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nature neuroscience • volume 2 no 10 • october 1999 853

The brain implements a variety of cogni-tive processes, which need to functiontogether efficiently. Although routine cog-nitive activities are often relatively auto-matic, more demanding situations mayrequire supervisory mechanisms to coor-dinate multiple sources of information orbehavioral responses. In one laboratorytask used to study this process (the Strooptask), people are asked to name the colorof the ink in which a word is printed,while ignoring the word itself. People areslower to respond when the color of theink and the word’s meaning suggest dif-ferent responses. For example, if the word“red” is printed in blue ink, then the prop-er response would be to say “blue.” How-

regions and the basal ganglia. The poste-rior ACC may be the subdivision that iscrucial for cognitively demanding situa-tions such as the Stroop task3. Functionalneuroimaging and electrophysiologicalstudies have provided support for ACCinvolvement in executive processes bydemonstrating higher levels of activity inthis area during Stroop tasks and situa-tions that require divided attention, con-flict resolution, response monitoring anderror detection1–6. In addition, clinicalstudies have suggested that ACC dysfunc-tions are associated with psychiatric dis-orders, such as obsessive compulsivedisorder and schizophrenia, that are asso-ciated with executive dysfunction7–10.

In this issue of Nature Neuroscience,neuropsychological evidence from Turkenand Swick11 suggests an intriguing alter-native view of the functional architectureof the ACC. They evaluated a patient(D.L.) who had a focal lesion in a circum-

ever, people are slow to say “blue” andoften erroneously say “red” instead. In thissituation, there is a conflict between theresponse suggested by one aspect of thestimulus and the response suggested byanother aspect. Examples of this kind ofconflict abound in everyday life. Forinstance, in driving from one place toanother, one must ignore numerous signsdirecting traffic toward other destinations.A process termed ‘executive control’ isimportant for detecting and resolving thiskind of conflict so that the correctresponse is ultimately produced1,2.

Several lines of research have suggest-ed that the anterior cingulate cortex(ACC), a brain structure located on themedial surface of the frontal lobes, may bea critical neurobiological substrate of suchexecutive control processes. This brainstructure has rich interconnections with anumber of cortical and subcortical brainareas, including association cortex (espe-cially dorsolateral prefrontal, orbitofrontaland parietal), motor systems, limbic

The anterior cingulate cortexlends a hand in responseselectionEdward Awh and William J. Gehring

The anterior cingulate cortex is involved in decisions betweenconflicting response tendencies. This exective function seemsto involve separate pathways for manual and verbal responses.

Edward Awh is in the Department ofPsychology, 1227 University of Oregon, Eugene,Oregon 97403, USA. William Gehring is in theDepartment of Psychology, University ofMichigan, East Hall, 525 East University, AnnArbor, Michigan 48109, USA.e-mail: awh@darkwing.uoregon.edu

several ganglion cells? Signals in adjacentphotoreceptors tend to be correlatedbecause of correlations in the naturalscene. Calculations suggest that, whenpartially correlated signals sum in a gan-glion cell, a dome-like weighting of theinputs leads to an optimal signal-to-noise ratio15. The same might be true formore central mechanisms that sum thepartially correlated signals of ganglioncells. This hypothesis might be testeddirectly using the efficient experimentalsystem that Chichilnisky and Baylor haveprovided.

The structure–function relationshipshown here is unlikely to prove com-pletely general. For example, ganglioncells are known to show nonlinearresponses to certain stimuli, and it wouldbe surprising if these were to be predict-

ed simply from reading the anatomicalcircuit. Similarly, it is unlikely that thefunctions of cortical circuits will be obvi-ous from their wiring, given that corti-cal synapses can undergo plastic changesin their physiological strength. Despitethis, the present results encourage one topress on with the effort to correlatestructure and function.

