Evaluating models of the topographical organization of working memory function in frontal cortex with event-related fMRI
Tóm tắt
Many influential claims about the organization of working memory function in prefrontal cortex (PFC) have been developed and/or tested with functional neuroimaging methods featuring the blocking of behavioral trials and the averaging across blocks of neuroimaging signal. Interpretation of the results of these first-generation neuroimaging studies is subject to several inferential constraints that thereby weaken the models derived from them. We reassessed several models of the functional organization of working memory in PFC by examining or reanalyzing data that were not subject to the same inferential constraints from three event-related fMRI studies of working memory function performed in our laboratory (D’Esposito, Postle, Ballard, & Lease, 1999; Postle, Berger, & D’Esposito, 1999; Postle & D’Esposito, 1999). This process permitted us to reject some of the models derived from first-generation neuroimaging data, to refine others, and to synthesize our results into a revised hybrid model of the working memory functions of PFC.
Tài liệu tham khảo
Aguirre, G. K., Zarahn, E., & D’Esposito, M. (1998). The variability of human, BOLD hemodynamic responses. NeuroImage, 8, 360–369.
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.
Baddeley, A. D. (1986). Working memory. Oxford: Oxford University Press.
Baker, S. C., Frith, C. D., Frackowiak, R. S. J., & Dolan, R. J. (1996). Active representation of shape and spatial location in man. Cerebral Cortex, 6, 612–619.
Belger, A., Puce, A., Krystal, J. H., Gore, J. C., Goldman-Rakic, P. S., & McCarthy, G. (1998). Dissociation of mnemonic and perceptual processes during spatial and nonspatial working memory using fMRI. Human Brain Mapping, 6, 14–32.
Boynton, G. M., Engel, S. A., Glover, G. H., & Heeger, D. J. (1996). Linear systems analysis of functional magnetic resonance imaging in human V1. Journal of Neuroscience, 16, 4207–4221.
Buckner, R. B., Bandettini, P. A., O’Craven, K. M., Savoy, R. L., Petersen, S. E., Raichle, M. E., & Rosen, B. R. (1996). Detection of cortical activation during averaged single trials of a cognitive task using functional magnetic resonance imaging. Proceedings of the National Academy of Sciences, 93, 14878–14883.
Chafee, M. V., & Goldman-Rakic, P. S. (1998). Matching patterns of activity in primate prefrontal area 8a and parietal area 7ip neurons during a spatial working memory task. Journal of Neurophysiology, 79, 2919–2940.
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.
Courtney, S. M., Ungerleider, L. G., Keil, K., & Haxby, J. (1996). Object and spatial visual working memory activate separate neural systems in human cortex. Cerebral Cortex, 6, 39–49.
Della Sala, S., Gray, C., Baddeley, A., Allamano, N., & Wilson, L. (1999). Pattern span: A tool for unwelding visuo-spatial memory. Neuropsychologia, 37, 1189–1199.
D’Esposito, M., Aguirre, G. K., Zarahn, E., & Ballard, D. (1998). Functional MRI studies of spatial and non-spatial working memory. Cognitive Brain Research, 7, 1–13.
D’Esposito, M., & Postle, B. R. (1999). The dependence of span and delayed-response performance on prefrontal cortex. Neuropsychologia, 37, 1303–1315.
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.
D’Esposito, M., Postle, B. R., Berger, J. S., & Taich, A. M. (1999). Quantitative analysis of prefrontal and parietal cortical activity, as measured with event-related fMRI, during discrete components of delayed-response tasks. Society for Neuroscience Abstracts, 25, 1289.
D’Esposito, M., Postle, B. R., & Rypma, B. (in press). Prefrontal cortical contributions to working memory: Evidence from event-related fMRI studies. Experimental Brain Research.
Fox, P. T., Mintun, M. A., Raichle, M. E., Miezin, F. M., Allman, J. M., & Van Essen, D. C. (1986). Mapping human visual cortex with positron emission tomography. Nature, 323, 806–809.
Fox, P. T., Mintun, M. A., Reiman, E. M., & Raichle, M. E. (1988). Enhanced detection of focal brain responses using intersubject averaging and change-distribution analysis of subtracted PET images. Journal of Cerebral Blood Flow & Metabolism, 8, 642–653.
