Abstract

In the monkey, 3 motor areas have been identified in the cortex occupying the banks of the cingulate sulcus (cgs): A rostral cingulate motor area and 2 caudal cingulate motor areas, 1 located in the dorsal bank and the other in the ventral bank of the sulcus. The homologs of these 3 cingulate motor areas in the human brain are poorly understood. The present functional magnetic resonance imaging study examined the anatomo-functional organization of the cingulate motor areas in the human brain. A subject by subject analysis revealed the existence of 3 motor areas along the cgs and these areas appear to be somatotopically organized. Importantly, these 3 motor areas relate to the specific morphological features of the cingulate/paracingulate cortex. These results demonstrate the location and organization of the 3 cingulate motor areas in the human brain and suggest a well-preserved organization of these motor areas from the monkey to the human brain.

Introduction

In the macaque monkey, 3 motor areas can be identified within the cingulate cortex: A rostral motor area (CMAr) located on both banks of the cingulate sulcus (cgs) and 2 caudal motor areas (CMAc), 1 located in the ventral bank (CMAv) and 1 in the dorsal bank (CMAd) of the cgs. These motor areas are located in the central part of the cgs, below and just in front of the medial extension of the primary somatomotor area and the supplementary motor area (SMA). Anatomical studies have shown direct connectivity of these motor areas with the ventral horn of the spinal cord, the primary motor cortex, and the premotor cortex (Hutchins et al. 1988; Dum and Strick 1991; Luppino et al. 1991; Shima et al. 1991; Morecraft and Van Hoesen 1992; Galea and Darian-Smith 1994; He et al. 1995; Dum and Strick 1996). These 3 areas appear to be somatotopically organized and to contain forelimb, hindlimb (Luppino et al. 1991; Shima et al. 1991; Wang et al. 2001), and face (Mitz and Godschalk 1989; Luppino et al. 1991; Morecraft et al. 1996; Wang et al. 2001) representations. Intracortical microstimulation has shown that CMAr contains a face, a hand, and a leg representation, that CMAv contains a hand and a leg representation, and that CMAd contains 2 arm representations and a leg representation (Luppino et al. 1991; Dum and Strick 1993).

Only a few functional neuroimaging studies suggested the existence of human cingulate motor zones. In an early positron emission tomography study, Grafton et al. (1993) provided some evidence for 1 motor area in the ventral bank of the cgs, exhibiting finger representation anterior to the shoulder representation. In a functional magnetic resonance imaging (fMRI) study aimed at examining pain representation and using nonpainful and painful electric stimulation, Arienzo et al. (2006) have, indirectly, provided evidence of a motor representation of the wrist located more anteriorly than a representation of the malleolus in the anterior cingulate cortex. Picard and Strick, based on meta-analysis of various studies that involved movement and had activations in the cingulate region, suggested the existence of 3 cingulate motor regions in the human brain (Picard and Strick 1996, 2001). Thus, there is some evidence that more than 1 cingulate motor area may exist in the human brain, but a direct and detailed examination focused on uncovering their precise number and organization, and how these areas may relate to the complex sulcal/gyral morphology of the human cingulate region is lacking. It was hypothesized that there might be links between morphological variability and specific functional activations since such links have already been successfully described in both the dorsal premotor cortex (Amiez et al. 2006) and the inferior frontal junction (Derrfuss et al. 2012).

The aim of the present functional neuroimaging study was 3-fold: 1) to shed light on the number of motor areas along the antero-posterior extent of the cgs in the human brain, 2) to examine whether specific motor areas relate to the variability of the sulcal anatomy in the cingulate region, and 3) to find out whether there is evidence for somatotopic organization of any human cingulate motor areas. Twelve human subjects were scanned with fMRI, while they performed hand, foot, mouth, and saccadic eye movements. Importantly, the data were analyzed on a subject by subject basis allowing us to examine the location of activation foci due to particular body movements in relation to particular aspects of the morphological anatomy of the cingulate region in individual subjects.

The results demonstrated that there are 3 motor areas along the antero-posterior extent of the human cgs, suggesting a well-preserved organization of the cingulate motor areas from the monkey to the human brain. A major finding is the discovery that these 3 motor areas relate to specific sulcal features of the cingulate/paracingulate cortical region in individual brains. Finally, there is clear evidence of somatotopic organization of these cingulate areas in the human brain, consistent with the macaque monkey data.

Material and Methods

Subjects

Twelve healthy volunteers (8 females and 4 males, mean age = 29 years ± 6.6 standard deviation) participated in this fMRI study. All volunteers were right handed. Informed written consent was obtained from all the participants according to the institutional guidelines established by the Ethics Committee of the Montreal Neurological Hospital and Institute.

Paradigms

To establish the locations of the different motor areas in the cgs, subjects performed hand, arm, foot, leg, mouth, tongue, eye blinking, and saccadic eye movements.

A sentence was presented on the screen for 1.5 s indicating to the subject the type of movement that they would have to perform in the trial (i.e. instruction period). After a delay varying from 4 to 6 s, a fixation point was presented for 5 s. The occurrence of this fixation point instructed the subject to perform the movement indicated in the instruction period, while maintaining eye fixation during the performance of the required movements. The disappearance of the fixation point 5 s later instructed the subject to stop performing the movement. The type of movement required was indicated as follows: The sentence “move your tongue” instructed the subjects to perform circular movements with their tongue without opening the mouth. The sentence “move your mouth” instructed the subjects to perform circular movements with their mouth with the mouth closed. The sentences “move your left hand” and “move your right hand” instructed the subjects to perform up and down small amplitude movements (maximum 20°) with their left or right hand straight, without moving the fingers and the wrist. The sentences “move your left arm” and “move your right arm” instructed the subjects to perform up and down small amplitude movements (maximum 10s°) with their left or right arm, keeping the arm, hand, and fingers straight. The sentences “move your left foot” and “move your right foot” instructed the subjects to perform up and down small amplitude movements (maximum 20°) with their left or right foot straight, without moving the toes and the ankle. The sentences “move your left leg” and “move your right leg” instructed the subjects to perform up and down small amplitude movements (maximum 10°) with their left or right leg, keeping the leg, foot, and toes straight. The sentence “do eye blinking” instructed the subjects to perform eye blinking movements. Note that the protocol was slightly different for the assessment of the eye fields since the subjects were asked to perform saccadic eye movements. In this case, the sentence “follow the dot: saccade” indicated to the subjects that, after the 4–6 s delay, they would have to perform a saccade to follow a dot presented in 1 of 3 possible locations on the screen (left, middle, or right), for 22.5 s. Each dot appeared for 750 ms at each location. This protocol has been described in detail in Amiez et al. (2006) and Amiez and Petrides (2009). Finally, the control condition was instructed by the sentence “fixate on the dot” in which the subject had to maintain an ocular fixation on the dot presented in the center of the screen during 22.5 s. After the movements, an intertrial interval varying from 8 to 10 s was presented. The presentation of the stimuli was controlled with E-prime 1.2 (Psychology Software Tools Inc.).

Note that, once installed in the scanner and prior the beginning of the scanning, subjects were asked to perform the different hand, arm, foot, and leg movements to check that the amplitude of the arm/leg and hand/foot was <20° and 10°, respectively.

Contrasts

The brain regions exhibiting increased activity in relation to the performance of each type of movement were assessed by comparing the blood oxygen level-dependent (BOLD) signal during the performance of each type of movements with the ocular fixation trials. In the present article, we focused our analysis on the following contrasts: Saccadic eye movements versus ocular fixation, tongue movements versus ocular fixation, left or right hand movements versus ocular fixation, and left or right foot movements versus ocular fixation.

The cartography of the cingulate cortex in the right hemisphere was assessed with the contrasts saccadic eye movements versus ocular fixation, tongue movements versus ocular fixation, left hand movements versus ocular fixation, and left foot movements versus ocular fixation. The cartography of the cingulate cortex in the left hemisphere was assessed with the contrasts saccadic eye movements versus ocular fixation, tongue movements versus ocular fixation, right hand movements versus ocular fixation, and right foot movements versus ocular fixation.

MRI Acquisition

Scanning was performed on a 3-T Siemens Magnetom TrioTim MRI Scanner (Siemens AG, Erlangen, Germany). Subjects wore earplugs during the scanning. A vacuum cushion was installed under the subjects' head to avoid as much as possible the impact of limb movements onto the head. After a high-resolution T1 anatomical scan (whole head, 1 mm³ isotropic resolution), 7–8 runs of 170 images each (30 horizontal T2* gradient echo-planar images (EPI), base resolution matrix = 128, voxel size = 2 × 2 × 2 mm, repetition time = 2.1 s, echo time = 30 ms, flip angle = 90°) sensitive to the BOLD signal were acquired. The field of view covered the medial wall. Visual stimuli were presented through an LCD projector with a mirror. Each subject was required to complete 5 (1 subject), 6 (3 subjects), or 7 (8 subjects) runs of fMRI data collection during the scanning session, each one lasting approximately 7 min. In each run, all the subjects performed the following blocks of trials presented randomly in successive fMRI runs: 22.5 s saccadic eye movements, 5 s mouth movements (i.e. about 5 rotations), 5 s tongue movements (i.e. about 5 rotations), 5 s left leg movements (i.e. about 8 up and down movements), 5 s right leg movements (i.e. about 8 up and down movements), 5 s left foot movements (i.e. about 8 up and down movements), 5 s right foot movements (i.e. about 8 up and down movements), 5 s left arm movements (i.e. about 8 up and down movements), 5 s right arm movements (i.e. about 8 up and down movements), 5 s left hand movements (i.e. about 8 up and down movements), 5 s right hand movements (i.e. about 8 up and down movements), 5 s eye blinking movements (i.e. about 8 blinking), and 22.5 s ocular fixation. The presentation of each instruction sentence was synchronized with the scanner acquisition via a trigger signal generated by the scanner.

Data Analysis

Preprocessing and data analysis were performed with Statistical Parametric Mapping software (SPM8B; Wellcome Department of Cognitive Neurology, University of College London, London, United Kingdom; http://www.fil.ion.ucl.ac.uk/spm) and Matlab 7.9 (www.mathworks.com).

First, the first 3 volumes of each run were removed to allow for T1 equilibrium effects. We applied a slice-timing correction using the time center of the volume as reference. Then, head motion correction was applied using rigid-body realignment. These realignment parameters were used as covariates during the statistical analysis to model out potential nonlinear head motion artifacts. Functional and morphological images were spatially normalized into standard MNI space using SPM's default templates. Finally, functional images were smoothed using a 6-mm full-width half maximum Gaussian kernel (Friston, Firth, Frackowiak et al. 1995; Friston, Firth, Turner et al. 1995; Friston, Holmes et al. 1995). A 128-s temporal “high-pass filter” regressor set was included in the design matrix to exclude low-frequency confounds.

Each trial was modeled with impulse regressors at the time of the presentation of the fixation point instructing the performance of the left/right hand movements, left/right arm movements, left/right foot movements, left/right leg movements, tongue movements, saccadic eye movements, eye blinking movements, or ocular fixation. These regressors were then convolved with the canonical hemodynamic response function and entered into a general linear model (GLM) of each subject's fMRI data. The 6 scan-to-scan motion parameters produced during realignment were included as additional regressors in the GLM to account for residual effects of subject movement.

