An area specialized for spatial working memory in human frontal cortex

Science

Volumn 279, Issue 5355, 1998, Pages 1347-1351

  Courtney, Susan M ^a   Petit, Laurent ^a   Maisog, José Ma ^a   Ungerleider, Leslie G ^a   Haxby, James V ^a  

^a NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; FRONTAL CORTEX; MEMORY; MENTAL TASK; MONKEY; NUCLEAR MAGNETIC RESONANCE IMAGING; PREFRONTAL CORTEX; PRIORITY JOURNAL; SPATIAL MEMORY;

ANIMALS; BRAIN MAPPING; EVOLUTION; FEMALE; FRONTAL LOBE; HAPLORHINI; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MEMORY, SHORT-TERM; PREFRONTAL CORTEX; PSYCHOMOTOR PERFORMANCE; SACCADES; SPACE PERCEPTION;

EID: 0032570786     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.279.5355.1347     Document Type: Article

References (43)

1. J. M. Fuster, The Prefrontal Cortex: Anatomy, Physiology, and Neuropsychology of the Frontal Lobe (Raven Press, New York, 1989); S. Funahashi and K. Kubota, Neurosci. Res. 21, 1 (1994); P. S. Goldman-Rakic, Neuron 14, 477 (1995).
2. J. M. Fuster, The Prefrontal Cortex: Anatomy, Physiology, and Neuropsychology of the Frontal Lobe (Raven Press, New York, 1989); S. Funahashi and K. Kubota, Neurosci. Res. 21, 1 (1994); P. S. Goldman-Rakic, Neuron 14, 477 (1995).
3. J. M. Fuster, The Prefrontal Cortex: Anatomy, Physiology, and Neuropsychology of the Frontal Lobe (Raven Press, New York, 1989); S. Funahashi and K. Kubota, Neurosci. Res. 21, 1 (1994); P. S. Goldman-Rakic, Neuron 14, 477 (1995).
4. E. E. Smith et al., J. Cogn. Neurosci. 7, 337 (1995).
5. J. A. Fiez et al., J. Neurosci. 16, 808 (1996).
6. G. McCarthy et al., Cereb. Cortex 6, 600 (1996); M. Petrides and B. Milner, Neuropsychologia 20, 249 (1982).
7. G. McCarthy et al., Cereb. Cortex 6, 600 (1996); M. Petrides and B. Milner, Neuropsychologia 20, 249 (1982).
8. A. M. Owen, A. C. Evans, M. Petrides, Cereb. Cortex 6, 31 (1996).
9. J. D. Cohen et al., Nature 386, 604 (1997).
10. S. M. Courtney, L. G. Ungerleider, K. Keil, J. V. Haxby, ibid., p. 608 (1997).
11. S. C. Rao, G. Rainer, E. K. Miller, Science 276, 821 (1997).
12. F. A. Wilson, S. P. O'Scalaidhe, P. S. Goldman-Rakic, ibid. 260, 1955 (1993).
13. In the monkey, physiological maps of the FEF based on single-unit activity (30) and low-threshold microstimulation (37) demonstrated that the FEF occupies the anterior bank of the arcuate sulcus, from the lip of the prearcuate gyrus to the floor of the sulcus, a region generally considered to be BA 8. Stanton et al. (32) showed that the FEF can also be identified histologically as the region in the anterior bank of the arcuate sulcus containing the highest concentration of large layer V pyramidal cells. They considered it to be a separate cytoarchitectonic area that straddles the border between BA 6 and BA 8.
14. G. McCarthy et al., Proc. Natl. Acad. Sci. U.S.A. 91, 8690 (1994).
15. E. E. Smith, J. Jonides, R. A. Koeppe, Cereb. Cortex 6, 11 (1996).
16. E. A. Walker, J. Comp. Neurol. 73, 59 (1940).
17. J. V. Haxby, L. G. Ungerleider, B. Horwitz, S. I. Rapoport, C. L. Grady, Hum. Brain Mapp. 3, 68 (1995).
18. S. M. Courtney, L. G. Ungerleider, K. Keil, J. V. Haxby, Cereb. Cortex 6, 39 (1996).
19. A. M. Owen, Eur. J. Neurosci. 9, 1329 (1997).
20. T. Paus, Neuropsychologia 34, 475 (1996); J. A. Sweeney et al., J. Neurophysiol. 75, 454 (1996); L. Petit, V. P. Clark, J. Ingeholm, J. V. Haxby, ibid. 77, 3386 (1997);
21. T. Paus, Neuropsychologia 34, 475 (1996); J. A. Sweeney et al., J. Neurophysiol. 75, 454 (1996); L. Petit, V. P. Clark, J. Ingeholm, J. V. Haxby, ibid. 77, 3386 (1997);
22. T. Paus, Neuropsychologia 34, 475 (1996); J. A. Sweeney et al., J. Neurophysiol. 75, 454 (1996); L. Petit, V. P. Clark, J. Ingeholm, J. V. Haxby, ibid. 77, 3386 (1997);
23. B. Luna et al., Cereb. Cortex 8, 40 (1998).
24. L. Petit et al., J. Neurosci. 16, 3714 (1996).
25. J. Jonides et al., Nature 363, 623 (1993).
26. S. C. Baker, C. D. Frith, R. S. J. Frackowiak, R. J. Dolan, Cereb. Cortex 6, 612 (1996).
27. E. Mellet et al., J. Neurosci. 16, 6504 (1996).
28. J. V. Haxby, J. M. Maisog, S. M. Courtney, in Mapping and Modeling the Human Brain, P. Fox, J. Lancaster, K. Friston, Eds. (Wiley, New York, in press); A. C. Rencher Methods of Multivariate Analysis (Wiley, New York, 1995).
29. J. V. Haxby, J. M. Maisog, S. M. Courtney, in Mapping and Modeling the Human Brain, P. Fox, J. Lancaster, K. Friston, Eds. (Wiley, New York, in press); A. C. Rencher Methods of Multivariate Analysis (Wiley, New York, 1995).
