Evidence for working memory storage operations in perceptual cortex

Abstract

Isolating the short-term storage component of working memory (WM) from the myriad of associated executive processes has been an enduring challenge. Recent efforts have identified patterns of activity in visual regions that contain information about items being held in WM. However, it remains unclear (1) whether these representations withstand intervening sensory input and (2) how communication between multimodal association cortex and the unimodal perceptual regions supporting WM representations is involved in WM storage. We present evidence that the features of a face held in WM are stored within face-processing regions, that these representations persist across subsequent sensory input, and that information about the match between sensory input and a memory representation is relayed forward from perceptual to prefrontal regions. Participants were presented with a series of probe faces and indicated whether each probe matched a target face held in WM. We parametrically varied the feature similarity between the probe and target faces. Activity within face-processing regions scaled linearly with the degree of feature similarity between the probe face and the features of the target face, suggesting that the features of the target face were stored in these regions. Furthermore, directed connectivity measures revealed that the direction of information flow that was optimal for performance was from sensory regions that stored the features of the target face to dorsal prefrontal regions, supporting the notion that sensory input is compared to representations stored within perceptual regions and is subsequently relayed forward. Together, these findings indicate that WM storage operations are carried out within perceptual cortex.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3

References

  1. Aguirre, G. K. (2007). Continuous carry-over designs for fMRI. NeuroImage, 35, 1480–1494.

    PubMed Central  PubMed  Article  Google Scholar 

  2. Al-Aidroos, N., Said, C. P., & Turk-Browne, N. B. (2012). Top-down attention switches coupling between low-level and high-level areas of human visual cortex. Proceedings of the National Academy of Sciences, 109, 14675–14680. doi:10.1073/pnas.1202095109

    Article  Google Scholar 

  3. Andrews, T. J., & Ewbank, M. P. (2004). Distinct representations for facial identity and changeable aspects of faces in the human temporal lobe. NeuroImage, 23, 905–913. doi:10.1016/j.neuroimage.2004.07.060

    PubMed  Article  Google Scholar 

  4. Artchakov, D., Tikhonravov, D., Ma, Y., Neuvonen, T., Linnankoski, I., & Carlson, S. (2009). Distracters impair and create working memory-related neuronal activity in the prefrontal cortex. Cerebral Cortex, 19, 2680–2689. doi:10.1093/cercor/bhp037

    PubMed  Article  Google Scholar 

  5. Awh, E., & Jonides, J. (2001). Overlapping mechanisms of attention and spatial working memory. Trends in Cognitive Sciences, 5, 119–126. doi:10.1016/S1364-6613(00)01593-X

    PubMed  Article  Google Scholar 

  6. Awh, E., Vogel, E. K., & Oh, S. (2006). Interactions between attention and working memory. Neuroscience, 139, 201–208. doi:10.1016/j.neuroscience.2005.08.023

    PubMed  Article  Google Scholar 

  7. Badre, D., & Wagner, A. D. (2007). Left ventrolateral prefrontal cortex and the cognitive control of memory. Neuropsychologia, 45, 2883–2901. doi:10.1016/j.neuropsychologia.2007.06.015

    PubMed  Article  Google Scholar 

  8. Brass, M., Derrfuss, J., Forstmann, B., & von Cramon, D. Y. (2005). The role of the inferior frontal junction area in cognitive control. Trends in Cognitive Sciences, 9, 314–316. doi:10.1016/j.tics.2005.05.001

    PubMed  Article  Google Scholar 

  9. Braver, T. S., Cohen, J. D., Nystrom, L. E., Jonides, J., Smith, E. E., & Noll, D. C. (1997). A parametric study of prefrontal cortex involvement in human working memory. NeuroImage, 5, 49–62.

    PubMed  Article  Google Scholar 

  10. Chelazzi, L., Duncan, J., Miller, E. K., & Desimone, R. (1998). Responses of neurons in inferior temporal cortex during memory-guided visual search. Journal of Neurophysiology, 80, 2918–2940.