The contrasts were thresholded using the minimum given by a Bonferroni correction and random field theory to account for multiple comparisons. The significance was assessed on the basis of the spatial extent of consecutive voxels. Concerning the group analysis, for a single voxel in an exploratory search involving all peaks within an estimated gray matter of 600 cm³ covered by the slices, the threshold for reporting a peak as significant (P < 0.05) was t = 6.23 if the peaks were predicted. In addition, a cluster volume extent >196.86 mm³ with a t-value >3 was significant (P < 0.05) corrected for multiple comparisons using the method of Friston, Holmes et al. (1995). For the individual subject analysis, we conducted a region of interest (ROI) analysis. The assessed ROI comprised the cingulate/paracingulate complex, the SMA, and the supplementary eye field (SEF). It has been shown that this ROI has a volume of 15.96 and 16.92 cm3 in the right and left hemispheres, respectively (volume of the cingulate/paracingulate complex = 12.38 cm3 in the right hemisphere and 12.70 cm3 in the left hemisphere, Paus, Otaky et al. 1996; volume of the SMA = 3.58 cm3 in the right hemisphere and 4.22 m3 in the left hemisphere, Makris et al. 2006). In this ROI, the threshold for reporting a peak as significant (P < 0.05) was t = 4.050 (right hemisphere) and t = 4.066 (left hemisphere) if the peaks were predicted. In addition, in this ROI, a predicted cluster of voxels with a t-value >2 and with a volume extent >264.07 mm3 (right hemisphere) and 270.40 mm3 (left hemisphere) was significant (P < 0.05), corrected for multiple comparisons using the method of Friston, Holmes et al. (1995).

Results

Morphological Features of the Cingulate/Paracingulate Region in the Participants

In the monkey, the cgs is a long simple sulcus that proceeds from the anterior part of the corpus callosum all the way posteriorly. In the human brain, the cgs is more complex and is frequently divided into several antero-posterior segments. In addition, in the medial frontal lobe, an additional cgs often appears, which is referred to as the paracgs (pcgs) (Vogt et al. 1995; Paus, Tomaiuolo et al. 1996; Vogt et al. 2005; Fornito et al. 2008). Three vertical paracingulate sulci joining either the cgs or the pcgs can be distinguished. The most posterior of these sulci is the paracentral sulcus (pacs), followed by the pre-paracentral sulcus (prpacs), and then the vertical pcgs (vpcgs), which is the most anterior.

Eleven of our subjects display only a cgs at least in 1 hemisphere (with S3, S4, S5, S9, and S12 exhibiting a cgs bilaterally) and 7 of them (S1, S2, S6, S7, S8, S10, and S11) display a pcgs at least in 1 hemisphere (with S2 exhibiting a pcgs bilaterally; Table 1 for a complete description of the anatomical characteristics of the cgs and pcgs in individual subjects). Thus, a pcgs was observed in at least 1 hemisphere in 58% of subjects, in agreement with the literature (Paus, Otaky et al. 1996; Paus, Tomaiuolo et al. 1996; Fornito et al. 2008; Buda et al., 2011).

Table 1

Morphology of the cingulate/paracingulate sulcal complex in individual subjects

 Cgs/pcgs Pcgs starts at y coordinates Cgs segmented or not Pcgs segmented or not 
Right hemisphere 
 Subject 1 Cgs  Not  
 Subject 2 Cgs and pcgs 32 Not Not 
 Subject 3 Cgs  3 segments  
 Subject 4 Cgs  2 segments  
 Subject 5 Cgs  Not  
 Subject 6 Cgs  Not  
 Subject 7 Cgs and pcgs Not Not 
 Subject 8 Cgs  Not  
 Subject 9 Cgs  2 segments  
 Subject 10 Cgs  Not  
 Subject 11 Cgs  Not  
 Subject 12 Cgs  Not  
Left hemisphere 
 Subject 1 Cgs and pcgs −4 Not 2 segments 
 Subject 2 Cgs and pcgs 18 Not Not 
 Subject 3 Cgs  Not  
 Subject 4 Cgs  Not  
 Subject 5 Cgs  Not  
 Subject 6 Cgs and pcgs −2 Not 2 segments 
 Subject 7 Cgs  Not  
 Subject 8 Cgs and pcgs Not 2 segments 
 Subject 9 Cgs  3 segments  
 Subject 10 Cgs and pcgs Not 2 segments 
 Subject 11 Cgs and pcgs −2 Not 2 segments 
 Subject 12 Cgs  Not  
 Cgs/pcgs Pcgs starts at y coordinates Cgs segmented or not Pcgs segmented or not 
Right hemisphere 
 Subject 1 Cgs  Not  
 Subject 2 Cgs and pcgs 32 Not Not 
 Subject 3 Cgs  3 segments  
 Subject 4 Cgs  2 segments  
 Subject 5 Cgs  Not  
 Subject 6 Cgs  Not  
 Subject 7 Cgs and pcgs Not Not 
 Subject 8 Cgs  Not  
 Subject 9 Cgs  2 segments  
 Subject 10 Cgs  Not  
 Subject 11 Cgs  Not  
 Subject 12 Cgs  Not  
Left hemisphere 
 Subject 1 Cgs and pcgs −4 Not 2 segments 
 Subject 2 Cgs and pcgs 18 Not Not 
 Subject 3 Cgs  Not  
 Subject 4 Cgs  Not  
 Subject 5 Cgs  Not  
 Subject 6 Cgs and pcgs −2 Not 2 segments 
 Subject 7 Cgs  Not  
 Subject 8 Cgs and pcgs Not 2 segments 
 Subject 9 Cgs  3 segments  
 Subject 10 Cgs and pcgs Not 2 segments 
 Subject 11 Cgs and pcgs −2 Not 2 segments 
 Subject 12 Cgs  Not  

Note: As in previous studies, the paracingulate sulcus was classified as present when there was a clear identifiable sulcus running dorsal and parallel to the cgs for 3 consecutive sagittal slices and was at least 20 mm in length (Fornito et al. 2008). Abbreviations: cgs, cingulate sulcus; pcgs, paracingulate sulcus.

Assessment of Motion Artifacts

Although the 6 scan-to-scan motion parameters produced during realignment were included as additional regressors in the GLM to account for residual effects of subject movement, we assessed in detail the impact of the small amplitude limb movements onto the EPI images in each functional run. Data show that average translation (±standard deviation) in our 12 subjects in the x, y, and z directions were, respectively, 0.2843 ± 0.1210 mm (with a minimum value = −0.1448 ± 0.1035 and a maximum value = 0.1395 ± 0.1030), 0.3479 mm ± 0.1459 mm (with a minimum value = −0.2442 ± 0.1309 and a maximum value = 0.1037 ± 0.1242), and 0.9852 ± 0.5381 mm (with a minimum value = −0.3928 ± 0.3386 and a maximum value = 0.5924 ± 0.4633). The average pitch, roll, and yaw rotation (±standard deviation) were, respectively, 0.0118 ± 0.0099° (with a minimum value = −0.0058 ± 0.0049 and a maximum value = 0.0060 ± 0.0099), 0.0073 ± 0.0032° (with a minimum value = −0.0045 ± 0.0038 and a maximum value = 0.0028 ± 0.0021), and 0.0062 ± 0.0037° (with a minimum value = −0.0037 ± 0.0033 and a maximum value = 0.0026 ± 0.0024). These values are within the acceptable range and, therefore, strongly suggest that the limb movements did not impact onto the EPI images. Therefore, the location of the cingulate motor areas described below cannot be displaced by limb movements.

Anatomo-Functional Organization of the Motor Areas in the Medial Frontal Lobe

We first performed a multisubject analysis. This analysis bilaterally revealed the existence of 2 saccadic eye movement regions, 2 tongue movement regions, 3 foot movement regions, and 4 hand movement regions within the cingulate cortex. In addition, increased activity was bilaterally observed in the supplementary motor cortex for all types of movement (Table 2). It should be emphasized that the above group results establish, statistically, the existence of multiple motor areas in the cingulate region, but do not provide any information about the relationship between these motor regions and specific morphological features of the cingulate cortex. As pointed out above, the cingulate region of the human brain is complex, including segments and considerable intersubject variability. Only a subject by subject analysis allows examination of the details of the anatomo-functional relationships. We therefore proceeded to examine the relationships between sulcal and gyral variability in the ROI and the activation foci in both hemispheres on an individual subject by subject basis. We therefore assessed in total 24 hemispheres.

Table 2

Coordinates of motor activity foci observed in the group analysis: The difference of BOLD signal between saccadic eye movement and ocular fixation trials, tongue movement and ocular fixation trials, hand movement and ocular fixation trials, and foot movement and ocular fixation trials

 Left hemisphere
 
Right hemisphere
 
 x y z t x y z t 
Middle CEF −6 66 6.19 10 56 6.61 
Anterior CEF −12 16 52 4.85 14 18 38 3.10 
SEF −4 −6 66 6.11 −4 66 6.68 
Middle cingulate tongue movement region −6 48 5.95 10 44 3.39 
Anterior cingulate tongue movement region −10 10 40 5.95 16 44 5.82 
SMA tongue region −6 68 9.18 −6 68 9.18 
Posterior cingulate foot movement region −16 −30 42 5.48 14 −30 46 3.71 
Middle cingulate foot movement region −6 54 6.58 14 −2 50 10.99 
Anterior cingulate foot movement region −2 18 30 3.27 10 42 5.89 
SMA foot region −4 −18 72 10.90 −8 68 12.31 
Posterior cingulate hand movement region 2 −4 −26 46 7.68 18 −34 46 6.44 
Posterior cingulate hand movement region 1 −4 −8 52 5.52 12 −20 46 7.92 
Middle cingulate hand movement region −4 40 8.50 42 10.20 
Anterior cingulate hand movement region −2 32 24 5.97 20 38 3.48 
SMA hand movement region −6 −10 58 7.98 12 −10 66 7.72 
 Left hemisphere
 
Right hemisphere
 
 x y z t x y z t 
Middle CEF −6 66 6.19 10 56 6.61 
Anterior CEF −12 16 52 4.85 14 18 38 3.10 
SEF −4 −6 66 6.11 −4 66 6.68 
Middle cingulate tongue movement region −6 48 5.95 10 44 3.39 
Anterior cingulate tongue movement region −10 10 40 5.95 16 44 5.82 
SMA tongue region −6 68 9.18 −6 68 9.18 
Posterior cingulate foot movement region −16 −30 42 5.48 14 −30 46 3.71 
Middle cingulate foot movement region −6 54 6.58 14 −2 50 10.99 
Anterior cingulate foot movement region −2 18 30 3.27 10 42 5.89 
SMA foot region −4 −18 72 10.90 −8 68 12.31 
Posterior cingulate hand movement region 2 −4 −26 46 7.68 18 −34 46 6.44 
Posterior cingulate hand movement region 1 −4 −8 52 5.52 12 −20 46 7.92 
Middle cingulate hand movement region −4 40 8.50 42 10.20 
Anterior cingulate hand movement region −2 32 24 5.97 20 38 3.48 
SMA hand movement region −6 −10 58 7.98 12 −10 66 7.72 

Note: The stereotaxic coordinates are expressed in mm within the MNI standard stereotaxic proportional space.

