Multiple neural states of representation in short-term memory? It's a matter of attention

Frontiers in Human Neuroscience

Volumn 8, Issue JAN, 2014, Pages

  LaRocque, Joshua J ^a   Lewis Peacock, Jarrod A ^b   Postle, Bradley R ^c  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^c UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

Attention; Multivariate pattern analysis; Representational states; Short term memory; Unattended memory items

Indexed keywords

ACCURACY; ATTENTION; AWARENESS; BEHAVIOR; ELECTROENCEPHALOGRAPHY; FOCUS OF ATTENTION; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; LONG TERM MEMORY; MEMORY CONSOLIDATION; REVIEW; SHORT TERM MEMORY; STIMULUS RESPONSE; THEORETICAL MODEL; VISUAL MEMORY; WORKING MEMORY;

EID: 84892951104     PISSN: 16625161     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnhum.2014.00005     Document Type: Review

References (91)

1. Aguirre, G. K., Zarahn, E., and D'Esposito, M. (1998). An area within human ventral cortex sensitive to "building" stimuli: evidence and implications. Neuron 21, 373-383. doi: 10.1016/s0896-6273(00)80546-2
2. Atkinson, R. C., and Shiffrin, R. M. (1968). "Human memory: a proposed system and its control processes, " in The Psychology of Learning and Motivation: Advances in Research and Theory (Vol. 2), eds K. W. Spence and J. T. Spence (New York: Academic Press), 89-195.
3. Baars, B. J., and Franklin, S. (2003). How conscious experience and working memory interact. Trends Cogn. Sci. 7, 166-172. doi: 10.1016/s1364-6613(03)00056-1
4. Baddeley, A. (2003). Working memory: looking back and looking forward. Nat. Rev. Neurosci. 4, 829-839. doi: 10.1038/nrn1201
5. Baddeley, A. D., and Hitch, G. (1974). "Working memory, " in Psychology of Learning and Motivation: Advances in Research and Theory (Vol. 8), ed H. B. Gordon (New York: Academic Press), 47-89.
6. Buchsbaum, B. R. (2013). The role of consciousness in the phonological loop: hidden in plain sight. Front. Psychol. 4:496. doi: 10.3389/fpsyg.2013.00496
7. Carlisle, N. B., Arita, J. T., Pardo, D., and Woodman, G. F. (2011). Attentional templates in visual working memory. J. Neurosci. 31, 9315-9322. doi: 10.1523/jneurosci.1097-11.2011
8. Cohen, M. A., Alvarez, G. A., and Nakayama, K. (2011). Natural-scene perception requires attention. Psychol. Sci. 22, 1165-1172. doi: 10.1177/0956797611419168
9. Cowan, N. (1988). Evolving conceptions of memory storage, selective attention and their mutual constraints within the human information-processing system. Psychol. Bull. 104, 163-191. doi: 10.1037//0033-2909.104.2.163
10. Cowan, N. (1995). Attention and Memory: An Integrated Framework. New York: Oxford University Press.
11. Curtis, C. E., and D'Esposito, M. (2003). Persistent activity in the prefrontal cortex during working memory. Trends Cogn. Sci. 7, 415-423. doi: 10.1016/s1364-6613(03)00197-9
12. D'Esposito, M., Postle, B. R., and Rypma, B. (2000). Prefrontal cortical contributions to working memory: evidence from event-related fMRI studies. Exp. Brain Res. 133, 3-11. doi: 10.1007/978-3-642-59794-7_2
13. Davis, T., and Poldrack, R. A. (2013). Measuring neural representations with fMRI: practices and pitfalls. Ann. N Y Acad. Sci. 1296, 108-134. doi: 10.1111/nyas.12156
14. Drew, T., Horowitz, T. S., Wolfe, J. M., and Vogel, E. K. (2011). Delineating the neural signatures of tracking spatial position and working memory during attentive tracking. J. Neurosci. 31, 659-668. doi: 10.1523/jneurosci.1339-10.2011
15. Drew, T., and Vogel, E. (2008). Neural measures of individual differences in selecting and tracking multiple moving objects. J. Neurosci. 28, 4183-4191. doi: 10.1523/jneurosci.0556-08.2008
