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.

Transient and sustained activity in a distributed neural system for human working memory

Abstract

Working memory involves the short-term maintenance of an active representation of information so that it is available for further processing. Visual working memory tasks, in which subjects retain the memory of a stimulus over brief delays, require both the perceptual encoding of the stimulus and the subsequent maintenance of its representation after the stimulus is removed from view. Such tasks activate multiple areas in visual and prefrontal cortices1–9. To delineate the roles these areas play in perception and working memory maintenance, we used functional magnetic resonance imaging (fMRI) to obtain dynamic measures of neural activity related to different components of a face working memory task—non-selective transient responses to visual stimuli, selective transient responses to faces, and sustained responses over memory delays. Three occipitotemporal areas in the ventral object vision pathway had mostly transient responses to stimuli, indicating their predominant role in perceptual processing, whereas three prefrontal areas demonstrated sustained activity over memory delays, indicating their predominant role in working memory. This distinction, however, was not absolute. Additionally, the visual areas demonstrated different degrees of selectivity, and the prefrontal areas demonstrated different strengths of sustained activity, revealing a continuum of functional specialization, from occipital through multiple prefrontal areas, regarding each area's relative contribution to perceptual and mnemonic processing.

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

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

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

Similar content being viewed by others

References

  1. Cohen, J. D. et al. Activation of the prefrontal cortex in a nonspatial working memory task with functional MRI. Hum. Brain Mapp. 1, 293–304 (1994).

    Article  CAS  Google Scholar 

  2. Courtney, S. M., Ungerleider, L. G., Keil, K. & Haxby, J. V. Object and spatial visual working memory activate separate neural systems in human cortex. Cereb. Cortex 6, 39–49 (1996).

    Article  CAS  Google Scholar 

  3. D'Esposito, M. et al. The neural basis of the central executive system of working memory. Nature 378, 279–281 (1995).

    Article  ADS  CAS  Google Scholar 

  4. Fiez, J. A. et al. A positron emission tomography study of the short-term maintenance of verbal information. J. Neurosci. 16, 808–822 (1996).

    Article  CAS  Google Scholar 

  5. Haxby, J. V., Ungerleider, L. G., Horwitz, B., Rapoport, S. I. & Grady, C. L. Hemispheric differences in neural systems for face working memory: A PET rCBF study. Hum. Brain Mapp. 3, 68–82 (1995).

    Article  Google Scholar 

  6. McCarthy, G. et al. Functional magnetic resonance imaging of human prefrontal cortex activation during a spatial working memory task. Proc. Natl Acad. Sci. USA 91, 8690–8694 (1994).

    Article  ADS  CAS  Google Scholar 

  7. Owen, A. M., Evans, A. C. & Petrides, M. Evidence for a two-stage model of spatial working memory processing within the lateral frontal cortex: a positron emission tomography study. Cereb. Cortex 6, 31–38 (1996).

    Article  CAS  Google Scholar 

  8. Petrides, M., Alivisatos, B., Evans, A. C. & Meyer, E. Dissociation of human mid-dorsolateral from posterior dorsolateral frontal cortex in memory processing. Proc. Natl Acad. Sci. USA 90, 873–877 (1993).

    Article  ADS  CAS  Google Scholar 

  9. Smith, E. E., Jonides, J. & Koeppe, R. A. Dissociating verbal and spatial working memory using PET. Cereb. Cortex 6, 11–20 (1996).

    Article  CAS  Google Scholar 

  10. Chao, L. L. & Knight, R. T. Prefrontal and posterior cortical activation during auditory working memory. Cog. Brain Res. 4, 27–37 (1996).

    Article  CAS  Google Scholar 

  11. Gevins, A. et al. High resolution evoked potential imaging of the cortical dynamics of human working memory. Electroenceph. Clin. Neurophys. 98, 327–348 (1996).

    Article  CAS  Google Scholar 

  12. Cohen, J. D. et al. Temporal dynamics of brain activation during a working memory task. Nature 386, 604–608 (1997).

    Article  ADS  CAS  Google Scholar 

  13. Felleman, D. J. & Van Essen, D. C. Distributed hierarchical processing in the primate cerebral cortex. Cereb. Cortex 1, 1–47 (1991).