The single-subject analysis demonstrated, in both hemispheres, the existence of 3 cingulate motor clusters and 1 supplementary motor cluster. Specifically, an anterior cluster of cingulate motor activation foci (i.e. hand, foot, tongue, and saccadic eye movements) was located at the intersection of the cgs/pcgs and vpcgs (Fig. 1). A middle cluster of cingulate motor activation foci (i.e. hand, foot, tongue, and saccadic eye movements) was located at the intersection of the cgs/pcgs and prpacs (Fig. 1). Finally, a posterior cluster of cingulate motor activation foci was located in the cgs, extending from the level of cs to pacs. In this posterior cluster, 2 motor hand foci and 1 foot focus were represented (Fig. 1). Importantly, the location of both the saccadic eye and tongue movement cingulate regions depended on whether a pcgs was present (Fig. 1A vs. B, Fig. 2 vs. Fig. 3, Fig. 4, Tables 3–6). Specifically, these 2 regions were located within the pcgs when present, and in the cgs when no pcgs was observed. By contrast, the hand and foot movements regions of the 3 motor clusters were systematically located in the cgs. As shown in Figs 2 and 3 which show the increased activity of each type of movement in each individual subject in both hemispheres, the different cingulate motor regions can be clearly dissociated from each other. Note that these motor regions can be consistently separated within subjects (Tables 3–6). Importantly, all these regions can be dissociated from activations on the dorsalmost part of the medial hemispheric surface, that is, the supplementary motor region, all located in front of the medial precentral sulcus (Figs 1–4 and Tables 7–10 for a complete description of all the increased activation foci in the supplementary motor region).

Table 3

Cingulate motor regions involved in the performance of saccadic eye movements: Difference of the BOLD signal between saccadic eye movement and ocular fixation trials

 MNI coordinates
 
t-statistic Sulcal location Presence of pcgs at the coordinates of the increased activity 
x y z 
Middle CEF 
 Right hemisphere 
  S1 – – – – –  
  S2 14 22 40 2.73 Cgs No 
  S3 54 4.39 Cgs  
  S4 10 54 5.78 Cgs  
  S5 10 58 3.70 Cgs  
  S6 12 54 4.04 Cgs  
  S7 – – – – – – 
  S8 12 54 2.69 Cgs  
  S9 10 44 7.32 Cgs  
  S10 – – – – –  
  S11 50 5.73 Cgs  
  S12 12 54 3.66 Cgs  
 Left hemisphere 
  S1 −6 56 2.33 Pcgs Yes 
  S2 −6 52 7.00 Cgs No 
  S3 – – – – –  
  S4 −8 50 4.37 Cgs  
  S5 −4 12 50 4.02 Cgs  
  S6 −6 54 4.64 Pcgs Yes 
  S7 – – – – –  
  S8 −4 58 6.57 Pcgs Yes 
  S9 −6 −6 46 3.56 Cgs  
  S10 −8 58 5.22 Pcgs Yes 
  S11 −6 10 56 7.97 Pcgs Yes 
  S12 −4 12 50 7.43 Cgs  
 Average x Average y Average z    
Average (±standard deviation) in both hemispheres    
 Cgs 7.4 ± 3.1 8.5 ± 5.3 50.8 ± 4.9    
 Pcgs 4.7 ± 1.5 5.3 ± 4.5 55.3 ± 3.0    
Anterior CEF 
 Right hemisphere 
  S1 – – – – –  
  S2 38 44 2.13 Pcgs Yes 
  S3 10 34 28 4.46 Cgs  
  S4 22 32 3.64 Cgs  
  S5 10 32 42 3.59 Cgs  
  S6 10 44 24 2.62 Cgs  
  S7 – – – – – – 
  S8 10 36 32 4.96 Cgs  
  S9 12 42 4.58 Cgs  
  S10 16 44 2.14 Cgs  
  S11 20 48 4.93 Cgs  
  S12 32 32 4.34 Cgs  
 Left hemisphere 
  S1 – – – – – – 
  S2 −6 26 44 3.78 Pcgs Yes 
  S3 −8 32 32 1.71 (ns) Cgs  
  S4 −8 20 36 3.79 Cgs  
  S5 – – – –   
  S6 −10 18 34 2.39 Cgs Yes 
  S7 – – – –   
  S8 28 42 5.35 Pcgs Yes 
  S9 −10 16 38 4.59 Cgs  
  S10 – – – – – – 
  S11 −8 30 40 4.27 Pcgs Yes 
  S12 −8 28 30 5.32 Cgs  
 Average x Average y Average z    
Average in both hemispheres    
 Cgs 8.3 ± 1.6 26.5 ± 9.5 35.4 ± 7.0    
 Pcgs 6.4 ± 3.8 28.0 ± 7.2 40.8 ± 4.1    
 MNI coordinates
 
t-statistic Sulcal location Presence of pcgs at the coordinates of the increased activity 
x y z 
Middle CEF 
 Right hemisphere 
  S1 – – – – –  
  S2 14 22 40 2.73 Cgs No 
  S3 54 4.39 Cgs  
  S4 10 54 5.78 Cgs  
  S5 10 58 3.70 Cgs  
  S6 12 54 4.04 Cgs  
  S7 – – – – – – 
  S8 12 54 2.69 Cgs  
  S9 10 44 7.32 Cgs  
  S10 – – – – –  
  S11 50 5.73 Cgs  
  S12 12 54 3.66 Cgs  
 Left hemisphere 
  S1 −6 56 2.33 Pcgs Yes 
  S2 −6 52 7.00 Cgs No 
  S3 – – – – –  
  S4 −8 50 4.37 Cgs  
  S5 −4 12 50 4.02 Cgs  
  S6 −6 54 4.64 Pcgs Yes 
  S7 – – – – –  
  S8 −4 58 6.57 Pcgs Yes 
  S9 −6 −6 46 3.56 Cgs  
  S10 −8 58 5.22 Pcgs Yes 
  S11 −6 10 56 7.97 Pcgs Yes 
  S12 −4 12 50 7.43 Cgs  
 Average x Average y Average z    
Average (±standard deviation) in both hemispheres    
 Cgs 7.4 ± 3.1 8.5 ± 5.3 50.8 ± 4.9    
 Pcgs 4.7 ± 1.5 5.3 ± 4.5 55.3 ± 3.0    
Anterior CEF 
 Right hemisphere 
  S1 – – – – –  
  S2 38 44 2.13 Pcgs Yes 
  S3 10 34 28 4.46 Cgs  
  S4 22 32 3.64 Cgs  
  S5 10 32 42 3.59 Cgs  
  S6 10 44 24 2.62 Cgs  
  S7 – – – – – – 
  S8 10 36 32 4.96 Cgs  
  S9 12 42 4.58 Cgs  
  S10 16 44 2.14 Cgs  
  S11 20 48 4.93 Cgs  
  S12 32 32 4.34 Cgs  
 Left hemisphere 
  S1 – – – – – – 
  S2 −6 26 44 3.78 Pcgs Yes 
  S3 −8 32 32 1.71 (ns) Cgs  
  S4 −8 20 36 3.79 Cgs  
  S5 – – – –   
  S6 −10 18 34 2.39 Cgs Yes 
  S7 – – – –   
  S8 28 42 5.35 Pcgs Yes 
  S9 −10 16 38 4.59 Cgs  
  S10 – – – – – – 
  S11 −8 30 40 4.27 Pcgs Yes 
  S12 −8 28 30 5.32 Cgs  
 Average x Average y Average z    
Average in both hemispheres    
 Cgs 8.3 ± 1.6 26.5 ± 9.5 35.4 ± 7.0    
 Pcgs 6.4 ± 3.8 28.0 ± 7.2 40.8 ± 4.1    

Note: The light gray lines indicate the subjects exhibiting a pcgs. The presence of a pcgs at the y level of the increased activity is noted (see Table 1 for the description of the morphology of the cgs and pcgs in individual brains). Note that, in the left hemisphere of S6, the anterior CEF is located in the cgs despite the presence of a pcgs. The increased activity observed in the anterior CEF in the left hemisphere of S3 is not statistically significant. However, it is unlikely to be a false-positive peak given that the corresponding increased activity in the opposite hemisphere is statistically significant.

Table 4

Cingulate motor regions involved in the performance of tongue movements: Difference of the BOLD signal between tongue movement and ocular fixation trials

 MNI coordinates
 
t-statistic Sulcal location Presence of pcgs at the coordinates of the increased activity 
x y z 
Middle tongue movement region 
 Right hemisphere 
  S1 38 4.67 Cgs  
  S2 12 18 42 5.30 Cgs No 
  S3 58 3.99 Cgs  
  S4 12 14 38 3.70 Cgs  
  S5 60 3.12 Cgs  
  S6 10 38 2.38 Cgs  
  S7 14 −2 46 3.12 Cgs No 
  S8 46 2.19 Cgs  
  S9 46 6.23 Cgs  
  S10 10 44 3.57 Cgs  
  S11 – – – – –  
  S12 12 36 3.95 Cgs  
 Left hemisphere 
  S1 −6 50 3.65 Pcgs Yes 
  S2 −6 50 6.83 Cgs No 
  S3 −6 12 36 3.68 Cgs  
  S4 −2 54 4.11 Cgs  
  S5 – – – – –  
  S6 −4 56 4.24 Pcgs Yes 
  S7 44 3.39 Cgs  
  S8 −6 56 4.16 Pcgs Yes 
  S9 −12 46 2.34 Cgs  
  S10 −2 −4 56 7.61 Pcgs Yes 
  S11 −6 10 56 7.97 Pcgs Yes 
  S12 −4 24 34 3.21 Cgs  
 Average x Average y Average z    
Average (±standard deviation) in both hemispheres    
 Cgs 4.9 ± 4.0 6.1 ± 8.3 44.1 ± 8.3    
 Pcgs 7.0 ± 4.0 3.0 ± 7.3 51.5 ± 5.4    
Anterior tongue movement region 
 Right hemisphere 
  S1 10 32 26 3.73 Cgs  
  S2 10 36 40 3.68 Pcgs Yes 
  S3 10 32 28 3.55 Cgs  
  S4 10 32 26 3.38 Cgs  
  S5 12 26 40 2.55 Cgs  
  S6 20 32 2.59 Cgs  
  S7 – – – – – – 
  S8 12 28 40 3.01 Cgs  
  S9 14 42 3.12 Cgs  
  S10 22 44 3.74 Cgs  
  S11 18 46 3.27 Cgs  
  S12 22 32 3.86 Cgs  
 Left hemisphere 
  S1 −6 26 36 3.89 Pcgs Yes 
  S2 −8 26 48 3.05 Pcgs Yes 
  S3 – – – – –  
  S4 −8 16 40 2.95 Cgs  
  S5 −12 18 36 1.99 (ns) Cgs  
  S6 −10 14 36 3.11 Cgs – 
  S7 −6 26 24 2.58 Cgs  
  S8 −10 20 44 3.51 Pcgs Yes 
  S9 −4 14 40 4.80 Cgs  
  S10 −4 12 46 4.41 Pcgs – 
  S11 −8 30 38 4.25 Pcgs Yes 
  S12 −2 32 20 3.30 Cgs  
 Average x Average y Average z    
Average in both hemispheres    
 Cgs 7.3 ± 3.6 23.5 ± 6.7 34.4 ± 8.1    
 Pcgs 8.0 ± 2.3 23.4 ± 8.6 41.1 ± 4.9    
 MNI coordinates
 
