(11):1178-1194.
37. LaRocque KF, et al. (2013) Global similarity and pattern separation in the human medial temporal lobe predict subsequent memory. J Neurosci 33(13):5466-5474.
38. Watanabe T, et al. (2011) Prediction of subsequent recognition performance using brain activity in the medial temporal lobe. Neuroimage 54(4):3085-3092.
39. Xue G, et al. (2010) Greater neural pattern similarity across repetitions is associated with better memory. Science 330(6000):97-101.
40. Brewer JB, Zhao Z, Desmond JE, Glover GH, Gabrieli JDE (1998) Making memories: brain activity that predicts how well visual experience will be remembered. Science 281(5380):1185-1187.
41. Coutanche MN, Thompson-Schill SL (2013) Informational connectivity: Identifying synchronized discriminability of multi-voxel patterns across the brain. Front Hum Neurosci 7:Article 15.
42. Kriegeskorte N, Mur M, Bandettini P (2008) Representational similarity analysis- Connecting the branches of systems neuroscience. Front Hum Neurosci 2:Article 4.
43. Rissman J, Wagner AD (2012) Distributed representations in memory: Insights from functional brain imaging. Annu Rev Psychol 63:101-128.
44. Kuhl BA, Rissman J, Wagner AD (2012) Multi-voxel patterns of visual category representation during episodic encoding are predictive of subsequent memory. Neuropsychologia 50(4):458-469.
45. Summerfield C, Egner T (2009) Expectation (and attention) in visual cognition. Trends Cogn Sci 13(9):403-409.
46. Copara MS, et al. (2014) Complementary roles of human hippocampal subregions during retrieval of spatiotemporal context. J Neurosci 34(20):6834-6842.
47. Bakker A, Kirwan CB, Miller M, Stark CEL (2008) Pattern separation in the human hippocampal CA3 and dentate gyrus. Science 319(5870):1640-1642.
48. Epstein RA (2008) Parahippocampal and retrosplenial contributions to human spatial navigation. Trends Cogn Sci 12(10):388-396.
49. Lee ACH, Yeung L-K, Barense MD (2012) The hippocampus and visual perception. Front Hum Neurosci 6(91):91.
50. Ranganath C, Ritchey M (2012) Two cortical systems for memory-guided behaviour. Nat Rev Neurosci 13(10):713-726.
51. Vann SD, Aggleton JP, Maguire EA (2009) What does the retrosplenial cortex do? Nat Rev Neurosci 10(11):792-802.
52. 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(2):340-375.
53. Epstein RA, Parker WE, Feiler AM (2007) Where am I now? Distinct roles for parahippocampal and retrosplenial cortices in place recognition. J Neurosci 27(23):6141-6149.
54. Park S, Chun MM (2009) Different roles of the parahippocampal place area (PPA) and retrosplenial cortex (RSC) in panoramic scene perception. Neuroimage 47(4):1747-1756.
55. Aly M, Ranganath C, Yonelinas AP (2013) Detecting changes in scenes: The hippocampus is critical for strength-based perception. Neuron 78(6):1127-1137.
56. Zeidman P, Mullally SL, Maguire EA (2015) Constructing, perceiving, and maintaining scenes: Hippocampal activity and connectivity. Cereb Cortex 25(10):3836-3855.
57. Smith SM, Nichols TE (2009) Threshold-free cluster enhancement: Addressing problems of smoothing, threshold dependence and localisation in cluster inference. Neuroimage 44(1):83-98.
58. Efron B, Tibshirani R (1986) Bootstrap methods for standard errors, confidence intervals, and other measures of statistical accuracy. Stat Sci 1(1):54-77.
59. Kimmig H, et al. (2001) Relationship between saccadic eye movements and cortical activity as measured by fMRI: Quantitative and qualitative aspects. Exp Brain Res 141(2):184-194.
60. Pernet CR, Wilcox R, Rousselet GA (2012) Robust correlation analyses: False positive and power validation using a new open source Matlab toolbox. Front Psychol 3:606.