Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Brief Communication
  • Published:

Cortical specialization for attended versus unattended working memory

Nature Neuroscience volume 21, pages 494–496 (2018)Cite this article

Subjects

Abstract

Items held in working memory can be either attended or not, depending on their current behavioral relevance. It has been suggested that unattended contents might be solely retained in an activity-silent form. Instead, we demonstrate here that encoding unattended contents involves a division of labor. While visual cortex only maintains attended items, intraparietal areas and the frontal eye fields represent both attended and unattended items.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Two-stage orientation-change discrimination task using retrocue selection.
Fig. 2: Representation of attended and unattended memory items.

Similar content being viewed by others

References

  1. Baddeley, A. D. Working Memory (Clarendon Press, Oxford, 1986).

  2. Christophel, T. B., Klink, P. C., Spitzer, B., Roelfsema, P. R. & Haynes, J.-D. Trends Cogn. Sci. 21, 111–124 (2017).

    Article  PubMed  Google Scholar 

  3. Stokes, M. G. Trends Cogn. Sci. 19, 394–405 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  4. Mongillo, G., Barak, O. & Tsodyks, M. Science 319, 1543–1546 (2008).

    Article  PubMed  CAS  Google Scholar 

  5. Larocque, J. J., Lewis-Peacock, J. A. & Postle, B. R. Front. Hum. Neurosci. 8, 5 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  6. Lewis-Peacock, J. A., Drysdale, A. T., Oberauer, K. & Postle, B. R. J. Cogn. Neurosci. 24, 61–79 (2012).

    Article  PubMed  Google Scholar 

  7. LaRocque, J. J., Riggall, A. C., Emrich, S. M. & Postle, B. R. Cereb. Cortex 27, 4881–4890 (2017).

    PubMed  Google Scholar 

  8. Wolff, M. J., Jochim, J., Akyürek, E. G. & Stokes, M. G. Nat. Neurosci. 20, 864–871 (2017).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  9. Olivers, C. N. L., Peters, J., Houtkamp, R. & Roelfsema, P. R. Trends Cogn. Sci. 15, 327–334 (2011).

    PubMed  Google Scholar 

  10. Allefeld, C. & Haynes, J.-D. Neuroimage 89, 345–357 (2014).

    Article  PubMed  Google Scholar 

  11. Harrison, S. A. & Tong, F. Nature 458, 632–635 (2009).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  12. Serences, J. T., Ester, E. F., Vogel, E. K. & Awh, E. Psychol. Sci. 20, 207–214 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  13. Ester, E. F., Sprague, T. C. & Serences, J. T. Neuron 87, 893–905 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  14. Ester, E. F., Serences, J. T. & Awh, E. J. Neurosci. 29, 15258–15265 (2009).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  15. Hebb, D. O. The Organization of Behavior(Wiley, New York, 1949).

  16. Itskov, V., Hansel, D. & Tsodyks, M. Front. Comput. Neurosci. https://doi.org/10.3389/fncom.2011.00040 (2011).

  17. Rerko, L. & Oberauer, K. J. Exp. Psychol. Learn. Mem. Cogn. 39, 1075–1096 (2013).

  18. Emrich, S. M., Lockhart, H. A. & Al-Aidroos, N. J. Exp. Psychol. Hum. Percept. Perform. 43, 1454–1465 (2017).

  19. Bae, G.-Y. & Luck, S. J. Vis. https://doi.org/10.1167/16.12.701 (2016).

  20. Ester, E. F., Anderson, D. E., Serences, J. T. & Awh, E. J. Cogn. Neurosci. 25, 754–761 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  21. Christophel, T. B., Hebart, M. N. & Haynes, J.-D. J. Neurosci. 32, 12983–12989 (2012).

    Article  PubMed  CAS  Google Scholar 

  22. Christophel, T. B. & Haynes, J.-D. Neuroimage 91, 43–51 (2014).

    Article  PubMed  Google Scholar 

  23. Christophel, T. B., Cichy, R. M., Hebart, M. N. & Haynes, J.-D. Neuroimage 106, 198–206 (2015).

    Article  PubMed  Google Scholar 

  24. Christophel, T. B., Allefeld, C., Endisch, C. & Haynes, J.-D. Cereb. Cortex https://doi.org/10.1093/cercor/bhx119 (2017)

  25. Schneegans, S. & Bays, P. M. J. Cogn. Neurosci. 29, 1977–1994 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  26. Brainard, D. H. Spat. Vis. 10, 433–436 (1997).