16. Edelman, G. M. (1989). The Remembered Present: A Biological Theory of Consciousness. New York: Basic Books.
17. Emrich, S. M., Al-Aidroos, N., Pratt, J., and Ferber, S. (2009). Visual search elicits the electrophysiological marker of visual working memory. PloS One 4:e8042. doi: 10.1371/journal.pone.0008042
18. Emrich, S. M., Riggall, A. C., LaRocque, J. J., and Postle, B. R. (2013). Distributed patterns of activity in sensory cortex reflect the precision of multiple items maintained in visual short-term memory. J. Neurosci. 33, 6516-6523. doi: 10.1523/jneurosci.1772-13.2013
19. Erickson, M. A., Maramara, L. A., and Lisman, J. (2009). A single brief burst induces GluR1-dependent associative short-term potentiation: a potential mechanism for short-term memory. J. Cogn. Neurosci. 22, 2530-2540. doi: 10.1162/jocn.2009.21375
20. Ester, E. F., Anderson, D. E., Serences, J. T., and Awh, E. (2013). A neural measure of precision in visual working memory. J. Cogn. Neurosci. 25, 754-761. doi: 10.1162/jocn_a_00357
21. Fuentemilla, L., Penny, W. D., Cashdollar, N., Bunzeck, N., and Duzel, E. (2010). Theta-coupled periodic replay in working memory. Curr. Biol. 20, 606-612. doi: 10.1016/j.cub.2010.01.057
22. Funahashi, S., Bruce, C. J., and Goldman-Rakic, P. S. (1989). Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex. J. Neurophysiol. 61, 331-349.
23. Fuster, J. M. (2003). More than working memory rides on long-term memory. Behav. Brain Sci. 26, 737. doi: 10.1017/s0140525x03300160
24. Griffin, I. C., and Nobre, A. C. (2003). Orienting attention to locations in internal representations. J. Cogn. Neurosci. 15, 1176-1194. doi: 10.1162/089892903322598139
25. Han, X., Berg, A. C., Oh, H., Samaras, D., and Leung, H.-C. (2013). Multi-voxel pattern analysis of selective representation of visual working memory in ventral temporal and occipital regions. Neuroimage 73, 8-15. doi: 10.1016/j.neuroimage.2013.01.055
26. Harrison, S. A., and Tong, F. (2009). Decoding reveals the contents of visual working memory in early visual areas. Nature 458, 632-635. doi: 10.1038/nature07832
27. Haxby, J. V., Gobbini, M. I., Furey, M. L., Ishai, A., Schouten, J. L., and Pietrini, P. (2001). Distributed and overlapping representations of faces and objects in ventral temporal cortex. Science 293, 2425-2430. doi: 10.1126/science.1063736
28. Haynes, J.-D., and Rees, G. (2006). Decoding mental states from brain activity in humans. Nat. Rev. Neurosci. 7, 523-534. doi: 10.1038/nrn1931
29. Hebb, D. O. (1949). The Organization of Behavior: A Neuropsychological Theory (p. 335). New York: Wiley.
30. Ikkai, A., McCullough, A. W., and Vogel, E. K. (2010). Contralateral delay activity provides a neural measure of the number of representations in visual working memory. J. Neurophysiol. 103, 1963-1968. doi: 10.1152/jn.00978.2009
31. Jafarpour, A., Horner, A. J., Fuentemilla, L., Penny, W. D., and Duzel, E. (2013). Decoding oscillatory representations and mechanisms in memory. Neuropsychologia 51, 772-780. doi: 10.1016/j.neuropsychologia.2012.04.002
32. Jensen, O., and Tesche, C. D. (2002). Frontal theta activity in humans increases with memory load in a working memory task. Eur. J. Neurosci. 15, 1395-1399. doi: 10.1046/j.1460-9568.2002.01975.x
33. Kang, M., Hong, S., Blake, R., and Woodman, G. F. (2011). Visual working memory contaminates perception. Psychon. Bull. Rev. 18, 860-869. doi: 10.3758/s13423-011-0126-5
34. Kanwisher, N., McDermott, J., and Chun, M. M. (1997). The fusiform face area: a module in human extrastriate cortex specialized for face perception. J. Neurosci. 17, 4302-4311.