t-statistic Sulcal location Presence of pcgs at the coordinates of the increased activity 
x y z 
Middle tongue movement region 
 Right hemisphere 
  S1 38 4.67 Cgs  
  S2 12 18 42 5.30 Cgs No 
  S3 58 3.99 Cgs  
  S4 12 14 38 3.70 Cgs  
  S5 60 3.12 Cgs  
  S6 10 38 2.38 Cgs  
  S7 14 −2 46 3.12 Cgs No 
  S8 46 2.19 Cgs  
  S9 46 6.23 Cgs  
  S10 10 44 3.57 Cgs  
  S11 – – – – –  
  S12 12 36 3.95 Cgs  
 Left hemisphere 
  S1 −6 50 3.65 Pcgs Yes 
  S2 −6 50 6.83 Cgs No 
  S3 −6 12 36 3.68 Cgs  
  S4 −2 54 4.11 Cgs  
  S5 – – – – –  
  S6 −4 56 4.24 Pcgs Yes 
  S7 44 3.39 Cgs  
  S8 −6 56 4.16 Pcgs Yes 
  S9 −12 46 2.34 Cgs  
  S10 −2 −4 56 7.61 Pcgs Yes 
  S11 −6 10 56 7.97 Pcgs Yes 
  S12 −4 24 34 3.21 Cgs  
 Average x Average y Average z    
Average (±standard deviation) in both hemispheres    
 Cgs 4.9 ± 4.0 6.1 ± 8.3 44.1 ± 8.3    
 Pcgs 7.0 ± 4.0 3.0 ± 7.3 51.5 ± 5.4    
Anterior tongue movement region 
 Right hemisphere 
  S1 10 32 26 3.73 Cgs  
  S2 10 36 40 3.68 Pcgs Yes 
  S3 10 32 28 3.55 Cgs  
  S4 10 32 26 3.38 Cgs  
  S5 12 26 40 2.55 Cgs  
  S6 20 32 2.59 Cgs  
  S7 – – – – – – 
  S8 12 28 40 3.01 Cgs  
  S9 14 42 3.12 Cgs  
  S10 22 44 3.74 Cgs  
  S11 18 46 3.27 Cgs  
  S12 22 32 3.86 Cgs  
 Left hemisphere 
  S1 −6 26 36 3.89 Pcgs Yes 
  S2 −8 26 48 3.05 Pcgs Yes 
  S3 – – – – –  
  S4 −8 16 40 2.95 Cgs  
  S5 −12 18 36 1.99 (ns) Cgs  
  S6 −10 14 36 3.11 Cgs – 
  S7 −6 26 24 2.58 Cgs  
  S8 −10 20 44 3.51 Pcgs Yes 
  S9 −4 14 40 4.80 Cgs  
  S10 −4 12 46 4.41 Pcgs – 
  S11 −8 30 38 4.25 Pcgs Yes 
  S12 −2 32 20 3.30 Cgs  
 Average x Average y Average z    
Average in both hemispheres    
 Cgs 7.3 ± 3.6 23.5 ± 6.7 34.4 ± 8.1    
 Pcgs 8.0 ± 2.3 23.4 ± 8.6 41.1 ± 4.9    

Note: The light gray lines indicate the subjects exhibiting a pcgs. The presence of a pcgs at the y level of the increased activity is noted (see Table 1 for the description of the morphology of the cgs and pcgs in individual brains). Note that, in the left hemisphere of S6, the anterior CEF is located in the cgs despite the presence of a pcgs. The increased activity observed in the anterior tongue movement region in the left hemisphere of S5 is no statistically significant. However, it is unlikely a false positive given that the corresponding increased activity in the opposite hemisphere is statistically significant.

Table 5

Cingulate motor regions involved in the performance of foot movements: Difference of the BOLD signal between foot movement and ocular fixation trials

 MNI coordinates
 
t-statistic Sulcal location Presence of pcgs at the coordinates of the increased activity 
x y z 
Posterior foot movement region 
 Right hemisphere 
  S1 −8 50 5.64 Cgs  
  S2 −12 50 4.59 Cgs No 
  S3 10 −24 50 2.93 Cgs  
  S4 −10 52 8.15 Cgs  
  S5 10 −22 44 3.66 Cgs  
  S6 16 −32 50 3.08  Cgs  
  S7 −12 48 4.44 Cgs No 
  S8 16 −36 54 5.27 Cgs  
  S9 10 −32 44 4.67 Cgs  
  S10 12 −6 50 4.65 Cgs  
  S11 −4 54 7.82 Cgs  
  S12 – – – – –  
 Left hemisphere 
  S1 −12 −36 50 4.62 Cgs No 
  S2 −10 −20 48 2.08 Cgs No 
  S3 −10 −6 42 3.27 Cgs  
  S4 −4 −38 58 9.12 Cgs  
  S5 −14 −28 40 2.73 Cgs  
  S6 −4 −8 50 4.12 Cgs No 
  S7 −14 −38 48 4.11 Cgs  
  S8 – – – – – – 
  S9 −10 −34 42 5.34 Cgs  
  S10 −6 −32 48 3.10 Cgs No 
  S11 −2 −32 46 3.65 Cgs No 
  S12 – – – – –  
 Average x Average y Average z    
Average (±standard deviation) in both hemispheres    
 Cgs 10.1 ± 4.0 −22.7 ± 13.2 48.4 ± 5.3    
 Pcgs 6.6 ± 3.6 −21.7 ± 11.5 48.6 ± 1.5    
Middle foot movement region 
 Right hemisphere 
  S1 46 4.30 Cgs  
  S2 −2 52 7.40 Cgs No 
  S3 48 5.10 Cgs  
  S4 – – – – –  
  S5 10 −4 54 7.30 Cgs  
  S6 16 46 4.40 Cgs  
  S7 12 52 2.60 Cgs No 
  S8 12 −6 48 4.60 Cgs  
  S9 −8 48 6.40 Cgs  
  S10 – – – – –  
  S11 – – – – –  
  S12 42 3.80 Cgs  
 Left hemisphere 
  S1 −4 −4 44 5.50 Cgs No 
  S2 −2 −2 50 6.50 Cgs Yes 
  S3 −12 38 3.20 Cgs  
  S4 −8 −6 48 7.60 Cgs  
  S5 −4 −4 50 7.20 Cgs  
  S6 −6 46 3.50 Cgs Yes 
  S7 −4 −6 42 4.90 Cgs  
  S8 −2 −6 50 6.70 Cgs No 
  S9 −8 −6 44 9.00 Cgs  
  S10 −2 −6 48 3.60 Cgs No 
  S11 −6 44 6.00 Cgs Yes 
  S12 −10 38 5.90 Cgs  
 Average x Average y Average z    
Average (±standard deviation) in both hemispheres    
 Cgs 7.8 ± 4.0 −1.7 ± 4.8 45.5 ± 4.6    
 Pcgs 4.8 ± 3.4 −2.0 ± 3.2 48.3 ± 3.3    
Anterior foot movement region 
 Right hemisphere 
  S1 10 30 30 4.00 Cgs  
  S2 – – – – – – 
  S3 10 32 28 2.30 Cgs  
  S4 14 40 3.60 Cgs  
  S5 32 38 4.70 Cgs  
  S6 12 36 28 2.40 Cgs  
  S7 22 34 2.30 Cgs Yes 
  S8 20 40 4.90 Cgs  
  S9 14 42 3.60 Cgs  
  S10 – – – – –  
  S11 12 18 40 4.40 Cgs  
  S12 – – – – –  
 Left hemisphere 
  S1 −6 20 26 2.60 Cgs Yes 
  S2 −8 38 3.00 Cgs No 
  S3 – – – – –  
  S4 16 34 2.50 Cgs  
  S5 −8 18 40 2.30 Cgs  
  S6 – – – – – – 
  S7 −2 14 38 7.00 Cgs  
  S8 −4 30 28 2.20 Cgs Yes 
  S9 −10 12 42 2.70 Cgs  
  S10 – – – – – – 
  S11 −12 20 32 2.20 Cgs Yes 
  S12 −10 22 32 2.20 Cgs  
 Average x Average y Average z    
Average in both hemispheres    
 Cgs 7.2 ± 4.0 21.4 ± 8.3 36.3 ± 5.2    
 Pcgs 6.8 ± 3.3 20.0 ± 7.9 31.6 ± 4.8    
 MNI coordinates
 
t-statistic Sulcal location Presence of pcgs at the coordinates of the increased activity 
x y z 
Posterior foot movement region 
 Right hemisphere 
  S1 −8 50 5.64 Cgs  
  S2 −12 50 4.59 Cgs No 
  S3 10 −24 50 2.93 Cgs  
  S4 −10 52 8.15 Cgs  
  S5 10 −22 44 3.66 Cgs  
  S6 16 −32 50 3.08  Cgs  
  S7 −12 48 4.44 Cgs No 
  S8 16 −36 54 5.27 Cgs  
  S9 10 −32 44 4.67 Cgs  
  S10 12 −6 50 4.65 Cgs  
  S11 −4 54 7.82 Cgs  
  S12 – – – – –  
 Left hemisphere 
  S1 −12 −36 50 4.62 Cgs No 
  S2 −10 −20 48 2.08 Cgs No 
  S3 −10 −6 42 3.27 Cgs  
  S4 −4 −38 58 9.12 Cgs  
  S5 −14 −28 40 2.73 Cgs  
  S6 −4 −8 50 4.12 Cgs No 
  S7 −14 −38 48 4.11 Cgs  
  S8 – – – – – – 
  S9 −10 −34 42 5.34 Cgs  
  S10 −6 −32 48 3.10 Cgs No 
  S11 −2 −32 46 3.65 Cgs No 
  S12 – – – – –  
 Average x Average y Average z    
Average (±standard deviation) in both hemispheres    
 Cgs 10.1 ± 4.0 −22.7 ± 13.2 48.4 ± 5.3    
 Pcgs 6.6 ± 3.6 −21.7 ± 11.5 48.6 ± 1.5    
Middle foot movement region 
 Right hemisphere 
  S1 46 4.30 Cgs  
  S2 −2 52 7.40 Cgs No 
  S3 48 5.10 Cgs  
  S4 – – – – –  
  S5 10 −4 54 7.30 Cgs  
  S6 16 46 4.40 Cgs  
  S7 12 52 2.60 Cgs No 
  S8 12 −6 48 4.60 Cgs  
  S9 −8 48 6.40 Cgs  
  S10 – – – – –  
  S11 – – – – –  
  S12 42 3.80 Cgs  
 Left hemisphere 
  S1 −4 −4 44 5.50 Cgs No 
  S2 −2 −2 50 6.50 Cgs Yes 
  S3 −12 38 3.20 Cgs  
  S4 −8 −6 48 7.60 Cgs  
  S5 −4 −4 50 7.20 Cgs  
  S6 −6 46 3.50 Cgs Yes 
  S7 −4 −6 42 4.90 Cgs  
  S8 −2 −6 50 6.70 Cgs No 
  S9 −8 −6 44 9.00 Cgs  
  S10 −2 −6 48 3.60 Cgs No 
  S11 −6 44 6.00 Cgs Yes 
  S12 −10 38 5.90 Cgs  
 Average x Average y Average z    
Average (±standard deviation) in both hemispheres    
 Cgs 7.8 ± 4.0 −1.7 ± 4.8 45.5 ± 4.6    
 Pcgs 4.8 ± 3.4 −2.0 ± 3.2 48.3 ± 3.3    
Anterior foot movement region 
 Right hemisphere 
  S1 10 30 30 4.00 Cgs  
  S2 – – – – – – 
  S3 10 32 28 2.30 Cgs  
  S4 14 40 3.60 Cgs  
  S5 32 38 4.70 Cgs  
  S6 12 36 28 2.40 Cgs  
  S7 22 34 2.30 Cgs Yes 
  S8 20 40 4.90 Cgs  
  S9 14 42 3.60 Cgs  
  S10 – – – – –  
  S11 12 18 40 4.40 Cgs  
  S12 – – – – –  
 Left hemisphere 
  S1 −6 20 26 2.60 Cgs Yes 
  S2 −8 38 3.00 Cgs No 
  S3 – – – – –  
  S4 16 34 2.50 Cgs  
  S5 −8 18 40 2.30 Cgs  
  S6 – – – – – – 
  S7 −2 14 38 7.00 Cgs  
  S8 −4 30 28 2.20 Cgs Yes 
  S9 −10 12 42 2.70 Cgs  
  S10 – – – – – – 
  S11 −12 20 32 2.20 Cgs Yes 
  S12 −10 22 32 2.20 Cgs  
 Average x Average y Average z    
Average in both hemispheres    
 Cgs 7.2 ± 4.0 21.4 ± 8.3 36.3 ± 5.2    
 Pcgs 6.8 ± 3.3 20.0 ± 7.9 31.6 ± 4.8    

Note: The light gray lines indicate the subjects exhibiting a pcgs. The presence of a pcgs at the y level of the increased activity is noted (see Table 1 for the description of the morphology of the cgs and pcgs in individual brains).

