Dissociating aspects of verbal working memory within the human frontal lobe: Further evidence for a “process-specific” model of lateral frontal organization

Abstract

There is now converging evidence that suggests that working memory processes within the dorsolateral and ventrolateral frontal cortices are organized according to the type of processing required, rather than according to the nature (i.e., domain) of the information being processed, as has been widely assumed. For example, recent positron emission tomography (PET) studies have demonstrated that either, or both, of these two lateral frontal areas can be activated in spatial working memory tasks, depending on the precise executive processes that are called upon by the task being performed. Moreover, in a recent study using functional magnetic resonance imaging, performances of visual spatial and visual nonspatial working memory tasks were shown to involve identical regions of the lateral prefrontal cortex when all the factors unrelated to the type of stimulus domain were appropriately controlled. These results concur fully with recent reviews of the imaging literature, which have demonstrated that spatial and nonspatial working memory studies, in general, have produced a widely distributed pattern of overlapping activation foci within these lateral frontal regions. In this study, the effects of varying the executive requirements of a simple verbal working memory task (forward vs. backward digit span) were explored in 8 subjects, using PET, in order to establish whether this model generalizes to the verbal domain. As was expected, during forward digit span, significant activation was observed within the midventrolateral frontal cortex, but not within the middorsolateral frontal cortex. In contrast, during backward digit span, significant activation was observed in both regions. The results provide further evidence that the middorsolateral and midventrolateral frontal cortical areas make distinct functional contributions to memory and that this corresponds, in psychological terms, to a fractionation of working memory processes.

References

  1. Andreasen, N. C., O’Leary, D. S., Arndt, S., Cizadlo, T., Hurtig, R., Rezai, K., Watkins, G. L., Boles Ponto, L. L., & Hichwa, R. D. (1995). Short-term and long-term verbal memory: A positron emission tomography study. Proceedings of the National Academy of Sciences, 92, 5111–5115.

    Article  Google Scholar 

  2. Awh, E., Jonides, J., Smith, E. E., Schumacher, E. H., Koeppe, R. A., & Katz, S. (1996). Dissociation of storage and rehearsal in verbal working memory: Evidence from positron emission tomography. Psychological Science, 7, 25–31.

    Article  Google Scholar 

  3. Baddeley, A. D. (1986). Working memory. New York: Oxford University Press.

    Google Scholar 

  4. Baker, S. C., Frith, C. D., Frackowiak, R. S. J., & Dolan, R. J. (1996). Active representation of shape and location in man. Cerebral Cortex, 6, 612–619.

    PubMed  Article  Google Scholar 

  5. Barch, D. M., Braver, T. S., Nystrom, L. E., Forman, S. D., Noll, D. C., & Cohen, J. D. (1997). Dissociating working memory from task difficulty in human prefrontal cortex. Neuropsychologia, 35, 1373–1380.

    PubMed  Article  Google Scholar 

  6. Becker, J. T., Mintun, M. A., Diehl, D. J., Dobkin, J., Martidis, A., Madoff, D. C., & DeKosky, S. T. (1994). Functional neuroanatomy of verbal free recall: A replication study. Human Brain Mapping, 1, 284–292.

    Article  Google Scholar 

  7. 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 

  8. Callicot, J. H., Mattay, V. S., Bertolino, A., Finn, K., Coppola, R., Frank, J. A., Goldberg, T. E., & Weinberger, D. R. (1999). Physiological characteristics of capacity constraints in working memory as revealed by functional MRI. Cerebral Cortex, 9, 20–26.

    Article  Google Scholar 

  9. Cohen, J. D., Forman, S. D., Braver, T. S., Casey, B. J., Servan-Schreiber, D., & Noll, D. C. (1994). Activation of prefrontal cortex in a nonspatial working memory task with functional MRI. Human Brain Mapping, 1, 293–304.

    Article  Google Scholar 

  10. Cohen, J. D., Perlstein, W. M., Braver, T. S., Nystrom, L. E., Noll, D. C., Jonides, J., & Smith, E. E. (1997). Temporal dynamics of brain activation during a working memory task. Nature, 386, 604–608.

    PubMed  Article  Google Scholar 

  11. Collette, F., Salmon, E., Van der Linden, M., Chicherio, C., Belleville, S., Degueldre, C., Delfiore, G., & Franck, G. (1999). Regional brain activity during tasks devoted to the central executive of working memory. Cognitive Brain Research, 7, 411–417.

    PubMed  Article  Google Scholar 

  12. Coull, J. T., Frith, C. D., Frackowiak, R. S. J., & Grasby, P. M. (1996). A fronto-parietal network for rapid visual information processing: A PET study of sustained attention and working memory. Neuropsychologia, 34, 1085–1095.

    PubMed  Article  Google Scholar 

  13. Courtney, S. M., Petit, L., Maisog, J. M., Ungerleider, L. G., & Haxby, J. V. (1998). An area specialized for spatial working memory in human frontal cortex. Science, 279, 1347–1351.

    PubMed  Article  Google Scholar 

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

    PubMed  Article  Google Scholar 

  15. Courtney, S. M., Ungerleider, L. G., Keil, K. K., & Haxby, J. V. (1997). Transient and sustained activity in a distributed neural system for human working memory. Nature, 386, 608–611.

    PubMed  Article  Google Scholar 

  16. D’Esposito, M., Aguirre, G. K., Zarahn, E., Ballard, D., Shin, R. K., Lease, J., & Tang, J. (1998). Functional MRI studies of spatial and nonspatial working memory. Cognitive Brain Research, 7, 1–13.

    PubMed  Article  Google Scholar 

  17. D’Esposito, M., Ballard, D., Aguirre, G. K., & Zarahn, E. (1998). Human prefrontal cortex is not specific for working memory: A functional MRI study. NeuroImage, 8, 274–282.

    PubMed  Article  Google Scholar 

  18. D’Esposito, M., Postle, B. R., Ballard, D., & Lease, J. (1999). Maintenance versus manipulation of information held in working memory: An event-related fMRI study. Brain & Cognition, 41, 66–86.

    Article  Google Scholar 

  19. de Zubicaray, G. I., Williams, S. C. R., Wilson, S. J., Rose, S. E., Brammer, M. J., Bullmore, E. T., Simmons, A., Chalk, J. B., Semple, J., Brown, A. P., Smith, G. A., Ashton, R., & Doddrell, D. M. (1998). Prefrontal cortex involvement in selective letter generation: A functional magnetic resonance imaging study. Cortex, 34, 389–401.

    PubMed  Article  Google Scholar 

  20. Elliot, R., & Dolan, R. J. (1999). Differential neural responses during performance of matching and nonmatching to sample tasks at two delay intervals. Journal of Neuroscience, 19, 5066–5073.

    Google Scholar 

  21. Fiez, J. A., Raife, E. A., Balota, D. A., Schwarz, J. P., Raichle, M. E., & Petersen, S. E. (1996). A positron emission tomography study of the short-term maintenance of verbal information. Journal of Neuroscience, 16, 808–822.

    PubMed  Google Scholar 

  22. Fletcher, P., Shallice, T., & Dolan, R. J. (1998). The functional roles of prefrontal cortex in episodic memory: I. Encoding. Brain, 121, 1239–1248.

    PubMed  Article  Google Scholar 

  23. Fletcher, P., Shallice, T., Frith, C. D., Frackowiak, R. S. J., & Dolan, R. J. (1998). The functional roles of prefrontal cortex in episodic memory: II. Retrieval. Brain, 121, 1249–1256.

    PubMed  Article  Google Scholar 

  24. Funahashi, S., Bruce, C. J., & Goldman-Rakic, P. S. (1989). Mnemonic coding of visual space in the monkey’s dorsolateral prefrontal cortex. Journal of Neurophysiology, 61, 1–19.

    Google Scholar 

  25. Funahashi, S., Bruce, C. J., & Goldman-Rakic, P. S. (1990). Visuospatial coding of primate prefrontal neurons revealed by oculomotor paradigms. Journal of Neurophysiology, 63, 814–831.

    PubMed  Google Scholar 

  26. Fuster, J. M. (1995). Memory in the cerebral cortex: An empirical approach to neural networks in the human and nonhuman primate brain. Cambridge, MA: MIT Press.

    Google Scholar 

  27. Gold, J. M., Berman, K. F., Randolph, C., Goldberg, T. E., & Weinberger, D. R. (1996). PET validation of a novel prefrontal task: Delayed response alternation. Neuropsychology, 10, 3–10.

    Article  Google Scholar 

  28. Goldberg, T. E., Berman, K. F., Fleming, K., Ostrem, J., Van Horn, J. D., Esposito, G., Mattey, V. S., Gold, J. M., & Weinberger, D. R. (1998). Uncoupling cognitive workload and prefrontal cortical physiology: A PET rCBF study. NeuroImage, 7, 296–303.

    PubMed  Article  Google Scholar 

  29. Goldberg, T. E., Berman, K. F., Randolph, C., Gold, J. M., & Weinberger, D. R. (1996). Isolating the mnemonic component in spatial delayed response: A controlled PET 15O-labelled water regional cerebral blood flow study in normal humans. NeuroImage, 3, 69–78.

    PubMed  Article  Google Scholar 

  30. Goldman-Rakic, P. S. (1987). Circuitry of primate prefrontal cortex and the regulation of behavior by representational memory. In F. Plum & V. Mountcastle (Eds.), Handbook of physiology: Sec. 1. The nervous system: Vol. 5. Higher functions of the brain (pp. 373–417). Bethesda, MD: American Physiological Society.

    Google Scholar 

  31. Goldman-Rakic, P. S. (1994). The issue of memory in the study of prefrontal functions. In A. M. Thierry, J. Glowinski, P. S. Goldman-Rakic, & Y. Christen (Eds.), Motor and cognitive functions of the prefrontal cortex. Berlin: Springer-Verlag.

    Google Scholar 

  32. Goldman-Rakic, P. S. (1995). Architecture of the prefrontal cortex and the central executive. In J. Grafman, K. J. Holyoak, & F. Boller (Eds.), Structure and functions of the human prefrontal cortex (Annals of the New York Academy of Sciences, Vol. 769, pp. 71–83). New York: New York Academy of Sciences.

    Google Scholar 

  33. Grasby, P. M., Frith, C. D., Friston, K. J., Bench, C., Frackowiak, R. S. J., & Dolan, R. J. (1993). Functional mapping of brain areas implicated in auditory-verbal memory function. Brain, 116, 1–20.

    PubMed  Article  Google Scholar 

  34. Grasby, P. M., Frith, C. D., Friston, K. J., Simpson, J., Fletcher, P. C., Frackowiak, R. S. J., & Dolan, R. J. (1994). A graded task approach to the functional mapping of brain areas implicated in auditory-verbal memory. Brain, 117, 1271–1282.

    PubMed  Article  Google Scholar 

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

    Article  Google Scholar 

  36. Honig, W. K. (1978). Studies of working memory in the pigeon. In S. H. Hulse, H. Fowler, & W. K. Honig (Eds.), Cognitive processes in animal behaviour (pp. 211–248). Hillsdale, NJ: Erlbaum.

    Google Scholar 

  37. Jonides, J., Schumacher, E. H., Smith, E. E., Koeppe, R. A., Awh, E., Reuter-Lorenz, P. A., Marshuetz, C., & Willis, C. R. (1998). The role of parietal cortex in verbal working memory. Journal of Neuroscience, 18, 5026–5034.

    PubMed  Google Scholar 

  38. 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.

    PubMed  Article  Google Scholar 

  39. 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.

    PubMed  Article  Google Scholar 

  40. 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 

  41. Kapur, S., Tulving, E., Cabeza, R., McIntosh, A. R., Houle, S., & Craik, F. I. M. (1996). The neural correlates of intentional learning of verbal materials: A PET study. Cognitive Brain Research, 4, 243–249.

    PubMed  Article  Google Scholar 

  42. Levy, R., & Goldman-Rakic, P. S. (1999). Association of storage and processing functions in the dorsolateral prefrontal cortex of the non-human primate. Journal of Neuroscience, 19, 5149–5158.

    PubMed  Google Scholar 

  43. McCarthy, G., Blamire, A. M., Puce, A., Nobre, A. C., Bloch, G., Hyder, F, Goldman-Rakic, P., & Shulman, R G. (1994). Functional magnetic resonance imaging of human prefrontal cortex activation during a spatial working memory task. Proceedings of the National Academy of Sciences, 91, 8690–8694.

    Article  Google Scholar 

  44. McCarthy, G., Puce, A., Constable, R. T., Krystal, J. H., Gore, J. C., & Goldman-Rakic, P. S. (1996). Activation of human prefrontal cortex activation during spatial and nonspatial working memory tasks measured by functional MRI. Cerebral Cortex, 6, 600–611.

    PubMed  Article  Google Scholar 

  45. Milner, B. (1971). Interhemispheric differences in the localisation of psychological processes in man. British Medical Bulletin, 27, 272–277.

    PubMed  Google Scholar 

  46. Olton, D. S. (1982). Spatially organised behaviours of animals: Behavioural and neurological studies. In M. Potegal (Ed.), Spatial abilities (pp. 325–360). New York: Academic Press.