1. Sterling, P. in Synaptic Organization of theBrain (ed. Shepherd, G. M.) 205–253 (OxfordUniv. Press, New York, 1998).

2. Boycott, B. & Wässle, H. Invest. Ophthalmol.Vis. Sci. 40,1313–1327 (1999).

3. Chichilnisky, E. J. & Baylor, D. A. Nat.Neurosci. 2, 889-893 (1999).

4. Freed, M. A., Smith, R. G. & Sterling, P. Proc.Natl. Acad. Sci. USA 89, 236–240 (1992).

5. Kier, C. K., Buchsbaum, G. & Sterling, P. J. Neurosci. 15, 7673–7683 (1995).

6. Peichl, L. & Wässle, H. J. Physiol. (Lond.) 291,117–141 (1979).

7. Meister, M., Lagnado, L. & Baylor, D. A.Science 270, 1207–1210 (1995).

8. Meister, M., Pine, J. & Baylor, D. A. J. Neurosci. Methods 51, 95–106 (1994).

9. Dacey, D. M. & Lee, B. B. Nature 367, 731–735(1994).

10. Calkins, D. J., Tsukamoto, Y. & Sterling, P. J. Neurosci. 18, 3373–3385 (1998).

11. Velte, T. J. & Masland, R. H. J. Neurophysiol.81, 1412–1417 (1999).

12. Kouyama, N. & Marshak, D. W. J. Neurosci.12, 1233–1252 (1992).

13. Williams, D. R., MacLeod, D. I. & Hayhoe, M.M. Vision Res. 21, 1357–1375 (1981).

14. Curcio, C. A. et al. J. Comp. Neurol. 312,610–624 (1991).

15. Tsukamoto, Y., Smith, R. G. & Sterling, P.Proc. Natl. Acad. Sci. USA 87, 1860–1864(1990).

Anteriorcingulate

cortex

Fig. 1. Mid-sagittal view of the brain, showingthe location of the anterior cingulate cortex.

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854 nature neuroscience • volume 2 no 10 • october 1999

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scribed part of the right ACC caused bysurgical resection of a glioma (Fig. 1). Suchlesions do not generally cause majorbehavioral impairments or large move-ment deficits. The precise nature of thelesion allowed a direct assessment of thecognitive processes that depend on theintegrity of the ACC. The authors exploredan alternative to the executive controlhypothesis of ACC function, in which theACC controls motor responses thatemerge as a result of earlier decisionprocesses rather than coordinating thedecision processes themselves12,13. Turkenand Swick11 tested D.L. in a variety of exec-utive control tasks that activate the ACCin neuroimaging studies. In addition tomanipulating the type of task performedby D.L., they varied the type of motorresponse required for each task (manualor vocal responses). They reasoned that ifthe ACC is responsible for general execu-tive control, then D.L. should be impairedin all tasks with high executive demands;however, if the ACC is responsible for con-trol of motor responses, the results shoulddepend on the motor responses that wererequired. Their results supported the lat-ter hypothesis. Compared to control sub-jects, D.L. was impaired specifically in tasksthat required manual responses, but notin the same tasks when they required vocalresponses.

One task required subjects to view suc-cessive displays of visual stimuli (see Fig.3a of Turken and Swick) and detectchanges in either a single dimension (thatis, attention to color or to shape) or mul-tiple dimensions (attention to color andshape). When D.L. indicated thesechanges with vocal responses, her perfor-mance was within the normal range.However, when manual responses wererequired, D.L. was significantly impairedon all versions of the task, even though thetasks required identical perceptual judg-ments. Another task (Fig. 3b of Turkenand Swick) required subjects to give eithervocal or manual responses to a compos-ite display that consisted of a word (‘left’or ‘right’) and an arrow pointing to theleft or right. Subjects were required toignore one stimulus and respond to theother. Neuroimaging studies have shownthat such tasks activate the ACC, particu-larly in situations where conflict betweenthe relevant and irrelevant stimuli is high1.Both D.L. and the control subjects wereslower to respond when the two stimuliindicated different responses. However,the interference was significantly greaterfor D.L. than for controls—but only whenshe had to make manual responses to the