Friston, K. J., Holmes, A. P., Poline, J.-B., Heather, J. D., & Frackowiak, R. S. J. (1995). Analysis of fMRI time-series revisited. NeuroImage, 2, 45–53.
Friston, K. J., Holmes, A. P., & Worsley, K. J. (1999). How many subjects constitute a study? NeuroImage, 10, 1–5.
Friston, K. J., Price, C. J., Fletcher, P., Moore, C., Frackowiak, R. S. J., & Dolan, R. J. (1996). The trouble with cognitive subtraction. NeuroImage, 4, 97–104.
Funahashi, S., Bruce, C. J., & Goldman-Rakic, P. S. (1990). Visuospatial coding in primate prefrontal neurons revealed by oculomotor paradigms. Journal of Neurophysiology, 63, 814–831.
Funahashi, S., Bruce, C. J., & Goldman-Rakic, P. (1993). Dorsolateral prefrontal lesions and oculomotor delayed-response performance: Evidence for mnemonic “scotomas.” Journal of Neuroscience, 13, 1479–1497.
Fuster, J. M. (1997). The prefrontal cortex: Anatomy, physiology, and neuropsychology of the frontal lobe (3rd ed.). Philadelphia: Lippincott-Raven.
Gabrieli, J. D. E., Poldrack, R. A., & Desmond, J. E. (1998). The role of left prefrontal cortex in language and memory. Proceedings of the National Academy of Sciences, 95, 906–913.
Goldman, P. S., & Rosvold, H. E. (1970). Localization of function within the dorsolateral prefrontal cortex of the rhesus monkey. Experimental Neurology, 27, 291–304.
Goldman-Rakic, P. S. (1987). Circuitry of the prefrontal cortex and the regulation of behavior by representational memory. In V. B. Mountcastle, F. Plum, & S. R. Geiger (Eds.), Handbook of neurobiology (pp. 373–417). Bethesda, MD: American Physiological Society.
Gross, C. G. (1963). A comparison of the effects of partial and total lateral frontal lesions on test performance by monkeys. Journal of Comparative & Physiological Psychology, 56, 41–47.
Haxby, J. V., Petit, L., Ungerleider, L. G., & Courtney, S. M. (2000). Distinguishing the functional roles of multiple regions in distributed neural systems for visual working memory. NeuroImage, 11, 380–391.
Henson, R. N. A., Burgess, N., & Frith, C. D. (2000). Recoding, storage, rehearsal and grouping in verbal short-term memory: An fMRI study. Neuropsychologia, 38, 426–440.
Josephs, O., Turner, R., & Friston, K. (1997). Event-related fMRI. Human Brain Mapping, 5, 243–248.
McCarthy, G., Puce, A., Constable, R. T., Krystal, J. H., Gore, J. C., & Goldman-Rakic, P. S. (1996). Activation of human prefrontal cortex during spatial and nonspatial working memory tasks measured by functional MRI. Cerebral Cortex, 6, 600–611.
Mishkin, M., & Manning, F. J. (1978). Non-spatial memory after selective prefrontal lesions in monkeys. Brain Research, 143, 313–323.
Nystrom, L. E., Braver, T. S., Sabb, F. W., Delgado, M. R., Noll, D. C., & Cohen, J. D. (2000). Working memory for letters, shapes and locations: fMRI evidence against stimulus-based regional organization of human prefrontal cortex. NeuroImage, 11, 424–446.
Oster, M. N., Snow, M., Miller, E. K., & Corkin, S. (1997). fMRI activation during performance on object and spatial components of a working memory task. Society for Neuroscience Abstracts, 23, 2110.
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.
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.
Owen, A. M., Iddon, J. L., Hodges, J. R., Summers, B. A., & Robbins, T. W. (1997). Spatial and non-spatial working memory at different stages of Parkinson’s disease. Neuropsychologia, 35, 519–532.
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 processing within the human lateral frontal cortex. Proceedings of the National Academy of Sciences, 95, 7721–7726.
Passingham, R. (1975). Delayed matching after selective prefrontal lesions in monkeys. Brain Research, 92, 89–102.
Paulesu, E., Frith, C. D., & Frackowiak, R. S. J. (1993). The neural correlates of the verbal component of working memory. Nature, 362, 342–345.