    Article  PubMed  CAS  Google Scholar 

  27. Pratte, M. S. & Tong, F. J. Vis. 14, 22 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  28. Görgen, K., Hebart, M.N., Allefeld, C. & Haynes, J.-D. Neuroimage https://doi.org/10.1016/j.neuroimage.2017.12.083 (2017).

  29. Friston, K. J. et al. Hum. Brain Mapp. 2, 189–210 (1994).

    Article  Google Scholar 

  30. Wang, L., Mruczek, R. E. B., Arcaro, M. J. & Kastner, S. Cereb. Cortex 25, 3911–3931 (2015).

    Article  PubMed  CAS  Google Scholar 

  31. Ashburner, J. & Friston, K. J. Neuroimage 26, 839–851 (2005).

    Article  PubMed  Google Scholar 

  32. Timm, N. H. Applied Multivariate Analysis (Springer, New York, 2002).

  33. Guggenmos, M., Wilbertz, G., Hebart, M. N. & Sterzer, P. eLife 5, e13388 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  34. Haynes, J. D. & Rees, G. Nat. Neurosci. 8, 686–691 (2005).

    Article  PubMed  CAS  Google Scholar 

  35. Haynes, J.-D. & Rees, G. Curr. Biol. 15, 1301–1307 (2005).

    Article  PubMed  CAS  Google Scholar 

  36. Haynes, J.-D. & Rees, G. Nat. Rev. Neurosci. 7, 523–534 (2006).

    Article  PubMed  CAS  Google Scholar 

  37. Kamitani, Y. & Tong, F. Nat. Neurosci. 8, 679–685 (2005).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  38. Soon, C. S., Brass, M., Heinze, H. J. & Haynes, J. D. Nat. Neurosci. 11, 543–545 (2008).

    Article  PubMed  CAS  Google Scholar 

  39. Sterzer, P., Haynes, J.-D. & Rees, G. J. Vis. 8, 10 (2008).

    Article  PubMed  Google Scholar 

  40. Cichy, R. M., Chen, Y. & Haynes, J. D. Neuroimage 54, 2297–2307 (2011).

    Article  PubMed  Google Scholar 

  41. Riggall, A. C. & Postle, B. R. J. Neurosci. 32, 12990–12998 (2012).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  42. Lee, S.-H., Kravitz, D. J. & Baker, C. I. Nat. Neurosci. 16, 997–999 (2013).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  43. Bettencourt, K. C. & Xu, Y. Nat. Neurosci. 19, 150–157 (2016).

    Article  PubMed  CAS  Google Scholar 

  44. Schäfer, J. & Strimmer, K. Stat. Appl. Genet. Mol. Biol. https://doi.org/10.2202/1544-6115.1175 (2005).

  45. Allefeld, C., Görgen, K. & Haynes, J.-D. Neuroimage 141, 378–392 (2016).

    Article  PubMed  Google Scholar 

  46. Dubois, J., de Berker, A. O. & Tsao, D. Y. J. Neurosci. 35, 2791–2802 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  47. Haynes, J.-D. Neuron 87, 257–270 (2015).

    Article  PubMed  CAS  Google Scholar 

  48. Hebart, M. N. & Baker, C. I. Neuroimage https://doi.org/10.1016/j.neuroimage.2017.08.005 (2017).

  49. Efron, B. & Tibshirani, R. J. An Introduction to the Bootstrap (CRC Press, Boca Raton, FL, USA, 1994).

Download references

Acknowledgements

This work was funded by the Bernstein Computational Neuroscience Program of the German Federal Ministry of Education and Research BMBF Grant 01GQ0411, by the Excellence Initiative of the German Federal Ministry of Education and Research and DFG Grants GSC86/1-2009, KFO247, HA 5336/1-1, SFB 940 and JA 945/3-1/SL185/1-1.

Author information

Author notes

  1. These authors contributed equally: Thomas B. Christophel and Polina Iamshchinina.

Authors and Affiliations

  1. Bernstein Center for Computational Neuroscience and Berlin Center for Advanced Neuroimaging and Clinic for Neurology, Charité Universitätsmedizin, corporate member of Freie Universität Berlin, Humboldt Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany

    Thomas B. Christophel, Polina Iamshchinina, Chang Yan, Carsten Allefeld & John-Dylan Haynes

  2. Berlin School of Mind and Brain, Humboldt Universität, Berlin, Germany

    John-Dylan Haynes

  3. Cluster of Excellence NeuroCure, Charité Universitätsmedizin, corporate member of Freie Universität Berlin, Humboldt Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany

    John-Dylan Haynes

  4. Department of Psychology, Humboldt Universität zu Berlin, Berlin, Germany

    John-Dylan Haynes

  5. SFB 940 Volition and Cognitive Control, Technische Universität Dresden, Dresden, Germany

    John-Dylan Haynes

Authors
  1. Thomas B. Christophel
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Polina Iamshchinina
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Chang Yan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Carsten Allefeld
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. John-Dylan Haynes
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

T.B.C., P.I. and J.-D.H. designed the study. P.I. and C.Y. acquired data. T.B.C., P.I. and C.A. analyzed the data. T.B.C., P.I., C.A. and J.-D.H. wrote the manuscript.