    PubMed  Google Scholar 

  11. Christophel, T. B., Hebart, M. N., & Haynes, J. D. (2012). Decoding the contents of visual short-term memory from human visual and parietal cortex. Journal of Neuroscience, 32, 12983–12989. doi:10.1523/JNEUROSCI.0184-12.2012

    PubMed  Article  Google Scholar 

  12. Cohen, J. R., Sreenivasan, K. K., & D’Esposito, M. (2012). Correspondence between stimulus encoding- and maintenance-related neural processes underlies successful working memory. Cerebral Cortex. doi:10.1093/cercor/bhs339. Advance online publication.

    Google Scholar 

  13. Cowan, N. (1993). Activation, attention, and short-term memory. Memory & Cognition, 21, 162–167.

    Article  Google Scholar 

  14. Cox, R. W. (1996). AFNI: Software for analysis and visualization of functional magnetic resonance neuroimages. Computers and Biomedical Research, 29, 162–173.

    PubMed  Article  Google Scholar 

  15. D’Esposito, M. (2007). From cognitive to neural models of working memory. Philosophical Transactions of the Royal Society B, 362, 761–772. doi:10.1098/rstb.2007.2086

    Article  Google Scholar 

  16. D’Esposito, M., & Postle, B. R. (1999). The dependence of span and delayed-response performance on prefrontal cortex. Neuropsychologia, 37, 1303–1315. doi:10.1016/S0028-3932(99)00021-4

    PubMed  Article  Google Scholar 

  17. D’Esposito, M., Postle, B. R., Jonides, J., & Smith, E. E. (1999). The neural substrate and temporal dynamics of interference effects in working memory as revealed by event-related functional MRI. Proceedings of the National Academy of Sciences, 96, 7514–7519.

    Article  Google Scholar 

  18. David, S. V., Hayden, B. Y., Mazer, J. A., & Gallant, J. L. (2008). Attention to stimulus features shifts spectral tuning of v4 neurons during natural vision. Neuron, 59, 509–521. doi:10.1016/j.neuron.2008.07.001

    PubMed Central  PubMed  Article  Google Scholar 

  19. Deco, G., Rolls, E. T., Albantakis, L., & Romo, R. (2013). Brain mechanisms for perceptual and reward-related decision-making. Progress in Neurobiology, 103, 194–213. doi:10.1016/j.pneurobio.2012.01.010

    PubMed  Article  Google Scholar 

  20. Derrfuss, J., Brass, M., Neumann, J., & von Cramon, D. Y. (2005). Involvement of the inferior frontal junction in cognitive control: Meta-analyses of switching and Stroop studies. Human Brain Mapping, 25, 22–34. doi:10.1002/hbm.20127

    PubMed  Article  Google Scholar 

  21. Deshpande, G., Sathian, K., & Hu, X. (2010). Effect of hemodynamic variability on Granger causality analysis of fMRI. NeuroImage, 52, 884–896.

    PubMed Central  PubMed  Article  Google Scholar 

  22. Desimone, R., & Duncan, J. (1995). Neural mechanisms of selective visual attention. Annual Review of Neuroscience, 18, 193–222. doi:10.1146/annurev.ne.18.030195.001205

    PubMed  Article  Google Scholar 

  23. Ding, M., Bressler, S. L., Yang, W., & Liang, H. (2000). Short-window spectral analysis of cortical event-related potentials by adaptive multivariate autoregressive modeling: Data preprocessing, model validation, and variability assessment. Biological Cybernetics, 83, 35–45.

    PubMed  Article  Google Scholar 

  24. Druzgal, T. J., & D’Esposito, M. (2001). A neural network reflecting decisions about human faces. Neuron, 32, 947–955.