Table 6

Cingulate motor regions involved in the performance of hand movements: Difference of the BOLD signal between hand movement and ocular fixation trials

 MNI coordinates
 
t-statistic Sulcal location Presence of pcgs at the coordinates of the increased activity 
x y z 
Posterior hand movement region 2 
 Right hemisphere 
  S1 −20 46 3.34 Cgs  
  S2 −28 46 5.01 Cgs No 
  S3 −24 52 5.20 Cgs  
  S4 −22 48 5.07 Cgs  
  S5 −30 52 6.40 Cgs  
  S6 10 −32 52 2.94 Cgs  
  S7 – – – – – – 
  S8 10 −34 58 5.41 Cgs  
  S9 10 −32 44 4.67 Cgs  
  S10 – – – – –  
  S11 10 −26 48 4.43 Cgs  
  S12 – – – – –  
 Left hemisphere 
  S1 −16 −36 42 2.39 Cgs No 
  S2 −8 −36 52 4.43 Cgs No 
  S3 −28 46 5.44 Cgs  
  S4 −2 −40 56 5.37 Cgs  
  S5 −14 −30 38 3.74 Cgs  
  S6 −6 −24 50 4.07 Cgs No 
  S7 −14 −38 48 4.11 Cgs  
  S8 −16 −38 42 2.23 Cgs No 
  S9 −4 −32 46 7.93 Cgs  
  S10 −4 −32 48 5.68 Cgs No 
  S11 −8 −40 50 5.04 Cgs No 
  S12 −6 −24 42 2.09 Cgs  
 Average x Average y Average z    
Average (±standard deviation) in both hemispheres    
 Cgs 7.4 ± 4.2 −29.4 ± 5.8 48.3 ± 5.4    
 Pcgs 8.9 ± 4.4 −33.4 ± 11.0 47.1 ± 7.1    
Posterior hand movement region 1 
 Right hemisphere 
  S1 – – – – – – 
  S2 −12 50 9.01 Cgs No 
  S3 −10 54 6.36 Cgs  
  S4 −8 42 2.47 Cgs  
  S5 −18 50 7.16 Cgs  
  S6 −20 50 5.18 Cgs  
  S7 – – – – – – 
  S8 −20 50 13.30 Cgs  
  S9 −8 48 6.39 Cgs  
  S10 – – – – –  
  S11 −22 50 5.00 Cgs  
  S12 – – – – –  
 Left hemisphere 
  S1 – – – – – – 
  S2 −10 −20 48 7.78 Cgs No 
  S3 −2 −6 42 4.10 Cgs  
  S4 −8 −26 48 7.50 Cgs  
  S5 −14 −18 38 2.17 Cgs  
  S6 −4 −14 54 6.93 Cgs No 
  S7 −6 −10 48 5.80 Cgs  
  S8 −6 −12 46 10.35 Cgs No 
  S9 −4 −16 54 11.60 Cgs  
  S10 −2 −10 54 5.58 Cgs No 
  S11 −12 −20 38 2.26 Cgs No 
  S12 −10 −6 46 3.19 Cgs  
 Average x Average y Average z    
Average (±standard deviation) in both hemispheres    
 Cgs 6.5 ± 3.3 −14.5 ± 6.7 47.7 ± 4.7    
 Pcgs 6.0 ± 3.6 −13.0 ± 3.7 49.3 ± 6.4    
Middle hand movement region 
 Right hemisphere 
  S1 10 44 2.32 Cgs  
  S2 10 14 40 6.10 Cgs No 
  S3 – – – – –  
  S4 14 38 2.15 Cgs  
  S5 58 8.10 Cgs  
  S6 40 3.29 Cgs  
  S7 −6 44 3.51 Cgs No 
  S8 −10 48 10.96 Cgs  
  S9 −16 48 6.93 Cgs  
  S10 10 44 2.99 Cgs  
  S11 46 5.30 Cgs  
  S12 10 −2 44 6.95 Cgs  
 Left hemisphere 
  S1 – – – – – – 
  S2 −6 −6 52 9.67 Cgs No 
  S3 40 4.31 Cgs  
  S4 −2 46 7.68 Cgs  
  S5 −4 48 7.97 Cgs  
  S6 −6 44 6.02 Cgs Yes 
  S7 44 4.97 Cgs  
  S8 – – – – – – 
  S9 42 8.33 Cgs  
  S10 10 48 4.43 Cgs Yes 
  S11 −8 40 4.06 Cgs Yes 
  S12 – – – – –  
 Average x Average y Average z    
Average in both hemispheres    
 Cgs 5.0 ± 3.8 1.4 ± 7.5 45.0 ± 4.9    
 Pcgs 5.3 ± 3.7 2.7 ± 8.2 44.7 ± 4.7    
Anterior hand movement region 
 Right hemisphere 
  S1 38 30 2.75 Cgs  
  S2 28 26 4.89 Cgs No 
  S3 10 40 3.92 Cgs  
  S4 – – – – –  
  S5 28 40 5.57 Cgs  
  S6 20 34 3.18 Cgs  
  S7 16 38 3.75 Cgs Yes 
  S8 18 42 5.24 Cgs  
  S9 14 42 3.57 Cgs  
  S10 – – – – –  
  S11 26 40 3.74 Cgs  
  S12 – – – – –  
 Left hemisphere 
  S1 −8 18 28 2.39 Cgs Yes 
  S2 −10 12 36 3.83 Cgs No 
  S3 22 34 3.71 Cgs  
  S4 −2 16 34 4.92 Cgs  
  S5 −6 16 38 4.22 Cgs  
  S6 −6 20 34 3.43 Cgs Yes 
  S7 −2 14 36 4.57 Cgs  
  S8 −10 14 36 3.37 Cgs Yes 
  S9 −2 14 40 4.40 Cgs  
  S10 −8 26 34 2.86 Cgs Yes 
  S11 −8 26 34 2.86 Cgs Yes 
  S12 −8 18 28 2.39 Cgs  
 Average x Average y Average z    
Average in both hemispheres    
 Cgs 4.8 ± 3.0 19.2 ± 8.6 37.5 ± 3.8    
 Pcgs 7.3 ± 2.6 20.0 ± 6.0 33.3 ± 4.1    
 MNI coordinates
 
t-statistic Sulcal location Presence of pcgs at the coordinates of the increased activity 
x y z 
Posterior hand movement region 2 
 Right hemisphere 
  S1 −20 46 3.34 Cgs  
  S2 −28 46 5.01 Cgs No 
  S3 −24 52 5.20 Cgs  
  S4 −22 48 5.07 Cgs  
  S5 −30 52 6.40 Cgs  
  S6 10 −32 52 2.94 Cgs  
  S7 – – – – – – 
  S8 10 −34 58 5.41 Cgs  
  S9 10 −32 44 4.67 Cgs  
  S10 – – – – –  
  S11 10 −26 48 4.43 Cgs  
  S12 – – – – –  
 Left hemisphere 
  S1 −16 −36 42 2.39 Cgs No 
  S2 −8 −36 52 4.43 Cgs No 
  S3 −28 46 5.44 Cgs  
  S4 −2 −40 56 5.37 Cgs  
  S5 −14 −30 38 3.74 Cgs  
  S6 −6 −24 50 4.07 Cgs No 
  S7 −14 −38 48 4.11 Cgs  
  S8 −16 −38 42 2.23 Cgs No 
  S9 −4 −32 46 7.93 Cgs  
  S10 −4 −32 48 5.68 Cgs No 
  S11 −8 −40 50 5.04 Cgs No 
  S12 −6 −24 42 2.09 Cgs  
 Average x Average y Average z    
Average (±standard deviation) in both hemispheres    
 Cgs 7.4 ± 4.2 −29.4 ± 5.8 48.3 ± 5.4    
 Pcgs 8.9 ± 4.4 −33.4 ± 11.0 47.1 ± 7.1    
Posterior hand movement region 1 
 Right hemisphere 
  S1 – – – – – – 
  S2 −12 50 9.01 Cgs No 
  S3 −10 54 6.36 Cgs  
  S4 −8 42 2.47 Cgs  
  S5 −18 50 7.16 Cgs  
  S6 −20 50 5.18 Cgs  
  S7 – – – – – – 
  S8 −20 50 13.30 Cgs  
  S9 −8 48 6.39 Cgs  
  S10 – – – – –  
  S11 −22 50 5.00 Cgs  
  S12 – – – – –  
 Left hemisphere 
  S1 – – – – – – 
  S2 −10 −20 48 7.78 Cgs No 
  S3 −2 −6 42 4.10 Cgs  
  S4 −8 −26 48 7.50 Cgs  
  S5 −14 −18 38 2.17 Cgs  
  S6 −4 −14 54 6.93 Cgs No 
  S7 −6 −10 48 5.80 Cgs  
  S8 −6 −12 46 10.35 Cgs No 
  S9 −4 −16 54 11.60 Cgs  
  S10 −2 −10 54 5.58 Cgs No 
  S11 −12 −20 38 2.26 Cgs No 
  S12 −10 −6 46 3.19 Cgs  
 Average x Average y Average z    
Average (±standard deviation) in both hemispheres    
 Cgs 6.5 ± 3.3 −14.5 ± 6.7 47.7 ± 4.7    
 Pcgs 6.0 ± 3.6 −13.0 ± 3.7 49.3 ± 6.4    
Middle hand movement region 
 Right hemisphere 
  S1 10 44 2.32 Cgs  
  S2 10 14 40 6.10 Cgs No 
  S3 – – – – –  
  S4 14 38 2.15 Cgs  
  S5 58 8.10 Cgs  
  S6 40 3.29 Cgs  
  S7 −6 44 3.51 Cgs No 
  S8 −10 48 10.96 Cgs  
  S9 −16 48 6.93 Cgs  
  S10 10 44 2.99 Cgs  
  S11 46 5.30 Cgs  
  S12 10 −2 44 6.95 Cgs  
 Left hemisphere 
  S1 – – – – – – 
  S2 −6 −6 52 9.67 Cgs No 
  S3 40 4.31 Cgs  
  S4 −2 46 7.68 Cgs  
  S5 −4 48 7.97 Cgs  
  S6 −6 44 6.02 Cgs Yes 
  S7 44 4.97 Cgs  
  S8 – – – – – – 
  S9 42 8.33 Cgs  
  S10 10 48 4.43 Cgs Yes 
  S11 −8 40 4.06 Cgs Yes 
  S12 – – – – –  
 Average x Average y Average z    
Average in both hemispheres    
 Cgs 5.0 ± 3.8 1.4 ± 7.5 45.0 ± 4.9    
 Pcgs 5.3 ± 3.7 2.7 ± 8.2 44.7 ± 4.7    
Anterior hand movement region 
 Right hemisphere 
  S1 38 30 2.75 Cgs  
  S2 28 26 4.89 Cgs No 
  S3 10 40 3.92 Cgs  
  S4 – – – – –  
  S5 28 40 5.57 Cgs  
  S6 20 34 3.18 Cgs  
  S7 16 38 3.75 Cgs Yes 
  S8 18 42 5.24 Cgs  
  S9 14 42 3.57 Cgs  
  S10 – – – – –  
  S11 26 40 3.74 Cgs  
  S12 – – – – –  
 Left hemisphere 
  S1 −8 18 28 2.39 Cgs Yes 
  S2 −10 12 36 3.83 Cgs No 
  S3 22 34 3.71 Cgs  
  S4 −2 16 34 4.92 Cgs  
  S5 −6 16 38 4.22 Cgs  
  S6 −6 20 34 3.43 Cgs Yes 
  S7 −2 14 36 4.57 Cgs  
  S8 −10 14 36 3.37 Cgs Yes 
  S9 −2 14 40 4.40 Cgs  
  S10 −8 26 34 2.86 Cgs Yes 
  S11 −8 26 34 2.86 Cgs Yes 
  S12 −8 18 28 2.39 Cgs  
 Average x Average y Average z    
Average in both hemispheres    
 Cgs 4.8 ± 3.0 19.2 ± 8.6 37.5 ± 3.8    
 Pcgs 7.3 ± 2.6 20.0 ± 6.0 33.3 ± 4.1    

Note: The light gray lines indicate the subjects exhibiting a pcgs. The presence of a pcgs at the y level of the increased activity is noted (see Table 1 for the description of the morphology of the cgs and pcgs in individual brains).

