Article | Published:

Integration of diverse information in working memory within the frontal lobe

Nature Neuroscience volume 3, pages 8590 (2000) | Download Citation

Subjects

Abstract

Ability to integrate diverse forms of information in current thought, or working memory, is essential for human reasoning and problem solving. We used functional imaging to identify brain regions preferentially involved in maintaining integrated versus unintegrated information in working memory. For equal amounts of verbal and spatial information, activation of prefrontal cortex was greater for maintaining integrated rather than unintegrated representations. Posterior brain regions showed the opposite pattern. These results demonstrate frontal-lobe specialization in maintaining working-memory representations that integrate verbal and spatial information. The role of prefrontal cortex in integrating multiple forms of information in working memory may underlie its unique contribution to high-level cognition that demands flexible mental representations.

  • Subscribe to Nature Neuroscience for full access:

    $59

    Subscribe

Additional access options:

Already a subscriber?  Log in  now or  Register  for online access.

References

  1. 1.

    , , & Active representation of shape and spatial location in man. Cereb. Cortex 6, 612–619 ( 1996).

  2. 2.

    et al. A parametric study of prefrontal cortex involvement in human working memory. Neuroimage 5, 49– 62 (1997).

  3. 3.

    et al. Activation of prefrontal cortex in a non-spatial working memory task with functional MRI. Hum. Brain Mapp. 1, 293–304 (1994).

  4. 4.

    et al. Temporal dynamics of brain activation during a working memory task. Nature 386, 604–607 (1997).

  5. 5.

    , , & Object and spatial visual working memory activate separate neural systems in human cortex. Cereb. Cortex 6, 39– 49 (1996).

  6. 6.

    , , & Transient and sustained activity in a distributed system for human working memory. Nature 386, 608– 611 (1997).

  7. 7.

    et al. An area specialized for spatial working memory in human frontal cortex. Science 279, 1347– 1351 (1998).

  8. 8.

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

  9. 9.

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

  10. 10.

    et al. Spatial working memory in humans as revealed by PET. Nature 363, 623–625 ( 1993).

  11. 11.

    et al. Verbal working memory load affects regional brain activation as measured by PET. J. Cogn. Neurosci. 9, 462–475 (1997).

  12. 12.

    , , & Inhibition in verbal working memory revealed by brain activation. Proc. Natl. Acad. Sci. USA 95, 8410– 8413 (1998).

  13. 13.

    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).

  14. 14.

    et al. Activation of human prefrontal cortex during spatial and nonspatial working memory tasks measured by functional MRI. Cereb. Cortex 6, 600–611 ( 1996).

  15. 15.

    , & 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).

  16. 16.

    et al. Functional organization of spatial and nonspatial working memory processing within the human lateral frontal cortex. Proc. Natl. Acad. Sci. USA 95, 7721–7726 (1998).

  17. 17.

    , & The neural correlates of the verbal component of working memory. Nature 362, 342– 345 (1993).

  18. 18.

    , , & Functional activation of the human frontal cortex during the performance of verbal working memory tasks. Proc. Natl. Acad. Sci. USA 90, 878–882 (1993).

  19. 19.

    , , & Dissociation of human mid-dorsolateral from posterior dorsolateral frontal cortex in memory processing. Proc. Natl. Acad. Sci. USA 90, 873–877 (1993).

  20. 20.

    , , , & Load-dependent roles of frontal brain regions in the maintenance of working memory. Neuroimage 9, 216–226 ( 1999).

  21. 21.

    & The roles of prefrontal brain regions in components of working memory: effects of memory load and individual differences. Proc. Natl. Acad. Sci. USA 96, 6558–6563 (1999).

  22. 22.

    et al. Spatial versus object working memory: PET investigations. J. Cogn. Neurosci. 7, 337– 356 (1995).

  23. 23.

    , & Dissociating verbal and spatial working memory using PET. Cereb. Cortex 6, 11– 20 (1996).

  24. 24.

    , , & Components of verbal working memory: Evidence from neuroimaging. Proc. Natl. Acad. Sci. USA 95, 876– 882 (1998).

  25. 25.

    & Storage and executive processes in the frontal lobes. Science 283, 1657– 1661 (1999).

  26. 26.

    & Neuroimaging analyses of human working memory. Proc. Natl. Acad. Sci. USA 95, 12061 –12068 (1999).