    PubMed  Article  Google Scholar 

  25. Emrich, S. M., Riggall, A. C., LaRocque, J. J., & Postle, B. R. (2013). Distributed patterns of activity in sensory cortex reflect the precision of multiple items maintained in visual short-term memory. Journal of Neuroscience, 33, 6516–6523. doi:10.1523/JNEUROSCI.5732-12.2013

    PubMed Central  PubMed  Article  Google Scholar 

  26. Ester, E. F., Anderson, D. E., Serences, J. T., & Awh, E. (2013). A neural measure of precision in visual working memory. Journal of Cognitive Neuroscience, 25, 754–761. doi:10.1162/jocn_a_00357

    PubMed  Article  Google Scholar 

  27. Fiebach, C. J., Rissman, J., & D’Esposito, M. (2006). Modulation of inferotemporal cortex activation during verbal working memory maintenance. Neuron, 51, 251–261. doi:10.1016/j.neuron.2006.06.007

    PubMed  Article  Google Scholar 

  28. Friston, K. J. (1994). Functional and effective connectivity in neuroimaging: A synthesis. Human Brain Mapping, 2, 56–78.

    Article  Google Scholar 

  29. Friston, K. J. (2009). Causal modelling and brain connectivity in functional magnetic resonance imaging. PLoS Biology, 7, e33. doi:10.1371/journal.pbio.1000033

    PubMed  Article  Google Scholar 

  30. Friston, K. J., Harrison, L., & Penny, W. (2003). Dynamic causal modelling. NeuroImage, 19, 1273–1302. doi:10.1016/S1053-8119(03)00202-7

    PubMed  Article  Google Scholar 

  31. Fuster, J. M., Bauer, R., & Jervey, J. (1985). Functional interactions between inferotemporal and prefrontal cortex in a cognitive task. Brain Research, 330, 299–307.

    PubMed  Article  Google Scholar 

  32. Gazzaley, A., Cooney, J. W., McEvoy, K., Knight, R. T., & D’Esposito, M. (2005). Top-down enhancement and suppression of the magnitude and speed of neural activity. Journal of Cognitive Neuroscience, 17, 507–517. doi:10.1162/0898929053279522

    PubMed  Article  Google Scholar 

  33. Gazzaley, A., & Nobre, A. C. (2012). Top-down modulation: Bridging selective attention and working memory. Trends in Cognitive Sciences, 16, 129–135. doi:10.1016/j.tics.2011.11.014

    PubMed Central  PubMed  Article  Google Scholar 

  34. Gazzaley, A., Rissman, J., & D’Esposito, M. (2004). Functional connectivity during working memory maintenance. Cognitive, Affective, & Behavioral Neuroscience, 4, 580–599. doi:10.3758/CABN.4.4.580

    Article  Google Scholar 

  35. Gold, J. I., & Shadlen, M. N. (2007). The neural basis of decision making. Annual Review of Neuroscience, 30, 535–574. doi:10.1146/annurev.neuro.29.051605.113038

    PubMed  Article  Google Scholar 

  36. Gratton, C., Sreenivasan, K. K., Silver, M. A., & D’Esposito, M. (2013). Attention selectively modifies the representation of individual faces in the human brain. Journal of Neuroscience, 33, 6979–6989. doi:10.1523/JNEUROSCI.4142-12.2013

    PubMed Central  PubMed  Article  Google Scholar 

  37. Harrison, S. A., & Tong, F. (2009). Decoding reveals the contents of visual working memory in early visual areas. Nature, 458, 632–635. doi:10.1038/nature07832

    PubMed Central  PubMed  Article  Google Scholar 

  38. Jha, A. P., Fabian, S. A., & Aguirre, G. K. (2004). The role of prefrontal cortex in resolving distractor interference. Cognitive, Affective, & Behavioral Neuroscience, 4, 517–527. doi:10.3758/CABN.4.4.517

    Article  Google Scholar 

  39. Jha, A. P., & McCarthy, G. (2000). The influence of memory load upon delay-interval activity in a working-memory task: An event-related functional MRI study. Journal of Cognitive Neuroscience, 12, 90–105.