Table 7

Supplementary saccadic eye movement region: Difference of the BOLD signal between saccadic eye movement and ocular fixation trials

 MNI coordinates
 
t-statistic 
x y z 
Right hemisphere 
 S1 16 −8 72 2.38 
 S2 64 9.88 
 S3 – – – – 
 S4 70 4.43 
 S5 10 −2 72 4.16 
 S6 72 4.74 
 S7 −4 66 4.11 
 S8 68 6.45 
 S9 −6 72 7.98 
 S10 68 3.30 
 S11 72 5.39 
 S12 −4 72 5.77 
Left hemisphere 
 S1 – – – – 
 S2 −2 64 8.46 
 S3 −4 66 3.38 
 S4 −4 62 6.64 
 S5 −6 −2 64 3.82 
 S6 −6 −4 64 3.20 
 S7 −4 66 3.17 
 S8 −8 72 5.04 
 S9 −4 60 9.69 
 S10 −2 68 6.23 
 S11 −4 −2 62 8.04 
 S12 −4 −2 68 8.48 
 Average x Average y Average z  
Average in both hemispheres  
 Cgs 6.3 ± 3.5 0.1 ± 4.2 68.3 ± 4.0  
 Pcgs 4.6 ± 2.8 −0.6 ± 3.0 65.7 ± 3.4  
 MNI coordinates
 
t-statistic 
x y z 
Right hemisphere 
 S1 16 −8 72 2.38 
 S2 64 9.88 
 S3 – – – – 
 S4 70 4.43 
 S5 10 −2 72 4.16 
 S6 72 4.74 
 S7 −4 66 4.11 
 S8 68 6.45 
 S9 −6 72 7.98 
 S10 68 3.30 
 S11 72 5.39 
 S12 −4 72 5.77 
Left hemisphere 
 S1 – – – – 
 S2 −2 64 8.46 
 S3 −4 66 3.38 
 S4 −4 62 6.64 
 S5 −6 −2 64 3.82 
 S6 −6 −4 64 3.20 
 S7 −4 66 3.17 
 S8 −8 72 5.04 
 S9 −4 60 9.69 
 S10 −2 68 6.23 
 S11 −4 −2 62 8.04 
 S12 −4 −2 68 8.48 
 Average x Average y Average z  
Average in both hemispheres  
 Cgs 6.3 ± 3.5 0.1 ± 4.2 68.3 ± 4.0  
 Pcgs 4.6 ± 2.8 −0.6 ± 3.0 65.7 ± 3.4  

Note: The light gray lines indicate the subjects exhibiting a pcgs.

Table 8

Supplementary tongue movement region: Difference of the BOLD signal between tongue movement and ocular fixation trials

 MNI coordinates
 
t-statistic 
x y z 
Right hemisphere 
 S1 72 4.75 
 S2 −2 64 7.22 
 S3 – – – – 
 S4 58 4.87 
 S5 64 2.18 
 S6 62 5.43 
 S7 10 60 2.44 
 S8 60 4.90 
 S9 −8 72 4.76 
 S10 62 6.70 
 S11 −6 64 4.71 
 S12 −4 68 5.06 
Left hemisphere 
 S1 −2 −8 72 6.32 
 S2 −6 −4 66 3.76 
 S3 −4 66 3.38 
 S4 −2 −8 66 3.09 
 S5 −4 58 3.41 
 S6 −2 −2 62 5.36 
 S7 – – – – 
 S8 −8 72 3.67 
 S9 −2 −2 60 6.75 
 S10 −2 −12 66 6.13 
 S11 −4 −2 60 7.97 
 S12 −2 −4 58 5.71 
 Average x Average y Average z  
Average in both hemispheres  
 Cgs 2.7 ± 1.7 −1.1 ± 4.6 63.6 ± 4.8  
 Pcgs 4.8 ± 3.0 −3.5 ± 4.5 65.3 ± 4.8  
 MNI coordinates
 
t-statistic 
x y z 
Right hemisphere 
 S1 72 4.75 
 S2 −2 64 7.22 
 S3 – – – – 
 S4 58 4.87 
 S5 64 2.18 
 S6 62 5.43 
 S7 10 60 2.44 
 S8 60 4.90 
 S9 −8 72 4.76 
 S10 62 6.70 
 S11 −6 64 4.71 
 S12 −4 68 5.06 
Left hemisphere 
 S1 −2 −8 72 6.32 
 S2 −6 −4 66 3.76 
 S3 −4 66 3.38 
 S4 −2 −8 66 3.09 
 S5 −4 58 3.41 
 S6 −2 −2 62 5.36 
 S7 – – – – 
 S8 −8 72 3.67 
 S9 −2 −2 60 6.75 
 S10 −2 −12 66 6.13 
 S11 −4 −2 60 7.97 
 S12 −2 −4 58 5.71 
 Average x Average y Average z  
Average in both hemispheres  
 Cgs 2.7 ± 1.7 −1.1 ± 4.6 63.6 ± 4.8  
 Pcgs 4.8 ± 3.0 −3.5 ± 4.5 65.3 ± 4.8  

Note: The light gray lines indicate the subjects exhibiting a pcgs.

Table 9

Supplementary foot movement region: Difference of the BOLD signal between foot movement and ocular fixation trials

 MNI coordinates
 
t-statistic 
x y z 
Right hemisphere 
 S1 10 −14 66 6.99 
 S2 66 6.47 
 S3 −10 78 7.06 
 S4 −12 74 12.68 
 S5 −12 76 7.69 
 S6 −2 58 4.21 
 S7 64 2.03 
 S8 68 6.63 
 S9 −12 80 11.38 
 S10 10 −6 70 8.72 
 S11 −14 68 8.47 
 S12 10 −14 66 6.99 
Left hemisphere 
 S1 −6 −14 74 9.43 
 S2 −2 −16 74 11.99 
 S3 −4 −2 58 3.09 
 S4 −14 74 10.28 
 S5 −2 −12 68 9.53 
 S6 −2 −4 60 2.88 
 S7 −8 58 3.39 
 S8 −4 74 6.36 
 S9 −2 −2 58 5.99 
 S10 −4 −16 72 12.03 
 S11 −2 −14 72 8.69 
 S12 −4 −4 74 9.57 
 Average x Average y Average z  
Average in both hemispheres  
 Cgs 5.1 ± 3.1 −7.1 ± 6.7 68.5 ± 7.7  
 Pcgs 3.8 ± 1.7 −6.0 ± 10.3 69.5 ± 5.4  
 MNI coordinates
 
t-statistic 
x y z 
Right hemisphere 
 S1 10 −14 66 6.99 
 S2 66 6.47 
 S3 −10 78 7.06 
 S4 −12 74 12.68 
 S5 −12 76 7.69 
 S6 −2 58 4.21 
 S7 64 2.03 
 S8 68 6.63 
 S9 −12 80 11.38 
 S10 10 −6 70 8.72 
 S11 −14 68 8.47 
 S12 10 −14 66 6.99 
Left hemisphere 
 S1 −6 −14 74 9.43 
 S2 −2 −16 74 11.99 
 S3 −4 −2 58 3.09 
 S4 −14 74 10.28 
 S5 −2 −12 68 9.53 
 S6 −2 −4 60 2.88 
 S7 −8 58 3.39 
 S8 −4 74 6.36 
 S9 −2 −2 58 5.99 
 S10 −4 −16 72 12.03 
 S11 −2 −14 72 8.69 
 S12 −4 −4 74 9.57 
 Average x Average y Average z  
Average in both hemispheres  
 Cgs 5.1 ± 3.1 −7.1 ± 6.7 68.5 ± 7.7  
 Pcgs 3.8 ± 1.7 −6.0 ± 10.3 69.5 ± 5.4  

Note: The light gray lines indicate the subjects exhibiting a pcgs.

Table 10

Supplementary hand movement region: Difference of the BOLD signal between hand movement and ocular fixation trials

 MNI coordinates
 
t-statistic 
x y z 
Right hemisphere 
 S1 −6 62 3.48 
 S2 64 7.82 
 S3 −8 70 3.65 
 S4 −8 60 10.18 
 S5 −10 68 7.22 
 S6 58 7.13 
 S7 −14 62 11.65 
 S8 72 9.40 
 S9 58 6.60 
 S10 – – – – 
 S11 – – – – 
 S12 −4 74 5.62 
Left hemisphere 
 S1 −2 −12 66 3.41 
 S2 −2 −12 72 6.87 
 S3 −2 10 68 3.29 
 S4 −16 60 11.33 
 S5 −4 −10 58 9.32 
 S6 −6 −6 62 6.72 
 S7 – – – – 
 S8 −6 −6 68 8.47 
 S9 −2 −4 60 5.84 
 S10 −2 −8 62 6.92 
 S11 −2 −10 60 7.89 
 S12 −8 −4 66 3.40 
 Average x Average y Average z  
Average in both hemispheres  
 Cgs 4.0 ± 2.6 −4.2 ± 7.0 64.2 ± 5.7  
 Pcgs 3.0 ± 1.9 −8.5 ± 4.5 64.5 ± 4.0  
 MNI coordinates
 
t-statistic 
x y z 
Right hemisphere 
 S1 −6 62 3.48 
 S2 64 7.82 
 S3 −8 70 3.65 
 S4 −8 60 10.18 
 S5 −10 68 7.22 
 S6 58 7.13 
 S7 −14 62 11.65 
 S8 72 9.40 
 S9 58 6.60 
 S10 – – – – 
 S11 – – – – 
 S12 −4 74 5.62 
Left hemisphere 
 S1 −2 −12 66 3.41 
 S2 −2 −12 72 6.87 
 S3 −2 10 68 3.29 
 S4 −16 60 11.33 
 S5 −4 −10 58 9.32 
 S6 −6 −6 62 6.72 
 S7 – – – – 
 S8 −6 −6 68 8.47 
 S9 −2 −4 60 5.84 
 S10 −2 −8 62 6.92 
 S11 −2 −10 60 7.89 
 S12 −8 −4 66 3.40 
 Average x Average y Average z  
Average in both hemispheres  
 Cgs 4.0 ± 2.6 −4.2 ± 7.0 64.2 ± 5.7  
 Pcgs 3.0 ± 1.9 −8.5 ± 4.5 64.5 ± 4.0  

Note: The light gray lines indicate the subjects exhibiting a pcgs.

Figure 1.

Location of the activation foci for eye (red), tongue (yellow), hand (green), and foot (blue) movements in the cingulate motor region (left panels) and the SMA/SEF (right panels) in 2 typical subjects. In A (case 1), the subject (S4) displays only a cgs in the left hemisphere, and in B (case 2), the subject (S2) displays a pcgs in the left hemisphere. Motor regions are projected on sagittal sections, at the mediolateral levels X = −6 and X = −3 (L hemisphere) in A, and X = −6 and X = −2 (L hemisphere) in B. The antero-posterior (y) and dorso-ventral (z) coordinates in the Montreal Neurological Institute (MNI) standard stereotaxic space are indicated in red. The color dots represent the location of the highest t-values observed in the contrasts “saccadic eye movements versus ocular fixation trials” (red), “tongue movements versus ocular fixation trials” (yellow), “hand movements versus ocular fixation trials” (green), and “foot movements versus ocular fixation trials” (blue). The posterior, middle, and anterior clusters are circled in purple, dark pink, and light pink, respectively. The SMA/SEF cluster is coded in blue. For each subject, the 4 raw functional maps are displayed. The color scale represents the range of t-values. Abbreviations: cgs, cingulate sulcus; pcgs, paracingulate sulcus; pacs, paracentral sulcus; prpacs, pre-paracentral sulcus; vpcgs, vertical paracingulate sulcus; cs, central sulcus; meps, medial paracentral sulcus.

Figure 1.

Location of the activation foci for eye (red), tongue (yellow), hand (green), and foot (blue) movements in the cingulate motor region (left panels) and the SMA/SEF (right panels) in 2 typical subjects. In A (case 1), the subject (S4) displays only a cgs in the left hemisphere, and in B (case 2), the subject (S2) displays a pcgs in the left hemisphere. Motor regions are projected on sagittal sections, at the mediolateral levels X = −6 and X = −3 (L hemisphere) in A, and X = −6 and X = −2 (L hemisphere) in B. The antero-posterior (y) and dorso-ventral (z) coordinates in the Montreal Neurological Institute (MNI) standard stereotaxic space are indicated in red. The color dots represent the location of the highest t-values observed in the contrasts “saccadic eye movements versus ocular fixation trials” (red), “tongue movements versus ocular fixation trials” (yellow), “hand movements versus ocular fixation trials” (green), and “foot movements versus ocular fixation trials” (blue). The posterior, middle, and anterior clusters are circled in purple, dark pink, and light pink, respectively. The SMA/SEF cluster is coded in blue. For each subject, the 4 raw functional maps are displayed. The color scale represents the range of t-values. Abbreviations: cgs, cingulate sulcus; pcgs, paracingulate sulcus; pacs, paracentral sulcus; prpacs, pre-paracentral sulcus; vpcgs, vertical paracingulate sulcus; cs, central sulcus; meps, medial paracentral sulcus.

Figure 2.

Dispersion of the eye, tongue, hand, and foot foci of the cingulate and SMA/SEF based on individual subject analysis in the hemispheres without a paracingulate sulcus. The eye (red), tongue (yellow), hand (green), and foot (blue) foci in the cingulate and supplementary motor regions in the right (A) and left (B) hemispheres of subjects exhibiting no pcgs (right hemisphere: S1, S3–S6, S8–S12); left hemisphere: S3–S5, S7, S9, S12). Each dot corresponds to the location of the highest t-value observed in each subject during the performance of saccadic eye, tongue, foot, and hand movements in the cingulate cortex (see Tables 3–6, for a complete description of the increased activities observed during saccadic eye, tongue, foot, and hand movements, respectively) and in the SMA/SEF (see Tables 7–10, for a complete description of the increased activities observed during saccadic eye, tongue, foot, and hand movements, respectively). Increased activities are shown on sagittal sections on the average anatomical brain of subjects showing no pcgs in the right (A) and the left (B) hemispheres. The antero-posterior (y) and dorso-ventral (z) coordinates in the MNI standard stereotaxic space are indicated in red. Abbreviations: cgs, cingulate sulcus; pacs, paracentral sulcus; prpacs, pre-paracentral sulcus; vpcgs, vertical paracingulate sulcus; cs, central sulcus; meps, medial paracentral sulcus.

Figure 2.

Dispersion of the eye, tongue, hand, and foot foci of the cingulate and SMA/SEF based on individual subject analysis in the hemispheres without a paracingulate sulcus. The eye (red), tongue (yellow), hand (green), and foot (blue) foci in the cingulate and supplementary motor regions in the right (A) and left (B) hemispheres of subjects exhibiting no pcgs (right hemisphere: S1, S3–S6, S8–S12); left hemisphere: S3–S5, S7, S9, S12). Each dot corresponds to the location of the highest t-value observed in each subject during the performance of saccadic eye, tongue, foot, and hand movements in the cingulate cortex (see Tables 3–6, for a complete description of the increased activities observed during saccadic eye, tongue, foot, and hand movements, respectively) and in the SMA/SEF (see Tables 7–10, for a complete description of the increased activities observed during saccadic eye, tongue, foot, and hand movements, respectively). Increased activities are shown on sagittal sections on the average anatomical brain of subjects showing no pcgs in the right (A) and the left (B) hemispheres. The antero-posterior (y) and dorso-ventral (z) coordinates in the MNI standard stereotaxic space are indicated in red. Abbreviations: cgs, cingulate sulcus; pacs, paracentral sulcus; prpacs, pre-paracentral sulcus; vpcgs, vertical paracingulate sulcus; cs, central sulcus; meps, medial paracentral sulcus.

Figure 3.

Dispersion of the eye, tongue, hand, and foot foci of the cingulate and SMA/SEF based on individual subject analysis in the hemispheres exhibiting a paracingulate sulcus. The eye (red), tongue (yellow), hand (green), and foot (blue) foci in the cingulate and supplementary motor regions in the right (A) and left (B) hemispheres of subjects exhibiting a pcgs (right hemisphere: S2, S7; left hemisphere: S1–S2, S6, S8, S10–S11). Each color dot corresponds to the location of the highest t-value observed in each subject during the performance of the different movements in the cingulate cortex (see Tables 3–6, for a complete description of the increased activities observed during saccadic eye, tongue, foot, and hand movements, respectively) and in the SMA/SEF (see Tables 7–10, for a complete description of the increased activities observed during saccadic eye, tongue, foot, and hand movements, respectively). Increased activities are shown on sagittal sections on the average anatomical brain of subjects showing a pcgs in the right (A) and left (B) hemispheres. The antero-posterior (y) and dorso-ventral (z) coordinates in the MNI standard stereotaxic space are indicated in red. Abbreviations: cgs, cingulate sulcus; pcgs, paracingulate sulcus; pacs, paracentral sulcus; prpacs, pre-paracentral sulcus; vpcgs, vertical paracingulate sulcus; cs, central sulcus; meps, medial paracentral sulcus.

Figure 3.

Dispersion of the eye, tongue, hand, and foot foci of the cingulate and SMA/SEF based on individual subject analysis in the hemispheres exhibiting a paracingulate sulcus. The eye (red), tongue (yellow), hand (green), and foot (blue) foci in the cingulate and supplementary motor regions in the right (A) and left (B) hemispheres of subjects exhibiting a pcgs (right hemisphere: S2, S7; left hemisphere: S1–S2, S6, S8, S10–S11). Each color dot corresponds to the location of the highest t-value observed in each subject during the performance of the different movements in the cingulate cortex (see Tables 3–6, for a complete description of the increased activities observed during saccadic eye, tongue, foot, and hand movements, respectively) and in the SMA/SEF (see Tables 7–10, for a complete description of the increased activities observed during saccadic eye, tongue, foot, and hand movements, respectively). Increased activities are shown on sagittal sections on the average anatomical brain of subjects showing a pcgs in the right (A) and left (B) hemispheres. The antero-posterior (y) and dorso-ventral (z) coordinates in the MNI standard stereotaxic space are indicated in red. Abbreviations: cgs, cingulate sulcus; pcgs, paracingulate sulcus; pacs, paracentral sulcus; prpacs, pre-paracentral sulcus; vpcgs, vertical paracingulate sulcus; cs, central sulcus; meps, medial paracentral sulcus.

Figure 4.

Organization of the eye, tongue, hand, and foot regions of the cingulate and SMA/SEF in the hemispheres exhibiting a cingulate sulcus (A) and a paracingulate sulcus (B): Group analysis. Each color dot corresponds to the average MNI coordinates of the highest t-value observed during the performance of saccadic eye (red), tongue (yellow), foot (blue), and hand (green) movements in the cingulate cortex and in the SMA/SEF in the hemispheres without pcgs (A) and in the hemispheres displaying a pcgs (B). These average MNI coordinates are presented on a typical hemisphere (i.e. left hemisphere of S4) without a pcgs (left panel) and on a typical hemisphere (i.e. left hemisphere of S1) with a pcgs (right panel). The average coordinates are described in Tables 3–10. Abbreviations: cgs, cingulate sulcus; pcgs, paracingulate sulcus; pacs, paracentral sulcus; prpacs, pre-paracentral sulcus; vpcgs, vertical paracingulate sulcus; cs, central sulcus; meps, medial paracentral sulcus.

Figure 4.

Organization of the eye, tongue, hand, and foot regions of the cingulate and SMA/SEF in the hemispheres exhibiting a cingulate sulcus (A) and a paracingulate sulcus (B): Group analysis. Each color dot corresponds to the average MNI coordinates of the highest t-value observed during the performance of saccadic eye (red), tongue (yellow), foot (blue), and hand (green) movements in the cingulate cortex and in the SMA/SEF in the hemispheres without pcgs (A) and in the hemispheres displaying a pcgs (B). These average MNI coordinates are presented on a typical hemisphere (i.e. left hemisphere of S4) without a pcgs (left panel) and on a typical hemisphere (i.e. left hemisphere of S1) with a pcgs (right panel). The average coordinates are described in Tables 3–10. Abbreviations: cgs, cingulate sulcus; pcgs, paracingulate sulcus; pacs, paracentral sulcus; prpacs, pre-paracentral sulcus; vpcgs, vertical paracingulate sulcus; cs, central sulcus; meps, medial paracentral sulcus.

As shown in Figure 4, in the anterior cingulate motor cluster and bilaterally, we observed in an anterior-to-posterior direction: The saccadic eye movement motor region, the tongue motor region, the foot motor region, and finally the hand motor region. In the middle cingulate motor cluster, we observed in both hemispheres and in an anterior-to-posterior direction: The saccadic eye movement motor region, the tongue motor region, the hand motor region, and the foot motor region. Finally, in the posterior cingulate motor cluster, we observed in an anterior-to-posterior direction, the hand motor, then the foot motor focus, and finally another hand motor activation focus. Figure 5 compares the cingulate motor areas observed in the human in the present investigation with those reported in the monkey.

Figure 5.

Summary of the organization of activation foci related to specific body parts in the cingulate motor regions of the human (A) and monkey (B) brains: Eye (red), tongue (yellow), hand (green), and foot (blue). In A, the cingulate motor areas (labeled as RCZa, RCZp, and CCZ) are shown separately for subjects without a paracingulate sulcus (pcgs; case 1) and subjects with a pcgs (case 2). In B the cingulate motor areas are represented the location of the CMAr, CMAv, and CMAd regions observed in the monkey brain (based on Dum and Strick 2002). Abbreviations: cgs, cingulate sulcus; pcgs, paracingulate sulcus; pacs, paracentral sulcus; prpacs, pre-paracentral sulcus; vpcgs, vertical paracingulate sulcus; cs, central sulcus; meps, medial paracentral sulcus.

Figure 5.

