The error-detection mechanism [5] is known to pro-vide a physiological mechanism supporting the stable func-tional state of the body by continuously comparing the actu-al state with the conditional model contained in short-termor long-term memory [1, 5, 6, 8]. Error detection (ED) is anunconscious mechanism controlling the performance quali-ty of stereotypical (routine) types of activity: for example,the feeling of discomfort, such as when leaving the housewith the iron left on or a door left open, a car driver’sresponse to new noises, suddenly feeling “not right” (some-thing wrong). Furthermore, according to Bekhtereva’s con-cept of the ED mechanism, it is stabilizing but not optimiz-ing, and operates both in normal and pathological brainstates [1, 7]. ED can therefore also stabilize pathologicalstates, setting these states as the new “norms” in the opera-tion of the ED mechanism, converting “error detectors” into“error definers” [1, 4]. This led to the hypothesis that obses-sive-compulsive disorder (OCD) is maintained by failure inED operation [4]. In other words, all the power of one of the

basic regulatory mechanisms of the brain is directed in thissituation to resisting efforts to extract the body from thepathological state, which explains the low efficacy of tradi-tional methods for treating these diseases. Thus, the mosteffective and widely used method for treating drug-resistantforms of OCD consists of stereotaxic surgical intervention.These procedures are used because employment of moresparing methods is ineffective. Cingulotomy is an invasiveprocedure and is associated with the risk of post-operativecomplications (like any other neurosurgical intervention).The efficacies of these operations are linked with actions onthe cerebral error detection system, leading to modificationof its operation, allowing the disease to be avoided [4].However, the whole history of psychosurgery shows thatsurgical interventions initially regarded as having goodgrounds are, with further studies of the pathology andassessment of surgical results, providing a fuller under-standing of the mechanisms of the disease replaced by thedevelopment of more sparing therapeutic approaches. Thismakes studies of the cerebral error detector very relevantboth in normal conditions and in pathology. The question ofthe possibility of controlling the operation of the EDremains open.

Neuroscience and Behavioral Physiology, Vol. 43, No. 5, June, 2013

The Brain’s Error-Detecting Mechanism – a PET Study

M. V. Kireev, A. D. Korotkov, Yu. I. Polyakov,A. D. Anichkov, and S. V. Medvedev

0097-0549/13/4305-0613 ©2013 Springer Science+Business Media New York

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Translated from Rossiiskii Fiziologicheskii Zhurnal imeni I. M. Sechenova, Vol. 97, No. 10, pp. 1060–1065,October, 2011. Original article submitted April 23, 2011.

The present study addresses the cerebral support for the mechanism of error detection (ED) operating dur-ing conscious execution of incorrect actions (deceptions) and in the resting state. Local cerebral bloodflow was measured by positron emission tomography (PET), and demonstrated involvement of the ante-rior cingulate gyrus in processes associated with conscious deception. The data obtained here showed thatED operates in persistently executed errors – conscious control of ED was shown to be impossible.The hypothesis that failure of ED is an important factor in the formation of obsessive-compulsive disorder(OCD) was supported by analysis of PET data on the rate of glucose metabolism in the state of operativerest. Normative data from healthy subjects were compared with results obtained from patients with diag-noses of OCD and Tourette’s syndrome. Patients showed decreases in glucose metabolism in the anteriorcingulate gyrus, which can be regarded as a reflection of abnormal functioning of the cerebral ED system.

Keywords: error detection mechanism, conscious deception, obsessive-compulsive disorder.

N. P. Bekhtereva Institute of the Human Brain, Russian Academyof Sciences, 9 Academician Pavlov Street, 197376 St. Petersburg,Russia; e-mail: max@ihb.spb.ru.

The aim of the present work was to study the operationof the cerebral error-detection mechanism both in the con-scious performance of erroneous incorrect actions and inthe resting state.