    Google Scholar 

  47. Owen, A. M. (1997). The functional organization of working memory processes within human lateral frontal cortex: The contribution of functional neuroimaging. European Journal of Neuroscience, 9, 1329–1339.

    PubMed  Article  Google Scholar 

  48. Owen, A. M. (in press). The role of the lateral frontal cortex in mnemonic processing: The contribution of functional neuroimaging. Experimental Brain Research.

  49. Owen, A. M., Downes, J. D., Sahakian, B. J., Polkey, C. E., & Robbins, T. W. (1990). Planning and spatial working memory following frontal lobe lesions in man. Neuropsychologia, 28, 1021–1034.

    PubMed  Article  Google Scholar 

  50. Owen, A. M., Doyon, J., Petrides, M., & Evans, A. C. (1996). Planning and spatial working memory examined with positron emission tomography (PET). European Journal of Neuroscience, 8, 353–364.

    PubMed  Article  Google Scholar 

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

    PubMed  Article  Google Scholar 

  52. Owen, A. M., Herrod, N. J., Menon, D. K., Clark, J. C., Downey, S. P. M. J., Carpenter, T. A., Minhas, P. S., Turkheimer, F. E., Williams, E. J., Robbins, T. W., Sahakian, B. J., Petrides, M., & Pickard, J. D. (1999). Redefining the functional organization of working memory processes within human lateral prefrontal cortex. European Journal of Neuroscience, 11, 567–574.

    PubMed  Article  Google Scholar 

  53. Owen, A. M., Morris, R. G., Sahakian, B. J., Polkey, C. E., & Robbins, T. W. (1996). Double dissociations of memory and executive functions in working memory tasks following frontal lobe excisions, temporal lobe excisions or amygdalo-hippocampectomy in man. Brain, 119, 1597–1615.

    PubMed  Article  Google Scholar 

  54. Owen, A. M., Sahakian, B. J., Semple, J., Polkey, C. E., & Robbins, T. W. (1995). Visuo-spatial short term recognition memory and learning after temporal lobe excisions, frontal lobe excisions or amygdalohippocampectomy in man. Neuropsychologia, 33, 1–24.

    PubMed  Article  Google Scholar 

  55. Owen, A. M., Stern, C. E., Look, R. B., Tracey, I., Rosen, B. R., & Petrides, M. (1998). Functional organization of spatial and nonspatial working memory processes within the human lateral frontal cortex. Proceedings of the National Academy of Sciences, 95, 7721–7726.

    Article  Google Scholar 

  56. Paulesu, E., Frith, C. D., & Frackowiak, R. S. J. (1993). The neural correlates of the verbal component of working memory. Nature, 362, 342–345.

    PubMed  Article  Google Scholar 

  57. Petrides, M. (1994). Frontal lobes and working memory: Evidence from investigations of the effects of cortical excisions in nonhuman primates. In F. Boller & J. Grafman (Eds.), Handbook of neuropsychology (Vol. 9, pp. 59–82). Amsterdam: Elsevier.

    Google Scholar 

  58. Petrides, M. (1995). Functional organization of the human frontal cortex for mnemonic processing. In J. Grafman, K. J. Holyoak, & F. Boller (Eds.), Structure and functions of the human prefrontal cortex (Annals of the New York Academy of Sciences, Vol. 769, pp. 85–96). New York: New York Academy of Sciences.

    Google Scholar 

  59. Petrides, M., Alivisatos, B., Evans, A. C., & Meyer, E. (1993). Functional activation of the human frontal cortex during the performance of verbal working memory tasks. Proceedings of the National Academy of Sciences, 90, 878–882.

    Article  Google Scholar 

  60. Petrides, M., & Milner, B. (1982). Deficits on subject-ordered tasks after frontal- and temporal-lobe lesions in man. Neuropsychologia, 20, 249–262.

    PubMed  Article  Google Scholar 

  61. Postle, B. R., Berger, J. S., & D’Esposito, M. (1999). Functional neuroanatomical double dissociation of mnemonic and executive control processes contributing to working memory performance. Proceedings of the National Academy of Sciences, 96, 12950–12964.

    Article  Google Scholar 

  62. Postle, B. R., Stern, C. E., Rosen, B. R., & Corkin, S. (2000). An fMRI investigation of cortical contributions to spatial and nonspatial visual working memory. NeuroImage, 11, 409–423.

    PubMed  Article  Google Scholar 

  63. Rao, S. C., Rainer, G., & Miller, E. K. (1997). Integration of what and where in the primate prefrontal cortex. Science, 276, 821–824.