35. Koch, C., and Tsuchiya, N. (2006). Attention and conciousness: two distinct brain processes. Trends Cogn. Sci. 11, 16-22. doi: 10.1016/j.tics.2006.10.012
36. Kundu, B., Sutterer, D. W., Emrich, S. M., and Postle, B. R. (2013). Strengthened effective connectivity underlies transfer of working memory training to tests of short-term memory and attention. J. Neurosci. 33, 8705-8715. doi: 10.1523/jneurosci.2231-13.2013
37. LaRocque, J. J., Lewis-Peacock, J. A., Drysdale, A. T., Oberauer, K., and Postle, B. R. (2013). Decoding attended information in short-term memory: an EEG study. J. Cogn. Neurosci. 25, 127-142. doi: 10.1162/jocn_a_00305
38. Lee, S.-H., Kravitz, D. J., and Baker, C. I. (2013). Goal-dependent dissociation of visual and prefrontal cortices during working memory. Nat. Neurosci. 16, 997-999. doi: 10.1038/nn.3452
39. Lepsien, J., and Nobre, A. C. (2007). Attentional modulation of object representations in working memory. Cereb. Cortex 17, 2072-2083. doi: 10.1093/cercor/bhl116
40. Lewis-Peacock, J. A., Drysdale, A. T., Oberauer, K., and Postle, B. R. (2012). Neural evidence for a distinction between short-term memory and the focus of attention. J. Cogn. Neurosci. 24, 61-79. doi: 10.1162/jocn_a_00140
41. Lewis-Peacock, J. A., and Postle, B. R. (2008). Temporary activation of long-term memory supports working memory. J. Neurosci. 28, 8765-8771. doi: 10.1523/jneurosci.1953-08.2008
42. Lewis-Peacock, J. A., and Postle, B. R. (2012). Decoding the internal focus of attention. Neuropsychologia 50, 470-478. doi: 10.1016/j.neuropsychologia.2011.11.006
43. Linke, A. C., Vicente-Grabovetsky, A., and Cusack, R. (2011). Stimulus-specific suppression preserves information in auditory short-term memory. Proc. Natl. Acad. Sci. U S A 108, 12961-12966. doi: 10.1073/pnas.1102118108
44. Luck, S. J., and Sawaki, R. (2011). Active suppression of distractors that match the contents of visual working memory. Vis. Cogn. 19, 956-972. doi: 10.1080/13506285.2011.603709
45. Maier, A., Wilke, M., Aura, C., Zhu, C., Ye, F. Q., and Leopold, D. A. (2008). Divergence of fMRI and neural signals in V1 during perceptual suppression in the awake monkey. Nat. Neurosci. 11, 1193-1200. doi: 10.1038/nn.2173
46. Mccarthy, G., Puce, A., Gore, J. C., and Truett, A. (1996). Face-specific processing in the human fusiform gyrus. J. Cogn. Neurosci. 9, 605-610. doi: 10.1162/jocn.1997.9.5.605
47. McElree, B. (1996). Accessing short-term memory with semantic and phonological information: a time-course analysis. Mem. Cognit. 24, 173-187. doi: 10.3758/bf03200879
48. McElree, B. (1998). Attended and non-attended states in working memory: accessing categorized structures. J. Mem. Lang. 38, 225-252. doi: 10.1006/jmla.1997.2545
49. McElree, B. (2006). Accessing recent events. Psychol. Learn. Motiv. 46, 155-200. doi: 10.1016/s0079-7421(06)46005-9
50. McElree, B., and Dosher, B. (1989). Serial position and set size in short-term memory: the time course of recognition. J. Exp. Psychol. 18, 346-373. doi: 10.1037/0096-3445.118.4.346
51. Melloni, L., Schwiedrzik, C. M., Müller, N., Rodriguez, E., and Singer, W. (2011). Expectations change the signatures and timing of electrophysiological correlates of perceptual awareness. J. Neurosci. 31, 1386-1396. doi: 10.1523/jneurosci.4570-10.2011
52. Mongillo, G., Barak, O., and Tsodyks, M. (2008). Synaptic theory of working memory. Science 319, 1543-1546. doi: 10.1126/science.1150769
53. Nee, D. E., and Jonides, J. (2008). Neural correlates of access to short-term memory. Proc. Natl. Acad. Sci. U S A 105, 14228-14233. doi: 10.1073/pnas.0802081105