MethodsA total of 12 healthy right-handed volunteers took part

in the study. Local cerebral blood flow (LBF) was measuredusing 15H2O synthesized at the Radiochemistry Laboratory,Institute of the Human Brain, Russian Academy of Sciences(IChM RAN). Studies were performed by positron emissiontomography (PET) on a PC2048-15B instrument, providing15 simultaneous axial images with spatial resolution of5–6 mm in three planes.

The test task for the present study was the task devel-oped in our previous studies with evoked potentials (EP)[2, 3]. The key feature of the task was that the subject

manipulated an opponent’s actions (a computer) by inde-pendently and consciously taking the decision either todeceive or not. Differences in local cerebral blood flowbetween the two sets of PET conditions during periods ofidentical duration were measured: 1) only truthful actions,and 2) deceitful and truthful actions performed with the aimof forcing the opponent to believe the deceit but not thetruth (i.e., manipulation). The test task was organized insuch a way as to provoke the subject to perform complexactions, simultaneously allowing an equal ratio of deceitfuland truthful actions to be performed [2, 3].

In the second study, PET data from nine patients (aged20–45 years) at operative rest were studied; patients under-went 18F-fluorodeoxyglucose (18-FDG) PET studies for diag-nostic purposes. Data were compared with PET results from11 healthy subjects of comparable age and gender as the studygroup, taken from the normal image collection of the IChM.

Kireev, Korotkov, Polyakov, et al.614

Fig. 1. Error detection mechanism during performance of conscious deceitful actions. A) Evoked potentials during truthful and deceitfulactions. The vertical dotted line shows the moment of keypressing; the thick plot shows deceitful actions and the thin line shows truthfulpresses. The area of statistically significant differences from the EP amplitude component is shaded. B) Increase in local blood flow rate inconscious deceitful actions. The white circle shows the area of the anterior cingulate gyrus traditionally linked with the error detection function.

TABLE 1. Locations of Clusters of Significant Increases in Local Brain Blood Flow in the PET Condition with Manipulations (deceitful and truthful) Comparedto the PET Condition with Truthful Actions

Location Brodman fieldNumber of voxels

in cluster

Coordinates of maximum

x y z

Right superior frontal gyrus 10 328 36 56 8

Medial frontal cortex 10 72 –34 42 6

Anterior cingulate gyrus 32 87 6 24 38

Inferior parietal Cortex 40 380 66 –52 32

Both PET studies were performed using a well describedmethod [7, 18]. PET images were analyzed using the pro-gram SPM 5 (www.fil.ion.ucl.ac.uk/spm). A 12 × 12 × 12 mmGauss spatial filter was used. Statistical maps were construct-ed voxel-by-voxel with a standard threshold of p < 0.05with correction for multiple comparisons using the FDRmethod [13]. Cluster locations in terms of Brodman fieldswere identified using programs developed for SPM5 at theIChM RAN by S. V. Pakhomov (www.ihb.spb.ru/~pet_lab/MSU/MSUMain.html).

ResultsComparison of the PET conditions “manipulation” and

“truthfulness” revealed an increase in LBF in manipulation(deceitful and truthful actions) as compared with trueactions, in the anterior cingulate gyrus (Brodman field (BF)32, in the right and left frontal cortex (BF 10) and the infe-rior temporal cortex (BF 40) (Fig. 1, B; Table 1).

These data point to involvement of the anterior cingu-late gyrus in processes associated with the conscious perfor-mance of incorrect actions (deceit), which may be evidencethat ED is operating. Given that ED may play an importantrole in maintaining pathological states [1, 4], making themresistant to treatment, full investigation of ED requires col-lection of additional data on the state of the ED system not

only during performance of activity, but also in the state ofoperative rest. In addition, in conditions affecting the brain,the functional state of the ED system can change – it hasbeen suggested that one cause of the therapeutic resistanceof OCD lies in failure of ED [4].