    PubMed  Article  Google Scholar 

  40. Jiang, Y., Haxby, J. V., Martin, A., Ungerleider, L. G., & Parasuraman, R. (2000). Complementary neural mechanisms for tracking items in human working memory. Science, 287, 643–646. doi:10.1126/science.287.5453.643

    PubMed  Article  Google Scholar 

  41. Jonides, J., Schumacher, E. H., Smith, E. E., Lauber, E. J., Awh, E., Minoshima, S., & Koeppe, R. A. (1997). Verbal working memory load affects regional brain activation as measured by PET. Journal of Cognitive Neuroscience, 9, 462–475. doi:10.1162/jocn.1997.9.4.462

    PubMed  Article  Google Scholar 

  42. Jonides, J., Smith, E. E., Koeppe, R. A., Awh, E., Minoshima, S., & Mintun, M. A. (1993). Spatial working-memory in humans as revealed by PET. Nature, 363, 623–625. doi:10.1038/363623a0

    PubMed  Article  Google Scholar 

  43. Jonides, J., Smith, E. E., Marshuetz, C., Koeppe, R. A., & Reuter-Lorenz, P. A. (1998). Inhibition in verbal working memory revealed by brain activation. Proceedings of the National Academy of Sciences, 95, 8410–8413.

    Article  Google Scholar 

  44. Kuo, B.-C., Stokes, M. G., & Nobre, A. C. (2012). Attention modulates maintenance of representations in visual short-term memory. Journal of Cognitive Neuroscience, 24, 51–60. doi:10.1162/jocn_a_00087

    PubMed Central  PubMed  Article  Google Scholar 

  45. Lee, T. G., & D’Esposito, M. (2012). The dynamic nature of top-down signals originating from prefrontal cortex: A combined fMRI-TMS study. Journal of Neuroscience, 32, 15458–15466. doi:10.1523/JNEUROSCI.0627-12.2012

    PubMed Central  PubMed  Article  Google Scholar 

  46. Lepsien, J., & Nobre, A. C. (2007). Attentional modulation of object representations in working memory. Cerebral Cortex, 17, 2072–2083. doi:10.1093/cercor/bhl116

    PubMed  Article  Google Scholar 

  47. Leung, H.-C., Gore, J. C., & Goldman-Rakic, P. S. (2002). Sustained mnemonic response in the human middle frontal gyrus during on-line storage of spatial memoranda. Journal of Cognitive Neuroscience, 14, 659–671. doi:10.1162/08989290260045882

    PubMed  Article  Google Scholar 

  48. Leung, H.-C., Seelig, D., & Gore, J. C. (2004). The effect of memory load on cortical activity in the spatial working memory circuit. Cognitive, Affective, & Behavioral Neuroscience, 4, 553–563. doi:10.3758/CABN.4.4.553

    Article  Google Scholar 

  49. Lewis-Peacock, J. A., & Postle, B. R. (2008). Temporary activation of long-term memory supports working memory. Journal of Neuroscience, 28, 8765–8771. doi:10.1523/JNEUROSCI.1953-08.2008

    PubMed Central  PubMed  Article  Google Scholar 

  50. Liebe, S., Hoerzer, G. M., Logothetis, N. K., & Rainer, G. (2012). Theta coupling between V4 and prefrontal cortex predicts visual short-term memory performance. Nature Neuroscience, 15(456–62), S1–S2. doi:10.1038/nn.3038

    Google Scholar 

  51. Liu, T., Hospadaruk, L., Zhu, D. C., & Gardner, J. L. (2011). Feature-specific attentional priority signals in human cortex. Journal of Neuroscience, 31, 4484–4495. doi:10.1523/JNEUROSCI.5745-10.2011

    PubMed  Article  Google Scholar 

  52. Miller, E. K., & Desimone, R. (1994). Parallel neuronal mechanisms for short-term memory. Science, 263, 520–522. doi:10.1126/science.8290960

    PubMed  Article  Google Scholar 

  53. Miller, E. K., Erickson, C. A., & Desimone, R. (1996). Neural mechanisms of visual working memory in prefrontal cortex of the macaque. Journal of Neuroscience, 16, 5154–5167.