Corresponding author

Correspondence to Thomas B. Christophel.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Integrated supplementary information

Supplementary Figure 1 Stimulus set.

The main experiment used a set of twelve orientations, six on the left and six on the right. On each side the stimulus set consisted of orientations that were 30° apart, but the two sets were separated by 15° to experimentally decorrelate the two conditions.

Supplementary Figure 2 Representation of attended and unattended memory items in different regions of the visual cortex.

Information about attended (AMI, circles) and unattended (UMI, squares) memory items as indicated by mean pattern distinctness D within different regions of the visual cortex. (n = 87 human subjects; error bars indicate SEM; *: p < 0.05; **: p < 0.01; ***: p < 0.001; Bonferroni corrected for multiple comparisons). Results were tested against chance using one-tailed one-sample t-tests (V1AMI: t86 = 3.34, p = 0.0006; V1UMI: t86 = -0.87, p = 0.81; V2AMI: t86 = 1.58, p = 0.059; V2UMI: t86 = 0.86, p = 0.19; V3AMI: t86 = 2.97, p = 0.002; V3UMI: t86 = 1.6, p = 0.057; V4AMI: t86 = 1.45, p = 0.076; V4UMI: t86 = 1.48, p = 0.071) and for differences between AMIs and UMIs using two-tailed paired-sample t-tests (V1: t86 = 3.42, p = 0.001; V2: t86 = 0.79, p = 0.43; V3: t86 = 0.61, p = 0.54; V4: t86 = 0.02, p = 0.98).

Supplementary Figure 3 Estimation of the probability of significance of the multivariate pattern analyses with a reduced number of subjects.

Probabilities were estimated using a bootstrapping procedure with 10000 iterations for each of the main multivariate pattern analyses, each area and each possible N ranging from 10 to 86. In each iteration, N values of D were drawn from the whole sample of 87 human subjects and a one-tailed one-sample t-test was testing against chance-level (D = 0) at an uncorrected threshold of p < 0.05. Please note that these estimates do not easily generalize to studies using a different stimulus set, different numbers of repetitions or an otherwise different experimental paradigm. Please further note that the qualitative difference in reliability of information in FEF for unattended over attended items is a result of a difference in variance.

Supplementary Figure 4 Representation of attended and unattended memory items across time.

Information about attended (AMI, circles) and unattended (UMI, squares) memory items as indicated by mean pattern distinctness D on a time-point by time-point basis. Vertical lines indicate the onset of the first cue and the two tasks. Grey panels demark the time-points used for the main analysis shown in Fig. 2. (n = 87 human subjects; error bars indicate SEM; Colored lines on the top part of the figure indicate time points with significant above-chance information at p < 0.05 for AMI [top] and UMI [bottom]; tested using one-tailed one-sample t-tests).

Supplementary Figure 5 Behavioral results.

Behavioral performance in the two-stage orientation change discrimination task shown separately for the first and second task in each trial. Data for the second task are shown separately for trials where the same item was probed twice (‘Repeat’) and where a different item was tested in the second task (‘Switch’). Mean proportion of correct responses (A; two-tailed Wilcoxon signed rank tests; Left: z = 6.40, p < 0.001; Right: z = 7.70, p < 0.001) and mean reaction time in seconds (B; two-sided Wilcoxon signed rank tests; Left: z = 1.10, p = 0.308; Right: z = 7.94, p < 0.001) are reported (n = 87 human subjects; error bars indicate SEM; *: p < 0.05; **: p < 0.01; ***: p < 0.001). Misses (2.44% ±0.26% SEM) were treated as incorrect responses to calculate proportions of correct responses and excluded from reaction time analyses. Miss rate did not differ significantly between conditions.

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Christophel, T.B., Iamshchinina, P., Yan, C. et al. Cortical specialization for attended versus unattended working memory. Nat Neurosci 21, 494–496 (2018). https://doi.org/10.1038/s41593-018-0094-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41593-018-0094-4

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing