Storage and Executive Processes in the Frontal Lobes

A. R. Luria Higher Cortical Functions in Man (Basic Books New York 1966).

Carpenter P. A., Just M. A., Shell P., Psychol. Rev. 97, 404 (1990).

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

P. S. Goldman-Rakic in Handbook of Physiology. Nervous System vol. 5 Higher Functions of the Brain F. Plum Ed. (American Physiological Society Bethesda MD 1987) pp. 373-417.

D. T. Stuss and D. F. Benson The Frontal Lobes (Raven New York 1986).

M. D'Esposito and B. R. Postle Attention and Performance XVIII (Academic Press New York in press).

Posner M. I., Petersen S. E., Fox P. T., Raichle M. E., Science 240, 1627 (1988).

A. Baddeley Working Memory (Clarendon Press/Oxford Univ. Press Oxford 1986).

Smith E. E., Jonides J., Marshuetz C., Koeppe R. A., Proc. Natl. Acad. Sci. U.S.A. 95, 876 (1998).

J. M. Fuster Memory in the Cerebral Cortex: An Empirical Approach to Neural Networks in the Human and Nonhuman Primate (MIT Press Cambridge MA 1995).

Paulesu E., Frith C. D., Frackowiak R. S., Nature 362, 342 (1993).

T. Shallice From Neuropsychology to Mental Structure (MIT Press Cambridge MA 1988).

None of the cited item-recognition studies found activation in DLPFC. However a recent item-recognition experiment found DLPFC activation with a memory load of six items compared with three items which suggests a role for DLPFC with larger memory loads (B. Rypma V. Prabhakaran J. E. Desmond Neuroimage in press). Follow-up work suggests that the role of DLPFC in this task is to mediate executive processes during encoding of the larger loads (M. D'Esposito personal communication).

E. Awh et al. Psychol. Sci. 7 125 (1996).

J. D. Cohen et al. Hum. Brain Mapp. 1 293 (1994).

E. H. Schumacher et al. Neuroimage 3 79 (1996);

Smith E. E., Jonides J., Koeppe R. A., Cereb. Cortex 6, 11 (1996);

10.1006/nimg.1996.0247

; J. D. Cohen et al. Nature 386 604 (1997); J. Jonides et al. J. Cognit. Neurosci. 9 462(1997).

J. A. Fiez et al. J. Neurosci. 16 808 (1996)

J. Jonides et al. ibid. 18 5026 (1998).

10.1126/science.8316836

There is currently some controversy about the degree of separation of object and spatial regions in PFC in nonhuman primates. Recent findings indicate that dorsal or ventral regions can contain neurons that process either spatial or object information or both [

10.1126/science.276.5313.821

Rainer G., Asaad W. F., Miller E. K., Proc. Natl. Acad. Sci. U.S.A. 95, 15008 (1998);

]. However even these studies find some neural segregation—a sizable proportion of neurons tested by Rainer et al. are selective only for location and these neurons predominate in posterior locations.

E. E. Smith et al. J. Cogn. Neurosci. 7 337 (1995)

G. B. McCarthy et al. Proc. Natl. Acad. Sci. U.S.A. 91 8690 (1994);

Courtney S. M., Ungerleider L. G., Keil K., Cereb. Cortex 6, 39 (1996).

Owen A. M., Evans A. C., Petrides M., Cereb. Cortex. 6, 31 (1996).

Faillenot I., Sakata H., Costes N., Neuroreport 8, 859 (1997);

; A. M. Owen et al. Proc. Natl. Acad. Sci. U.S.A. 95 7721 (1998).

10.1038/386608a0

10.1126/science.279.5355.1347

J. Jonides et al. Nature 363 623 (1993); P. A. Reuter-Lorenz et al. in press; references cited in (19 21).

Ungerleider L. G., Courtney S. M., Haxby J. V., Proc. Natl. Acad. Sci. U.S.A. 95, 883 (1998).

Awh E., Jonides J., Reuter-Lorenz P. A., J. Exp. Psychol. Hum. Percept. Perform. 24, 780 (1998).

E. Awh and J. Jonides in The Attentive Brain R. Parasurama Ed. (MIT Press Cambridge MA 1997) pp. 353–380.

Two other recent meta-analyses of neuroimaging studies of working memory also found evidence that PFC is organized by storage versus executive processes [M. D'Esposito et al. Cogn. Brain Res. 7 1 (1998);

Owen A. M., Eur. J. Neurosci. 9, 1329 (1997);

]. However neither of these meta-analyses found evidence that PFC was organized by modality. There are at least two reasons for this discrepancy from the present analyses. Neither of the previous meta-analyses focused on verbal storage or included recent fMRI studies that isolate delay-period activity and that provide relatively strong evidence for a difference between spatial and object storage (22 23).

J. R. Stroop J . Exp. Psychol. 18 643 (1935).

Dyer F. N., Mem. Cogn. 1, 106 (1973);

Cohen J. D., Dunbar K., McClelland J. L., Psychol. Rev. 97, 332 (1990);

Macleod C. M., Psychol. Bull. 109, 163 (1991).

Pardo J. V., Pardo P. J., Janer K. W., Proc. Natl. Acad. Sci. U.S.A. 87, 256 (1990);

; C. J. Bench et al. Neuropsychologia 31 907 (1993);

Carter C. S., Mintun M., Cohen J. D., Neuroimage 2, 264 (1995);

; M. S. George et al. J. Neuropsychol. Clin. Neurosci. 9 55 (1997);

Taylor S. F., Kornblum S., Lauber E. J., Neuroimage 6, 81 (1997);

Derbyshire S. W., Vogt B. A., Jones A. K., Exp. Brain Res. 118, 52 (1998).

Taylor S. F., Kornblum S., Minoshima S., Neuropsychologia 32, 249 (1994);

Iacoboni M., Woods R. P., Mazziotta J. C., J. Neurophysiol. 76, 321 (1996);

Bush G., Whalen P. J., Rosen B. R., Hum. Brain Mapp. 6, 270 (1998).

Jonides J., Smith E. E., Marshuetz C., Koeppe R. A., Reuter-Lorenz P.A., Proc. Natl. Acad. Sci. U.S.A. 95, 8410 (1998).

M. D'Esposito et al. paper presented at Cognitive Neuroscience Society Meeting San Francisco (1998).

C. S. Carter et al. Science 280 74 (1998).

The anterior cingulate is also activated in tasks that do not involve response inhibition indicating that the cingulate serves multiple functions. [

10.1006/nimg.1998.0326

Whalen P. J., et al., Biol. Psychiatry 44, 1219 (1998).

Attention and inhibition may also be involved in self-ordering tasks such as the following: on each series of trials a set of forms is presented in random positions and participants must point to a form they have not selected on a previous trial in that series. This task activates the anterior cingulate and DLPFC similar to tasks that involve attention and inhibition [

Petrides M., Alivisatos B., Evans A. C., Proc. Natl. Acad. Sci. U.S.A. 90, 873 (1993);

]. Some researchers have proposed that self-ordering tasks reflect the executive process of monitoring but alternatively they may involve an appreciable working memory load and some inhibition either of which may cause the frontal activations.

Spector A., Biederman I., Am. J. Psychol. 89, 669 (1976).

M. D'Esposito et al. Nature 378 279 (1995).

J. Talairach and P. Tournoux A Co-Planar Stereotaxic Atlas of the Human Brain: An Approach to Medical Cerebral Imaging (Thieme New York 1988).

J. A. Sweeney et al. J. Neurophysiol. 75 454 (1996).

Supported by grants from the National Institute on Aging and the Office of Naval Research. We are indebted to the members of our laboratory for discussion of these issues and to D. Badre for his substantial contributions to the preparation of this manuscript.