54. Nee, D. E., and Jonides, J. (2011). Dissociable contributions of prefrontal cortex and the hippocampus to short-term memory: evidence for a 3-state model of memory. Neuroimage 54, 1540-1548. doi: 10.1016/j.neuroimage.2010.09.002
55. Nee, D. E., and Jonides, J. (2013). Neural evidence for a 3-state model of visual short-term memory. Neuroimage 74, 1-11. doi: 10.1016/j.neuroimage.2013.02.019
56. Nelissen, N., Stokes, M. G., Nobre, A. C., and Rushworth, M. F. S. (2013). Frontal and parietal cortical interactions with distributed visual representations during selective attention and action selection. J. Neurosci. 33, 16443-16458. doi: 10.1523/JNEUROSCI.2625-13.2013
57. Nobre, A. C., Coull, J. T., Maquet, P., Frith, C. D., Vandenberghe, R., and Mesulam, M. M. (2004). Orienting attention to locations in perceptual versus mental representations. J. Cogn. Neurosci. 16, 363-373. doi: 10.1162/089892904322926700
58. Norman, K. A., Polyn, S. M., Detre, G., and Haxby, J. V. (2006). Beyond mind-reading: multi-voxel pattern analysis of fMRI data. Trends Cogn. Sci. 10, 424-430. doi: 10.1016/j.tics.2006.07.005
59. O'Reilly, R. C., Munakata, Y., Frank, M. J., Hazy, T. E., and Contributors. (2012). Computational Cognitive Neuroscience. 1st Edn., Wiki Book.
60. Oberauer, K. (2001). Removing irrelevant information from working memory: a cognitive aging study with the modified Sternberg task. J. Exp. Psychol. Learn. Mem. Cogn. 27, 948-957. doi: 10.1037/0278-7393.27.4.948
61. Oberauer, K. (2002). Access to information in working memory: exploring the focus of attention. J. Exp. Psychol. Learn. Mem. Cogn. 28, 411-421. doi: 10.1037/0278-7393.28.3.411
62. Oberauer, K. (2005). Control of the contents of working memory-a comparison of two paradigms and two age groups. J. Exp. Psychol. Learn. Mem. Cogn. 31, 714-728. doi: 10.1037/0278-7393.31.4.714
63. Oberauer, K. (2009). "Design for a working memory, " in The Psychology of Learning and Motivation (Vol. 51), 1st Edn., ed B. H. Ross (San Diego, CA: Academic Press), 45-100.
64. Oberauer, K. (2013). The focus of attention in working memory-from metaphors to mechanisms. Front. Hum. Neurosci. 7:673. doi: 10.3389/fnhum.2013.00673
65. Oberauer, K., and Hein, L. (2012). Attention to information in working memory. Curr. Dir. Psychol. Sci. 21, 164-169. doi: 10.1177/0963721412444727
66. 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
67. Oztekin, I., Davachi, L., and McElree, B. (2010). Are representations in working memory distinct from representations in long-term memory? Neural evidence in support of a single store. Psychol. Sci. 21, 1123-1133. doi: 10.1177/0956797610376651
68. Pasternak, T., and Greenlee, M. W. (2005). Working memory in primate sensory systems. Nat. Rev. Neurosci. 6, 97-107. doi: 10.1038/nrn1603
69. Peters, J. C., Roelfsema, P. R., and Goebel, R. (2012). Task-relevant and accessory items in working memory have opposite effects on activity in extrastriate cortex. J. Neurosci. 32, 17003-17011. doi: 10.1523/jneurosci.0591-12.2012
70. Postle, B. R. (2006). Working memory as an emergent property of the mind and brain. Neuroscience 139, 23-38. doi: 10.1016/j.neuroscience.2005.06.005
71. Postle, B. R. (in press). "Activation and information in working memory research, " in The Wiley-Blackwell Handbook on the Cognitive Neuroscience of Memory, eds A. Duarte, M. Barense and D. R. Addis (West Sussex, UK: Wiley-Blackwell), 897-901.
72. Ranganath, C., and Blumenfeld, R. S. (2005). Doubts about double dissociations between short-and long-term memory. Trends Cogn. Sci. 9, 374-380. doi: 10.1016/j.tics.2005.06.009
73. Rerko, L., and Oberauer, K. (2013). Focused, unfocused and defocused information in working memory. J. Exp. Psychol. Learn. Mem. Cogn. 39, 1075-1096. doi: 10.1037/a0031172