    PubMed  Article  Google Scholar 

  64. Robbins, T. W., James, M., Owen, A. M., Sahakian, B. J., McInnes, L., & Rabbitt, P. (1998). A study of performance on tests from the CANTAB battery sensitive to frontal lobe dysfunction in a large sample of normal volunteers: Implications for theories of executive function and cognitive ageing. Journal of the International Neuropsychological Society, 4, 474–490.

    PubMed  Article  Google Scholar 

  65. Rushworth, M. F. S., Nixon, P. D., Eacott, M. J., & Passingham, R. E. (1997). Ventral prefrontal cortex is not essential for working memory. Journal of Neuroscience, 17, 4829–4838.

    PubMed  Google Scholar 

  66. Rushworth, M. F. S., & Owen, A. M. (1998). The functional organization of the lateral frontal cortex: Conjecture or conjuncture in the electrophysiology literature. Trends in Cognitive Sciences, 2, 46–53.

    PubMed  Article  Google Scholar 

  67. Rypma, B., Prabhakaran, V., Desmond, J. E., Glover, G. H., & Gabrieli, J. D. E. (1999). Load-dependent roles of frontal brain regions in the maintenance of working memory. NeuroImage, 9, 216–226.

    PubMed  Article  Google Scholar 

  68. Salmon, E., Van der Linden, M., Collette, F., Delfiore, G., Maquet, P., Degueldre, C., Luxen, A., & Franck, G. (1996). Regional brain activity during working memory tasks. Brain, 119, 1617–1625.

    PubMed  Article  Google Scholar 

  69. Schumacher, E. H., Lauber, E., Awh, E., Jonides, J., Smith, E., & Koeppe, R. A. (1996). PET evidence for an amodal verbal working memory system. NeuroImage, 3, 79–88.

    PubMed  Article  Google Scholar 

  70. Smith, E., & Jonides, J. J. (1999). Storage and executive processes in the frontal lobes. Science, 283, 1657–1661.

    PubMed  Article  Google Scholar 

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

    PubMed  Article  Google Scholar 

  72. Smith, E., Jonides, J. 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.

    PubMed  Article  Google Scholar 

  73. Stern, C. E., Owen, A. M., Look, R. B., Tracey, I., Rosen, B. R., & Petrides, M. (2000). Activity in ventrolateral and mid-dorsolateral prefrontal cortex during non-spatial visual working memory processing: Evidence from functional magnetic resonance imaging. NeuroImage, 11, 392–399.

    PubMed  Article  Google Scholar 

  74. Sweeney, J. A., Mintun, M. A., Kwee, S., Wiseman, M. B., Brown, D. L., Rosenberg, D. R., & Carl, J. R. (1996). Positron emission tomography study of voluntary saccadic eye movements and spatial working memory. Journal of Neurophysiology, 75, 454–468.

    PubMed  Google Scholar 

  75. Van der Linden, M., Collette, F., Salmon, E., Delfiore, G., Degueldre, C., Luxen, A., & Franck, G. (1999). The neural correlates of updating of information in verbal working memory. Memory, 7, 549–560.

    PubMed  Article  Google Scholar 

  76. Wilson, F. A. W., Scalaidhe, S. P. O., & Goldman-Rakic, P. S. (1993). Dissociations of object and spatial processing domains in primate prefrontal cortex. Science, 260, 1955–1958.

    PubMed  Article  Google Scholar 

  77. Worsley, K. J., Evans, A. C., Marrett, S., & Neelin, P. (1992). Determining the number of statistically significant areas of activation in subtracted activation studies from PET. Journal of Cerebral Blood Flow & Metabolism, 12, 900–918.

    Article  Google Scholar 

  78. Worsley, K. J., Marrett, S., Neelin, P., Vandal, A. C., Friston, K. J., & Evans, A. C. (1996). A unified statistical approach for determining significant signals in images of cerebral activation. Human Brain Mapping, 4, 58–73.

    PubMed  Article  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Adrian M. Owen.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Owen, A.M., Lee, A.C.H. & Williams, E.J. Dissociating aspects of verbal working memory within the human frontal lobe: Further evidence for a “process-specific” model of lateral frontal organization. Psychobiology 28, 146–155 (2000). https://doi.org/10.3758/BF03331974

Download citation

Keywords

  • Positron Emission Tomography
  • Frontal Cortex
  • Work Memory Task
  • Digit Span
  • Spatial Working Memory