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.
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References
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).
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).
D'Esposito, M. et al. The neural basis of the central executive system of working memory. Nature 378, 279–281 (1995).
Fiez, J. A. et al. A positron emission tomography study of the short-term maintenance of verbal information. J. Neurosci. 16, 808–822 (1996).
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).
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).
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).
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).
Smith, E. E., Jonides, J. & Koeppe, R. A. Dissociating verbal and spatial working memory using PET. Cereb. Cortex 6, 11–20 (1996).
Chao, L. L. & Knight, R. T. Prefrontal and posterior cortical activation during auditory working memory. Cog. Brain Res. 4, 27–37 (1996).
Gevins, A. et al. High resolution evoked potential imaging of the cortical dynamics of human working memory. Electroenceph. Clin. Neurophys. 98, 327–348 (1996).
Cohen, J. D. et al. Temporal dynamics of brain activation during a working memory task. Nature 386, 604–608 (1997).
Felleman, D. J. & Van Essen, D. C. Distributed hierarchical processing in the primate cerebral cortex. Cereb. Cortex 1, 1–47 (1991).
Buckner, R. L. Beyond HERA: Contributions of specific prefrontal brain areas to long-term memory retrieval. Psychonom. Bull. Rev. 3, 149–158 (1996).
Haxby, J. V. et al. Face encoding and recognition in the human brain. Proc. Natl Acad. Sci. USA 93, 922–927 (1996).
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).
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).
Paus, T. Location and function of the human frontal eye-field: a selective review. Neuropsychologia 34, 475–483 (1996).
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).
Desimone, R. & Ungerleider, L. G. in Handbook of Neuropsychology (eds Boiler, F. & Grafman, J.) Vol. 2, 267–300 (Elsevier, Amsterdam, 1989).
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).
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).
Miyashita, Y. & Chang, H. S. Neuronal correlate of pictorial short-term memory in the primate temporal cortex. Nature 331, 68–70 (1988).
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).
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).
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).
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).
Friston, K. J. et al. Analysis of fMRI time-series revisited. Neurolmage 2, 45–53 (1995).
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).
Talairach, J. & Tournoux, P. Co-Planar Stereotaxis Atlas of the Human Brain (transl. Rayport, M.) (Thieme Medical, New York, 1988).
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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
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DOI: https://doi.org/10.1038/386608a0
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