With the aim of testing this hypothesis, we performedadditional PET studies using 18F-fluorodeoxyglucose,which allows changes in glucose metabolism to be fol-lowed. Comparison of healthy subjects and OCD patients inthe state of operative rest showed that patients diagnosedwith OCD had a statistically significant decrease in the rateof glucose metabolism in the anterior cingulate gyrus(BF 24/32; Fig. 2; Table 2).

DiscussionOur previous series of experiments showed that con-

scious incorrect actions were characterized by increases inthe amplitude of the negative component of EP with a laten-cy of about 200 msec [2, 3] (Fig. 1, A). Comparison of theseresults with the PET data obtained in the present study indi-cated that the increase in the amplitude of the negative com-ponent recorded on EP in consciously deceitful actions andthe increase in LBF in the anterior cingulate gyrus are man-ifestations of one and the same process (Fig. 1), i.e., activa-tion of the error-detection mechanism during conscious

The Brain’s Error-Detecting Mechanism – a PET Study 615

Fig. 2. Comparison of the rate of glucose metabolism in patients with diagnoses of “obsessive compulsive disorder” and healthysubjects. A) PET image showing significant decrease in glucose metabolism in patients with OCD as compared with the group ofhealthy subjects; B) the dark lines show the location of changes (anterior cingulate gyrus – BF 24/32) in the coordinates of theTalairach stereotaxic atlas [16].

TABLE 2. Locations of Clusters of Significant Decreases in Local Brain Blood Flow in Patients with Diagnoses of OCD (compared with healthy subjects)

Location Brodman fieldNumber of voxels

in cluster

Coordinates of maximum

x y z

Right cingulate gyrus 24/32 214 10 28 32

incorrect actions. This is supported by data pointing to a keyrole for the anterior cingulate gyrus in supporting processesmonitoring actions and detecting errors [9, 15]. This meansthat ED operates even when errors are made consciously.Thus, we report the first evidence of the fundamentalimpossibility of consciously controlling the operation of theED system. This extends our concept of the range of func-tional potentials of ED and supports a relationship betweenits activity and anterior cingulate cortex function.

Our data may provide an explanation for the persis-tence of drug-resistant forms of OCD. This is indicated byresults obtained from comparing PET data from patientswith OCD and the group of healthy subjects, which showedthat OCD is associated with a decrease in the rate of glucosemetabolism in the anterior cingulate gyrus (Fig. 2). Thus,the normal operation of this area in the resting state appearsto be impaired. This may explain the “abnormal” operationof the cerebral error detection system, which is probablythe cause of OCD. In all probability, the hyperactivity of thecingulate gyrus noted in the literature when OCD patientsare involved in activity (activatory explorations) representsincorrect operation of the ED system [10–12, 14, 17].

In relation to this, it should be noted that the locationsof changes in functional activity in both involvement inactivity and at rest are comparable and involve the anteriorcingulate gyrus. This observations allows us to link thesephenomena with the error detection function.

Attention is drawn to the relationship between glucosehypometabolism at rest and hyperactivity during the activestate seen in OCD. It is interesting that such a combinationof manifestations of the functional state could be observedin epilepsy with localized causation: local decreases in glu-cose metabolism in the state of operative rest (PET data)and hyperactivation of this area during epileptic seizures. Inour view, this observation provokes some quite adventurousspeculation. However, it is still premature to discuss possi-ble common or similar pathophysiological mechanisms forthese conditions – verification of this suggestion requiresmore specific studies.

In addition, the fact of a decrease in glucose metabolismin the cingulate gyrus may be useful for understanding theefficacy of stereotaxic cingulotomy. The present studies showthat the functional state of the cingulate gyrus at rest is not atall normal, which may not exclude morphological changesnot yet detected with contemporary diagnostic methods.Thus, the action is on the focus of pathological activity. Theremay be a need to improve the classical concept of functionalstereotaxis as a means of correcting status by means ofactions only on morphologically and functionally intact brainstructures involved in forming the pathological state.

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