    PubMed  Google Scholar 

  54. Miller, B. T., Vytlacil, J., Fegen, D., Pradhan, S., & D’Esposito, M. (2011). The prefrontal cortex modulates category selectivity in human extrastriate cortex. Journal of Cognitive Neuroscience, 23, 1–10. doi:10.1162/jocn.2010.21516

    PubMed  Article  Google Scholar 

  55. Morris, S. B., & DeShon, R. P. (2002). Combining effect size estimates in meta-analysis with repeated measures and independent-groups designs. Psychological Methods, 7, 105–125. doi:10.1037/1082-989X.7.1.105

    PubMed  Article  Google Scholar 

  56. Munk, M. H., Linden, D. E., Muckli, L., Lanfermann, H., Zanella, F. E., Singer, W., & Goebel, R. (2002). Distributed cortical systems in visual short-term memory revealed by event-related functional magnetic resonance imaging. Cerebral Cortex, 12, 866–876. doi:10.1093/cercor/12.8.866

    PubMed  Article  Google Scholar 

  57. Pandya, D. N., Dye, P., & Butters, N. (1971). Efferent cortico-cortical projections of the prefrontal cortex in the rhesus monkey. Brain Research, 31, 35–46. doi:10.1016/0006-8993(71)90632-9

    PubMed  Article  Google Scholar 

  58. Pandya, D. N., & Kuypers, H. G. J. M. (1969). Cortico-cortical connections in the rhesus monkey. Brain Research, 13, 13–36. doi:10.1016/0006-8993(69)90141-3

    PubMed  Article  Google Scholar 

  59. Pasternak, T., & Greenlee, M. W. (2005). Working memory in primate sensory systems. Nature Reviews Neuroscience, 6, 97–107. doi:10.1038/nrn1603

    PubMed  Article  Google Scholar 

  60. Peters, J. C., Roelfsema, P. R., & Goebel, R. (2012). Task-relevant and accessory items in working memory have opposite effects on activity in extrastriate cortex. Journal of Neuroscience, 32, 17003–17011. doi:10.1523/JNEUROSCI.0591-12.2012

    PubMed  Article  Google Scholar 

  61. 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

    PubMed Central  PubMed  Article  Google Scholar 

  62. Ranganath, C., Cohen, M. X., Dam, C., & D’Esposito, M. (2004). Inferior temporal, prefrontal, and hippocampal contributions to visual working memory maintenance and associative memory retrieval. Journal of Neuroscience, 24, 3917–3925. doi:10.1523/JNEUROSCI.5053-03.2004

    PubMed  Article  Google Scholar 

  63. Riggall, A. C., & Postle, B. R. (2012). The relationship between working memory storage and elevated activity as measured with functional magnetic resonance imaging. Journal of Neuroscience, 32, 12990–12998. doi:10.1523/JNEUROSCI.1892-12.2012

    PubMed Central  PubMed  Article  Google Scholar 

  64. Rissman, J., Gazzaley, A., & D’Esposito, M. (2004). Measuring functional connectivity during distinct stages of a cognitive task. NeuroImage, 23, 752–763. doi:10.1016/j.neuroimage.2004.06.035

    PubMed  Article  Google Scholar 

  65. Roebroeck, A., Formisano, E., & Goebel, R. (2005). Mapping directed influence over the brain using Granger causality and fMRI. NeuroImage, 25, 230–242. doi:10.1016/j.neuroimage.2004.11.017

    PubMed  Article  Google Scholar 

  66. Sakai, K., Rowe, J. B., & Passingham, R. (2002). Active maintenance in prefrontal area 46 creates distractor-resistant memory. Nature Neuroscience, 5, 479–484.