Another possibility, however, is thatthe command signal originates within theACC. That is, the executive system thatdetects conflicts and errors itself may beorganized according to response modali-ty. Thus, a manual response control sys-tem might detect conflict, facilitate correctresponses and suppress errors in manualresponses without having to interact withthe system in the vocal subdivision of theACC that performs these functions forvocal responses. One would expect that apatient with damage limited to the man-ual subdivision of this system would showmaximal deficits in exactly the conditionswhere patient D.L. has the most difficul-ty: those where correct manual responsesconflict with incorrect manual responses.According to this view, the executiveprocesses that detect conflict or errors andthe processes that control responses neednot be separate from each other, but mayinstead be tightly interwoven within eachmodality1,2,12,13. The data of Turken andSwick11 suggest that at least one part of theexecutive system is organized in a modal-ity-specific fashion, such that the process-es governing manual and vocal responsesare implemented by different regions ofthe ACC10. The command signal may beintact, as Turken and Swick argue, or thecommand signal itself may arise in modal-ity-specific ACC regions. In either case,their finding underscores an importantcharacteristic of ACC organization thathas not been fully appreciated in cogni-tive neuroscience.

1. Carter, C. S.et al. Science 280, 747–749 (1998).

2. Posner, M. I. & DiGirolamo, G. J. in TheAttentive Brain (ed. Parasuraman, R.) 401–423(MIT Press, Cambridge, Massachusetts,1998).

3. Devnisky, O., Morrell, M. J. & Vogt, B. A.Brain 118, 279–306 (1995).

4. Cabeza, R. & Nyberg, L. J. Cogn. Neurosci. 9,1–26 (1997).

5. Dehaene, S., Posner, M. I. & Tucker, D. M.Psychol. Sci. 5, 303–305 (1994).

6. Gehring, W. J., Goss, B., Coles, M. G. H.,Meyer, D. E. & Donchin, E. Psychol. Sci. 4,385–390 (1993).

7. Tamminga, C. A. et al. Arch. Gen. Psychiatry49, 522–530 (1992).

8. Breiter, H. C. et al. Arch. Gen. Psychiatry 53,595–606 (1996).

9. Baer, L. et al. Arch. Gen. Psychiatry 52,384–392 (1995).

10. Gehring, W. J., Himle, J. & Nisenson, L. G.Psychol. Sci. (in press).

11. Turken, A. U. & Swick, D. Nat. Neurosci. 2,920-924 (1999).

12. Paus, T., Petrides, M., Evans, A. C. & Meyer, E.J. Neurophysiol. 70, 453–469 (1993).

13. Paus, T., Koski, L., Caramanos, Z. & Westbury,C. Neuroreport 9, R37–47 (1998).

words. When vocal responses wererequired, D.L. showed the same amountof interference as controls. In both tasks,D.L.’s impairment surfaced as a functionof the output modality rather than as afunction of the judgments that had to bemade.

One crucial aspect of these data is thatD.L.’s impairment was most evident whenresponse selection requirements weremost demanding: when fast and accurateresponding required not only the initia-tion of the correct response, but also thesuppression or abandonment of compet-ing, erroneous responses. For example,whereas D.L. was impaired during all themanual response conditions of the divid-ed attention task, she showed the greatestimpairment during the manual responsecondition that required attention to mul-tiple attributes. In this condition, theresponse suggested by one attendedattribute may not have been the same asthat suggested by the other, causing agreater demand for executive processes toselect from multiple responses. Similarly,during the Stroop conflict task, D.L.’sabnormal interference levels were highestin the manual response condition thatinvolved the highest level of conflict (aninterpretation supported by the greaterdifficulty control subjects had in the samecondition). Thus, although D.L.’s deficitwas associated with manual responses, thedegree of difficulty in selecting the manualresponses was also critical.

The specific impairment of manualresponses following a restricted lesion tothe posterior part of the ACC in D.L. sug-gests that manual and vocal responses aremediated by independent parts of theACC. This view is in line with previousneuroimaging evidence for somatotopicorganization of the ACC (that is, differ-ent parts of the ACC activated duringmanual, vocal and oculomotor respons-es)10,12. This idea has important implica-tions for theories of ACC function andexecutive control. Turken and Swickreport that D.L. showed “intact executivefunction,” along with impairment in theinitiation and control of manual respons-es. They suggest that a command signalindicating the need for executive controloriginates in a lateral prefrontal system,rather than in the ACC. According to thisview, the prefrontal command signal caus-es a modality-specific portion of the ACCto facilitate correct responses and to sup-press errors12. Turken and Swick proposethat in D.L. the command signal is intact,but the ACC is unable to facilitate or sup-press responses appropriately.

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