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 (pp. 59–82). Amsterdam: Elsevier.
Posner, M. I., Petersen, S. E., Fox, P. T., & Raichle, M. E. (1988). Localization of cognitive operations in the human brain. Science, 240, 1627–1632.
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, 12959–12964.
Postle, B. R., & D’Esposito, M. (1999). “What”-then-“where” in visual working memory: An event-related fMRI study. Journal of Cognitive Neuroscience, 11, 585–597.
Postle, B. R., Jonides, J., Smith, E., Corkin, S., & Growdon, J. H. (1997). Spatial, but not object, delayed response is impaired in early Parkinson’s disease. Neuropsychology, 11, 1–9.
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.
Postle, B. R., Zarahn, E., & D’Esposito, M. (2000). Using event-related fMRI to assess delay-period activity during performance of spatial and nonspatial working memory tasks. Brain Research Protocols, 5, 57–66.
Rainer, G., Asaad, W. F., & Miller, E. K. (1998). Memory fields of neurons in the primate prefrontal cortex. Proceedings of the National Academy of Sciences, 95, 15008–15013.
Rao, S. C., Rainer, G., & Miller, E. K. (1997). Integration of what and where in the primate prefrontal cortex. Science, 276, 821–824.
Richter, W., Ugurbil, K., Georgopoulos, A., & Kim, S.-G. (1997). Time-resolved fMRI of mental rotation. NeuroReport, 8, 3697–3702.
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.
Sarter, M., Berntson, G. G., & Cacioppo, J. T. (1996). Brain imaging and cognitive neuroscience: Toward strong inference in attributing function to structure. American Psychologist, 51, 13–21.
Smith, E. E., & Jonides, J. (1999). Storage and executive processes of the frontal lobes. Science, 283, 1657–1661.
Smith, E. E., Jonides, J., Koeppe, R. A., Awh, E., Schumacher, E. H., & Minoshima, S. (1995). Spatial vs. object working memory: PET investigations. Journal of Cognitive Neuroscience, 7, 337–356.
Smith, E. E., Jonides, J., Marshuetz, C., & Koeppe, R. A. (1998). Components of verbal working memory: Evidence from neuroimaging. Proceedings of the National Academy of Sciences, 95, 876–882.
Tresch, M. C., Sinnamon, H. M., & Seamon, J. G. (1993). Double dissociation of spatial and object visual memory: Evidence from selective interference in intact human subjects. Neuropsychologia, 31, 211–219.
Ungerleider, L. G., Courtney, S. M., & Haxby, J. V. (1998). A neural system for visual working memory. Proceedings of the National Academy of Sciences, 95, 883–890.
Ungerleider, L. G., & Haxby, J. (1994). “What” and “where” in the human brain. Current Opinion in Neurobiology, 4, 157–165.
Ungerleider, L. G., & Mishkin, M. (1982). Two cortical visual systems. In D. J. Ingle, M. A. Goodale, & R. J. W. Mansfield (Eds.), Analysis of visual behavior (pp. 549–586). Cambridge, MA: MIT Press.
Wagner, A. D. (1999). Working memory contributions to human learning and remembering. Neuron, 22, 19–22.
Wilson, F. A. W., O’Scalaidhe, S. P., & Goldman-Rakic, P. S. (1993). Dissociation of object and spatial processing domains in primate prefrontal cortex. Science, 260, 1955–1958.
Woods, R. P. (1996). Modeling for intergroup comparisons of imaging data. NeuroImage, 4, S84–S94.
Worsley, K. J., & Friston, K. J. (1995). Analysis of fMRI time-series revisited—Again. NeuroImage, 2, 173–182.
Zarahn, E., Aguirre, G. K., & D’Esposito, M. (1997a). Empirical analyses of BOLD fMRI statistics: I. Spatially unsmoothed data collected under null-hypothesis conditions. NeuroImage, 5, 179–197.
Zarahn, E., Aguirre, G. K., & D’Esposito, M. (1997b). A trial-based experimental design for fMRI. NeuroImage, 6, 122–138.
Zarahn, E., Aguirre, G. K., & D’Esposito, M. (1999). Temporal isolation of the neural correlates of spatial mnemonic processing with functional MRI. Cognitive Brain Research, 7, 255–268.