    PubMed  Google Scholar 

  67. Salazar, R. F., Dotson, N. M., Bressler, S. L., & Gray, C. M. (2012). Content-specific fronto-parietal synchronization during visual working memory. Science, 338, 1097–1100. doi:10.1126/science.1224000

    PubMed  Article  Google Scholar 

  68. Schippers, M. B., Renken, R., & Keysers, C. (2011). The effect of intra- and inter-subject variability of hemodynamic responses on group level Granger causality analyses. NeuroImage, 57, 22–36. doi:10.1016/j.neuroimage.2011.02.008

    PubMed  Article  Google Scholar 

  69. Serences, J. T., Ester, E. F., Vogel, E. K., & Awh, E. (2009). Stimulus-specific delay activity in human primary visual cortex. Psychological Science, 20, 207–214. doi:10.1111/j.1467-9280.2009.02276.x

    PubMed Central  PubMed  Article  Google Scholar 

  70. Seth, A. K. (2010). A MATLAB toolbox for Granger causal connectivity analysis. Journal of Neuroscience Methods, 186, 262–273. doi:10.1016/j.jneumeth.2009.11.020

    PubMed  Article  Google Scholar 

  71. Seth, A. K., Chorley, P., & Barnett, L. C. (2013). Granger causality analysis of fMRI BOLD signals is invariant to hemodynamic convolution but not downsampling. NeuroImage, 65, 540–555. doi:10.1016/j.neuroimage.2012.09.049

    PubMed  Article  Google Scholar 

  72. Smith, E. E., & Jonides, J. (1998). Neuroimaging analyses of human working memory. Proceedings of the National Academy of Sciences, 95, 12061–12068.

    Article  Google Scholar 

  73. Smith, E. E., & Jonides, J. (1999). Storage and executive processes in the frontal lobes. Science, 283, 1657–1661. doi:10.1126/science.283.5408.1657

    PubMed  Article  Google Scholar 

  74. Smith, E. E., Jonides, J., Koeppe, R. A., Awh, E., Schumacher, E. H., & Minoshima, S. (1995). Spatial versus object working memory: PET investigations. Journal of Cognitive Neuroscience, 7, 337–356. doi:10.1162/jocn.1995.7.3.337

    PubMed  Article  Google Scholar 

  75. Smith, S. M., Miller, K. L., Salimi-Khorshidi, G., Webster, M., Beckmann, C. F., Nichols, T. E., & Woolrich, M. W. (2011). Network modelling methods for FMRI. NeuroImage, 54, 875–891. doi:10.1016/j.neuroimage.2010.08.063

    PubMed  Article  Google Scholar 

  76. Soto, D., Llewelyn, D., & Silvanto, J. (2012). Distinct causal mechanisms of attentional guidance by working memory and repetition priming in early visual cortex. Journal of Neuroscience, 32, 3447–3452. doi:10.1523/JNEUROSCI.6243-11.2012

    PubMed  Article  Google Scholar 

  77. Speer, N. K., Jacoby, L. L., & Braver, T. S. (2003). Strategy-dependent changes in memory: Effects on behavior and brain activity. Cognitive, Affective, & Behavioral Neuroscience, 3, 155–167. doi:10.3758/CABN.3.3.155

    Article  Google Scholar 

  78. Sreenivasan, K. K., & Jha, A. P. (2007). Selective attention supports working memory maintenance by modulating perceptual processing of distractors. Journal of Cognitive Neuroscience, 19, 32–41. doi:10.1162/jocn.2007.19.1.32

    PubMed  Article  Google Scholar 

  79. Sreenivasan, K. K., Katz, J., & Jha, A. P. (2007). Temporal characteristics of top-down modulations during working memory maintenance: An event-related potential study of the N170 component. Journal of Cognitive Neuroscience, 19, 1836–1844. doi:10.1162/jocn.2007.19.11.1836