74. Riggall, A., and Postle, B. R. (2012). The relationship between working memory storage and elevated activity as measured with functional magnetic resonance imaging. J. Neurosci. 32, 12990-12998. doi: 10.1523/jneurosci.1892-12.2012
75. Rose, N. S., Olsen, R. K., Craik, F. I. M., and Rosenbaum, R. S. (2012). Working memory and amnesia: the role of stimulus novelty. Neuropsychologia 50, 11-18. doi: 10.1016/j.neuropsychologia.2011.10.016
76. Ruchkin, D. S., Grafman, J., Cameron, K., and Berndt, R. S. (2003). Working memory retention systems: a state of activated long-term memory. Behav. Brain Sci. 26, 709-728. discussion 728-777. doi: 10.1017/s0140525x03000165
77. Sanderson, D. J., Good, M. A., Skelton, K., Sprengel, R., Seeburg, P. H., Rawlins, J. N., et al. (2009). Enhanced long-term and impaired short-term spatial memory in GluA1 AMPA receptor subunit knockout mice: evidence for a dual-process memory model. Learn. Mem. 16, 379-386. doi: 10.1101/lm.1339109
78. Scocchia, L., Valsecchi, M., Gegenfurtner, K. R., and Triesch, J. (2013). Visual working memory contents bias ambiguous structure from motion perception. PloS One 8:e59217. doi: 10.1371/journal.pone.0059217
79. Serences, J. T., Ester, E. F., Vogel, E. K., and Awh, E. (2009). Stimulus-specific delay activity in human primary visual cortex. Psychol. Sci. 20, 207-214. doi: 10.1111/j.1467-9280.2009.02276.x
80. Simanova, I., van Gerven, M., Oostenveld, R., and Hagoort, P. (2010). Identifying object categories from event-related EEG: toward decoding of conceptual representations. PloS One 5:e14465. doi: 10.1371/journal.pone.0014465
81. Soto, D., Mäntylä, T., and Silvanto, J. (2011). Working memory without consciousness. Curr. Biol. 21, R912-R913. doi: 10.1016/j.cub.2011.09.049
82. Stokes, M. G., Kusunoki, M., Sigala, N., Nili, H., Gaffan, D., and Duncan, J. (2013). Dynamic coding for cognitive control in prefrontal cortex. Neuron 78, 364-375. doi: 10.1016/j.neuron.2013.01.039
83. Sugase-Miyamoto, Y., Liu, Z., Wiener, M. C., Optican, L. M., and Richmond, B. J. (2008). Short-term memory trace in rapidly adapting synapses of inferior temporal cortex. PLoS Comput. Biol. 4:e1000073. doi: 10.1371/journal.pcbi.1000073
84. Talmi, D., Grady, C. L., Goshen-Gottstein, Y., and Moscovitch, M. (2005). Neuroimaging the serial position curve. A test of single-store versus dual-store models. Psychol. Sci. 16, 716-723. doi: 10.1111/j.1467-9280.2005.01601.x
85. Todd, J. J., and Marois, R. (2004). Capacity limit of visual short-term memory in human posterior parietal cortex. Nature 428, 751-754. doi: 10.1038/nature02466
86. Tong, F., and Pratte, M. S. (2012). Decoding patterns of human brain activity. Annu. Rev. Psychol. 63, 483-509. doi: 10.1146/annurev-psych-120710-100412
87. Trapp, S., and Lepsien, J. (2012). Attentional orienting to mnemonic representations: reduction of load-sensitive maintenance-related activity in the intraparietal sulcus. Neuropsychologia 50, 2805-2811. doi: 10.1016/j.neuropsychologia.2012.08.003
88. Van Boxtel, J. J. A., Tsuchiya, N., and Koch, C. (2010). Consciousness and attention: on sufficiency and necessity. Front. Psychol. 1:217. doi: 10.3389/fpsyg.2010.00217
89. 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. doi: 10.1126/science.277.5324.376
90. Vogel, E. K., McCollough, A. W., and Machizawa, M. G. (2005). Neural measures reveal individual differences in controlling access to working memory. Nature 438, 500-503. doi: 10.1038/nature04171
91. Yonelinas, A. P. (2013). The hippocampus supports high-resolution binding in the service of perception, working memory and long-term memory. Behav. Brain Res. 254, 34-44. doi: 10.1016/j.bbr.2013.05.030