    Article  CAS  Google Scholar 

  14. Buckner, R. L. Beyond HERA: Contributions of specific prefrontal brain areas to long-term memory retrieval. Psychonom. Bull. Rev. 3, 149–158 (1996).

    Article  CAS  Google Scholar 

  15. Haxby, J. V. et al. Face encoding and recognition in the human brain. Proc. Natl Acad. Sci. USA 93, 922–927 (1996).

    Article  ADS  CAS  Google Scholar 

  16. Demb, J. B. et al. Semantic encoding and retrieval in the left inferior prefrontal cortex: a functional MRI study of task difficulty and process specificity. J. Neurosci. 15, 5870–5878 (1995).

    Article  CAS  Google Scholar 

  17. McCarthy, G., Blamire, A. M., Rothman, D. L., Gruetter, R. & Shulman, R. G. Echo-planar magnetic resonance imaging studies of frontal cortex activation during word generation in humans. Proc. Natl Acad. Sci. USA 90, 4952–4956 (1993).

    Article  ADS  CAS  Google Scholar 

  18. Paus, T. Location and function of the human frontal eye-field: a selective review. Neuropsychologia 34, 475–483 (1996).

    Article  CAS  Google Scholar 

  19. Courtney, S. M., Maisog, J. M., Ungerleider, L. G. & Haxby, J. V. Extrastriate and frontal contributions to face and location working memory. Soc. Neurosci. Abstr. 22, 968 (1996).

    Google Scholar 

  20. Desimone, R. & Ungerleider, L. G. in Handbook of Neuropsychology (eds Boiler, F. & Grafman, J.) Vol. 2, 267–300 (Elsevier, Amsterdam, 1989).

    Google Scholar 

  21. Perrett, D. I., Rolls, E. T. & Caan, W. Visual neurons responsive to faces in the monkey temporal cortex. Exp. Brain Res. 47, 329–342 (1982).

    Article  CAS  Google Scholar 

  22. Desimone, R., Albright, T. D., Gross, C. G. & Bruce, C. Stimulus selective properties of inferior temporal neurons in the macaque. J. Neurosci. 4, 2051–2062 (1984).

    Article  CAS  Google Scholar 

  23. Miyashita, Y. & Chang, H. S. Neuronal correlate of pictorial short-term memory in the primate temporal cortex. Nature 331, 68–70 (1988).

    Article  ADS  CAS  Google Scholar 

  24. Miller, E. K., Li, L. & Desimone, R. Activity of neurons in anterior inferior temporal cortex during a short-term memory task. J. Neurosci. 13, 1460–1478 (1993).

    Article  CAS  Google Scholar 

  25. Fuster, J. M. Memory in the Cerebral Cortex: An Empirical Approach to Neural Networks in the Human and Nonhuman Primate (MIT Press, Cambridge, Massachusetts, 1995).

    Google Scholar 

  26. Wilson, F. A., O'Scalaidhe, S. P. & Goldman-Rakic, P. S. Dissociation of object and spatial processing domains in primate prefrontal cortex. Science 260, 1955–1957 (1993).

    Article  ADS  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  28. Friston, K. J. et al. Analysis of fMRI time-series revisited. Neurolmage 2, 45–53 (1995).

    Article  CAS  Google Scholar 

  29. Friston, K. J., Worsley, K. J., Frackowiak, R. S. J., Mazziotta, J. C. & Evans, A. C. Assessing the significance of focal activations using their spatial extent. Hum. Brain Mapp. 1, 210–220 (1994).

    Article  CAS  Google Scholar 

  30. Talairach, J. & Tournoux, P. Co-Planar Stereotaxis Atlas of the Human Brain (transl. Rayport, M.) (Thieme Medical, New York, 1988).

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Courtney, S., Ungerleider, L., Keil, K. et al. Transient and sustained activity in a distributed neural system for human working memory. Nature 386, 608–611 (1997). https://doi.org/10.1038/386608a0

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/386608a0

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

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