    PubMed  Article  Google Scholar 

  80. Sreenivasan, K. K., Sambhara, D., & Jha, A. P. (2011). Working memory templates are maintained as feature-specific perceptual codes. Journal of Neurophysiology, 106, 115–121. doi:10.1152/jn.00776.2010

    PubMed Central  PubMed  Article  Google Scholar 

  81. St James, J. D., & Eriksen, C. W. (1991). Response competition produces a “fast same effect” in same–different judgments. In G. R. Lockhead & J. R. Pomerantz (Eds.), The perception of structure: Essays in honor of Wendell R. Garner (pp. 157–168). Washington: American Psychological Association. doi:10.1037/10101-009

    Google Scholar 

  82. Steiger, J. H. (1980). Tests for comparing elements of a correlation matrix. Psychological Bulletin, 87, 245–251. doi:10.1037/0033-2909.87.2.245

    Article  Google Scholar 

  83. Sugase-Miyamoto, Y., Liu, Z., Wiener, M. C., Optican, L. M., & Richmond, B. J. (2008). Short-term memory trace in rapidly adapting synapses of inferior temporal cortex. PLoS Computational Biology, 4, e1000073. doi:10.1371/journal.pcbi.1000073

    PubMed Central  PubMed  Article  Google Scholar 

  84. Thompson-Schill, S. L., D’Esposito, M., Aguirre, G. K., & Farah, M. J. (1997). Role of left inferior prefrontal cortex in retrieval of semantic knowledge: A reevaluation. Proceedings of the National Academy of Sciences, 94, 14792–14797.

    Article  Google Scholar 

  85. Todd, J. J., & Marois, R. (2004). Capacity limit of visual short-term memory in human posterior parietal cortex. Nature, 428, 751–754. doi:10.1038/nature02466

    PubMed  Article  Google Scholar 

  86. Tsotsos, J. K., Culhane, S. M., Kei Wai, W. Y., Lai, Y., Davis, N., & Nuflo, F. (1995). Modeling visual attention via selective tuning. Artificial Intelligence, 78, 507–545.

    Article  Google Scholar 

  87. Wager, T. D., & Smith, E. E. (2003). Neuroimaging studies of working memory: A meta-analysis. Cognitive, Affective, & Behavioral Neuroscience, 3, 255–274. doi:10.3758/CABN.3.4.255

    Article  Google Scholar 

  88. Wen, X., Rangarajan, G., & Ding, M. (2013). Is Granger causality a viable technique for analyzing fMRI data? PLoS ONE, 8, e67428. doi:10.1371/journal.pone.0067428

    PubMed Central  PubMed  Article  Google Scholar 

  89. Yoon, J. H., Curtis, C. E., & D’Esposito, M. (2006). Differential effects of distraction during working memory on delay-period activity in the prefrontal cortex and the visual association cortex. NeuroImage, 29, 1117–1126. doi:10.1016/j.neuroimage.2005.08.024

    PubMed  Article  Google Scholar 

  90. Zanto, T. P., Rubens, M. T., Thangavel, A., & Gazzaley, A. (2011). Causal role of the prefrontal cortex in top-down modulation of visual processing and working memory. Nature Neuroscience, 14, 656–661. doi:10.1038/nn.2773

    PubMed Central  PubMed  Article  Google Scholar 

  91. Zhang, J. X., Leung, H.-C., & Johnson, M. K. (2003). Frontal activations associated with accessing and evaluating information in working memory: An fMRI study. NeuroImage, 20, 1531–1539. doi:10.1016/S1053-8119(03)00466-X

    PubMed  Article  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Kartik K. Sreenivasan.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Figure S1

(PDF 100 kb)

Table S1

(DOCX 68.0 KB)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Sreenivasan, K.K., Gratton, C., Vytlacil, J. et al. Evidence for working memory storage operations in perceptual cortex. Cogn Affect Behav Neurosci 14, 117–128 (2014). https://doi.org/10.3758/s13415-013-0246-7

Download citation

Keywords

  • Working memory
  • Functional connectivity