  27. 27.

    & in Analysis of Visual Behavior (eds. Ingle, D. J., Goodale, M. A. & Mansfield, R. J. W.) 549–586 (MIT Press, Cambridge, Massachusetts, 1982).

  28. 28.

    , , & Dissociation of object and spatial processing domains in primate prefrontal cortex. Science 260, 1955– 1957 (1993).

  29. 29.

    & The functional logic of cortical connections. Nature 335, 311–317 (1988).

  30. 30.

    , & Memory fields of neurons in the primate prefrontal cortex. Proc. Natl. Acad. Sci. USA 95, 15008 –15013 (1998).

  31. 31.

    , & Selective representation of relevant information by neurons in the primate prefrontal cortex. Nature 393, 577–579 (1998).

  32. 32.

    , & Integration of what and where in the primate prefrontal cortex. Science 276, 821– 824 (1997).

  33. 33.

    The Prefrontal Cortex: Anatomy, Physiology, and Neuropsychology of the Frontal Lobe (Lippincott-Raven, New York, 1997).

  34. 34.

    , , & Cellular discharge in the dorsolateral prefrontal cortex of the monkey in cognitive tasks. Exp. Neurol. 77, 679–694 (1982).

  35. 35.

    , & Functional MRI studies of spatial and non-spatial working memory. Cognit. Brain Res. 7, 1– 13 (1998).

  36. 36.

    The functional organization of working memory processes within human lateral cortex: the contribution of functional neuroimaging. Eur. J. Neurosci. 9, 1329–1339 ( 1997).

  37. 37.

    Working Memory (Oxford Univ. Press, New York, 1986).

  38. 38.

    & Mental Images in Human Cognition (Elsevier Science, New York, 1991).

  39. 39.

    & The capacity of visual working memory for features and conjunctions. Nature 390, 279–281 (1997).

  40. 40.

    , , , & Neural substrates of fluid reasoning: An fMRI study of neocortical activation during performance of the Raven's Progressive Matrices Test. Cognit. Psychol. 33, 43–63 (1997).

  41. 41.

    et al. Neural systems engaged by planning: a PET study of the Tower of London task. Neuropsychologia 34, 515 –526 (1996).

  42. 42.

    , & Fluid intelligence after frontal lobe lesions. Neuropsychologia 33, 261–268 (1995).

  43. 43.

    et al. A system for relational reasoning in human prefrontal cortex. Psychol. Sci. 10, 119– 125 (1999).

  44. 44.

    , , & The seats of reason? An imaging study of deductive and inductive reasoning. Neuroreport 8, 1305–1310 ( 1997).

  45. 45.

    , , , & The role of anterior prefrontal cortex in human cognition. Nature 399, 148–151 (1999).

  46. 46.

    & Self-navigated spiral fMRI: interleaved versus single-shot. Magn. Reson. Med. 39, 361–368 (1995).

  47. 47.

    & Co-Planar Stereotaxic Atlas of the Human Brain (Thieme, Stuttgart, 1988).

  48. 48.

    , , & Comparing functional (PET) images: The assessment of significant change. J. Cereb. Blood Flow Metab. 11, 690– 699 (1991).

Download references

Acknowledgements

This work was supported by grants from the National Institute on Aging and the National Center for Research Resources. V.P. is supported by a NRSA training grant awarded by the National Institutes of Health. The authors thank Mark D'Esposito for comments on earlier drafts of this manuscript.

Author information

Affiliations

  1. Program in Neurosciences, Jordan Hall, Bldg. 420, Stanford University, Stanford, California 94305, USA

    • V. Prabhakaran
    •  & J. D. E. Gabrieli
  2. Dept. of Psychology, Jordan Hall, Bldg. 420, Stanford University, Stanford, California 94305, USA

    • K. Narayanan
    • , Z. Zhao
    •  & J. D. E. Gabrieli

Authors

  1. Search for V. Prabhakaran in:

  2. Search for K. Narayanan in:

  3. Search for Z. Zhao in:

  4. Search for J. D. E. Gabrieli in:

Corresponding author

Correspondence to V. Prabhakaran.

About this article

Publication history

Received

Accepted

Published

DOI

https://doi.org/10.1038/71156

Rights and permissions

To obtain permission to re-use content from this article visit RightsLink.