30. Both precentral and superior frontal sulci in each hemisphere were anatomically defined in each subject by using their Talairach normalized axial structural MR images from 39 to 55 mm above the bicommissural plane, based on the extent of FEF activation in previous studies (17). The region of interest delineating the precentral sulcus included 6 mm of the cortex on each bank of the sulcus from, and including, the junction with the superior frontal sulcus to the lateral convexity. The region of interest delineating the superior frontal sulcus included 6 mm of the cortex along each of the banks of the sulcus from the limit of the precentral region of interest forward to the anterior convexity. The inferior and middle frontal cortical regions of interest were broadly defined as all cortex anterior to the 6 mm of cortex on the anterior bank of the precentral sulcus from 38 to 16 mm above the bicommissural plane for the middle frontal cortex and from 15 mm above to 12 mm below the bicommissural plane for the inferior frontal cortex. The division between middle and inferior frontal regions was chosen to be midway between the mean locations of all areas reported as BA 45 or 47 and all areas reported as BA 9 or 46 in recent working memory imaging reviews (3, 16). These ventral regions were defined once for all subjects by using the aver-age of all 11 subjects' structural MR images. Thus, this analysis did not include medial and orbital frontal regions; neither of these regions showed content-specific sustained activity.
31. 3 and 0.39 and 0.25% in the inferior frontal cortex (medians across subjects; P > 0.1 for all comparisons).
32. Others (2, 4, 20) have also directly contrasted object and spatial working memory and, as we did, they found evidence for domain specificity in prefrontal cortex. However, their evidence indicated that domain specificity is primarily a hemispheric laterally effect, with left frontal regions specialized for object working memory and right frontal regions specialized for spatial working memory. In our previous studies of face (7, 14) and in this study of spatial working memory, we found activations with similar coordinates, but the activations tended to be bilateral. Smith ef al. (2) attributed the left lateralization of object working memory to rehearsal of a symbolically or linguistically encoded representation of the object. In this study and previously (14) we have seen left lateralization for face working memory under conditions that encouraged more symbolic or verbal encoding of faces, but we have also seen right lateralization under conditions that allowed for more image-based encoding (14, 15). We argue that laterally effects in visual memory may be influenced by a variety of factors, such as memory set size, retention interval length, and item familiarity, all of which may affect the extent to which subjects engage in symbolic or verbal encoding and rehearsal.
33. Whereas activation in the superior frontal sulcus was overwhelmingly associated with sustained activity during spatial working memory (89% of activated cortex), activation in the precentral sulcus was a mixture of voxels demonstrating sustained (53%) and transient (43%) activity during working memory as well as saccade-related activity (74%; median percentages for four subjects include overlap). The presence of both sustained and transient activity in the precentral sulcus at the level of the FEF is consistent with results of physiological studies in monkeys that have demonstrated that some FEF neurons show sustained activity during fixation or during the delays in memory-guided saccade tasks, and others show transient activity during saccadic and pursuit eye movements (27, 33). Transient activity observed in the precentral sulcus is likely to be related to eye movements to the locations where pictures appeared, because subjects were instructed to look directly at each picture as it was shown and to avoid moving their eyes during delay periods. Regions of the precentral sulcus activated by the spatial working memory task but not by the saccadic eye movement task may be related to mechanisms of oculomotor control other than those controlling horizontal saccades. However, it is highly unlikely that sustained activity in the superior frontal sulcus is related to oculomotor control because current and previous eye movement studies in humans have localized activity related to visually guided saccades, self-paced saccades, smooth pursuit, and fixation within or posterior to the precentral sulcus and not within the superior frontal sulcus (17, 18).
34. S. Funahashi, C. J. Bruce, P. S. Goldman-Rakic, J. Neurophysiol. 61, 331 (1989).
35. L. G. Ungerleider and J. V. Haxby Curr. Opin. Neurobiol. 4, 157 (1994); L. G. Ungerleider, Science 270, 769 (1995).
36. L. G. Ungerleider and J. V. Haxby Curr. Opin. Neurobiol. 4, 157 (1994); L. G. Ungerleider, Science 270, 769 (1995).
37. D. T. Stuss and D. F. Benson, The Frontal Lobes (Raven Press, New York, 1986).
38. C. J. Bruce and M. E. Goldberg, J. Neurophysiol. 53, 603 (1985).
39. -, ibid. 54, 714 (1985).
40. G. B. Stanton, S.-Y. Deng, M. E. Goldberg, N. T. McMullen, J. Comp. Neurol. 282, 415 (1989).
41. M. E. Goldberg and M. A. Segraves, in The Neurobiology of Saccadic Eye Movements, R. H. Wurtz and M. E. Goldberg, Eds. (Elsevier, Amsterdam, 1989), p. 283; J. P. Gottlieb et al., J. Neurophysiol. 72, 1634 (1994).
42. M. E. Goldberg and M. A. Segraves, in The Neurobiology of Saccadic Eye Movements, R. H. Wurtz and M. E. Goldberg, Eds. (Elsevier, Amsterdam, 1989), p. 283; J. P. Gottlieb et al., J. Neurophysiol. 72, 1634 (1994).
43. The authors thank R. Desimone and A. Martin for comments on an earlier draft of the manuscript; E. Hoffman and J. Schouten for help with subject recruitment, scheduling, and training; and P. Jezzard and the staff of the NIH In Vivo NMR Center for assistance with MR scanning.