Summary of the organization of activation foci related to specific body parts in the cingulate motor regions of the human (A) and monkey (B) brains: Eye (red), tongue (yellow), hand (green), and foot (blue). In A, the cingulate motor areas (labeled as RCZa, RCZp, and CCZ) are shown separately for subjects without a paracingulate sulcus (pcgs; case 1) and subjects with a pcgs (case 2). In B the cingulate motor areas are represented the location of the CMAr, CMAv, and CMAd regions observed in the monkey brain (based on Dum and Strick 2002). Abbreviations: cgs, cingulate sulcus; pcgs, paracingulate sulcus; pacs, paracentral sulcus; prpacs, pre-paracentral sulcus; vpcgs, vertical paracingulate sulcus; cs, central sulcus; meps, medial paracentral sulcus.

Discussion

The present study demonstrated the existence of 3 clusters of motor activation foci within the cingulate/paracingulate sulcal region in the human brain. Importantly, these 3 cingulate motor clusters can be clearly dissociated from the cluster of activation foci in the supplementary motor region, which is more dorsally located on the medial surface of the hemisphere (Figs 1–3). The other major contribution of the present study is the demonstration that the location of these 3 cingulate motor clusters relates to specific morphological features of the cingulate/paracingulate sulcal region. It also provides clear evidence that these motor regions are somatotopically organized.

The demonstration of 3 motor clusters within mid-cingulate region of the human brain is consistent with the hypothesis of Picard and Strick that 3 cingulate motor regions may exist in the human brain (Picard and Strick 1996, 2001). These authors suggested that the human anterior rostral cingulate zone (RCZa) may be the homolog of monkey CMAr, a region involved in higher order aspects of motor behavior. Our anterior cluster of motor activations at the rostral part of the cingulate region, above the genu of the corpus callosum (Figs 2–4), is consistent with an anterior cingulate motor zone in the human brain. The other 2 cingulate motor zones proposed by Picard and Strick (1996, 2001) were a posterior rostral cingulate zone (RCZp) and a caudal cingulate zone (CCZ). They tentatively proposed that the RCZp might correspond to monkey CMAv and that the CCZ may correspond to CMAd (Picard and Strick 1996, 2003). Our middle and posterior clusters are likely to correspond, respectively, to the RCZp and CCZ. This hypothesis is also supported by a recent study showing distinct probabilistic connectivity profiles of 9 regions of the cingulate cortex with magnetic diffusion tractography (Beckmann et al. 2009). Our 3 clusters correspond well to clusters 4, 5, and 6 in this diffusion tractography study, which appeared to have motor function as shown by probabilistic interconnections with motor structures, such as the dorsal striatum, the premotor cortex, and the precentral cortex. Importantly, these cingulate motor areas could be clearly dissociated from activation foci in the SMA. Note that we did not observe increased activity within the pre-SMA during the performance of the simple movements required. The available evidence suggests that the pre-SMA is involved in self-generated actions, rather than in actions instructed by external cues in the environment such as the ones that our subjects had to perform in the present experiment (see Nachev et al. 2008 for review).

An important discovery of the present investigation is that the location of the cingulate motor regions in the human brain relates to specific morphological features of the cingulate/paracingulate sulcal complex. The posterior cluster of motor foci was located within the cgs immediately below the paracentral lobule and extending anteriorly as far as the pacs (i.e. where the paracentral lobule ends) and contains 2 hand and 1 foot representation. The middle cluster of motor activations was observed within the cgs close to the intersection of cgs/pcgs and the prpacs (i.e. anterior to the paracentral lobule at the level of the supplementary motor cortex). Finally, the anterior motor cluster was located in individual subjects at the intersection between cgs/pcgs and vpcgs. Note that the hand and foot activity for the middle and anterior clusters was consistently located within the cgs, but the saccadic and tongue movement activity lay in the pcgs if it extended caudally to this region (Figs 2–4). Both clusters include a saccadic eye movement region located anterior and dorsal to the tongue region, itself located anterior to the hand and foot representations.

Although the available evidence concerning the existence of representation of eye movements in the cingulate motor regions, in both the monkey and the human brains, is weak, it provides indirect support to the present results that demonstrated 2 cingulate eye fields. In the human brain, Paus et al. (1993) reported 2 regions of the cgs in which activity was related to the performance of an oculomotor conditional task. In the monkey, a connectivity study by Wang et al. (2004) reported 2 cingulate regions interconnected with the frontal eye field. The first one, the rostral cingulate eye field, was located anterior to the forelimb movement region within the CMAr. The second one, the caudal cingulate eye field, was located adjacent to the forelimb movement region within the CMAc. Furthermore, in a (14C)-2-deoxyglucose functional imaging study in the monkey, Moschovakis et al. (2004) have reported 2 regions within the anterior cingulate cortex that are related to extraocular motoneurons.

Representations of the hand and foot have been reported in each one of the CMAr, CMAv, and CMAd regions in monkeys (Dum and Strick 1991, 1993; He et al. 1995). In the present study, we show the existence of 1 foot representation in each of the 3 motor zones, and the existence of 2 hand representations in the posterior zone and 1 hand representation in the middle and anterior zones. Our observation that the posterior zone contains 2 hand representations and that the middle and anterior zones contain 1 hand representation is consistent with intracortical microstimulation studies in the monkey, showing that the CMAd (the putative homolog of our posterior zone) contains 2 arm representations and that both CMAv (the putative homolog of our middle zone) and CMAr (the putative homolog of our anterior zone) contain 1 arm representation (Luppino et al. 1991; Dum and Strick 1993). In addition, the investigations in the monkey reported a leg region in each one of the motor areas, located adjacent to the arm representations; the latter finding being consistent with our results in the human brain. Importantly, the observation that the human homolog of the monkey CMAd contains, as in the macaque monkey, 2 arm representations could not be demonstrated in the meta-analysis by Picard and Strick (1996) and in the diffusion-weighted imaging study by Beckmann et al. (2009). This result provides strong evidence that this part of the human brain resembles the CMAd of other primates.

Concerning the existence of representations of the face (mouth/tongue) in the cingulate motor areas, the only pertinent information comes, indirectly, from speech production activation foci in the cingulate region of the brain. Paus et al. (1993), in a positron emission tomography study using cognitive tasks with different motor outputs, such as hand movements, speech production, and saccadic eye movements, showed that the location of activation foci within the cingulate cortex during the performance of these tasks differed, depending of the type of motor output. There were 2 hand response-related foci, 1 located posterior, and 1 anterior to the anterior commissure, as well as 2 speech-related foci (1 anterior and 1 posterior) and 2 saccadic eye movement foci (1 anterior and 1 posterior), both located at similar locations and anterior to the anterior commissure. The most posterior speech and saccadic eye regions were located immediately anterior to the anterior hand region. The most anterior speech and saccadic eye regions were located in front of the genu of the corpus callosum (Paus et al. 1998; Koski and Paus 2000; Paus 2001). Based on the reported standard stereotaxic coordinates, the posterior region related to hand movement output in the Paus et al. study appears to fall within our posterior motor area, while the anterior hand response foci and posterior speech/saccadic eye movement foci fall within our middle cingulate motor cluster. Note, however, that the most anterior speech/saccadic eye movement-related activity reported in the Paus et al. study falls clearly anterior to our anterior cluster. Our cluster is located just posterior to the genu of the corpus callosum, probably in area 24c′, and not in the pure area 24c. This difference should not be surprising because the conflict cognitive tasks would be expected to reveal cognitive activity that is not necessarily related to motor output (Pardo et al. 1990; MacDonald et al. 2000). Interestingly, in the monkey, area 24c is likely to contain a face motor cluster as the electrical stimulation of the perigenual aspect of areas 24c and 32 in monkey elicits vocalization (for review, see Jurgens 2009). Secondly, Chassagnon et al. (2008) have shown that the electrical stimulation of some sites within the cgs elicited speech arrest in epileptic patients undergoing brain surgery. These sites were located anterior to the representation of the leg and arm. Altogether, these results reinforce our data showing that, in the middle (RCZp) and anterior cluster (RCZa), the saccade and tongue motor areas are located anterior to the foot and hand motor areas. Finally, in their neuroimaging meta-analysis study, Picard and Strick (1996) concluded that, whereas within both the RCZa and RCZp, a face area might be located anterior to an arm motor area, only an arm area appeared to lie in the CCZ. Our data are consistent with these indirect observations as we observed no saccade and tongue motor areas in our most caudal cingulate motor cluster (probably, the CCZ).

The present functional neuroimaging results indicate a comparable organization of the cingulate motor areas between the human and the nonhuman primate brain (Fig. 5). The tripartite organization of the cingulate motor areas appears to be a general feature of cingulate organization in primates and has also been observed in prosimians, such as bushbabies (Wu et al. 2000), suggesting that the human cingulate organization is conforming to a phylogenetically old pattern.

The present results raise one critical question that must be resolved: How do the cingulate regions involved in various high-level cognitive processes relate to the cingulate motor maps demonstrated in the present study, and in particular, the more anterior cingulate motor area (i.e. RCZa)? In a recent experiment, we showed that a cingulate region located slightly more anterior to the RCZa, but overlapping partly with it, was involved in the analysis of visual behavioral feedback in exploratory situations (Amiez et al. 2012). At the present time, it is unclear how feedback-related activations reported in the anterior cingulate region relate to the cingulate motor areas and ongoing experiments aim to test these relationships.

Notes

This research was supported by the Canadian Institutes of Health Research (CIHR) grant FRN 37753 to M.P. C.A. was supported by Neurodis Foundation. We thank E. Rubin-Ferreira, T Sprung-Much, and R. Pavan for their help with data acquisition and analysis. Conflict of Interest: None declared.

References

Amiez
C
Kostopoulos
P
Champod
AS
Petrides
M
Local morphology predicts functional organization of the dorsal premotor region in the human brain
J Neurosci
 , 
2006
, vol. 
26
 (pg. 
2724
-
2731
)
Amiez
C
Petrides
M
Anatomical organization of the eye fields in the human and non-human primate frontal cortex
Prog Neurobiol
 , 
2009
, vol. 
89
 (pg. 
220
-
230
)
Amiez
C
Sallet
J
Procyk
E
Petrides
M
Modulation of feedback related activity in the rostral anterior cingulate cortex during trial and error exploration
Neuroimage
 , 
2012
, vol. 
63
 (pg. 
1078
-
1090
)
Arienzo
D
Babiloni
C
Ferretti
A
Caulo
M
Del Gratta
C
Tartaro
A
Rossini
PM
Romani
GL
Somatotopy of anterior cingulate cortex (ACC) and supplementary motor area (SMA) for electric stimulation of the median and tibial nerves: an fMRI study
Neuroimage
 , 
2006
, vol. 
33
 (pg. 
700
-
705
)
Beckmann
M
Johansen-Berg
H
Rushworth
MF
Connectivity-based parcellation of human cingulate cortex and its relation to functional specialization
J Neurosci
 , 
2009
, vol. 
29
 (pg. 
1175
-
1190
)
Buda
M
Fornito
A
Bergstrom
ZM
Simons
JS
A specific brain structural basis for individual differences in reality monitoring
J Neurosci
 , 
2011
, vol. 
31
 (pg. 
14308
-
14313
)
Chassagnon
S
Minotti
L
Kremer
S
Hoffmann
D
Kahane
P
Somatosensory, motor, and reaching/grasping responses to direct electrical stimulation of the human cingulate motor areas
J Neurosurg
 , 
2008
, vol. 
109
 (pg. 
593
-
604
)
Derrfuss
J
Vogt
VL
Fiebach
CJ
von Cramon
DY
Tittgemeyer
M
Functional organization of the left inferior precentral sulcus: dissociating the inferior frontal eye field and the inferior frontal junction
Neuroimage
 , 
2012
, vol. 
59
 (pg. 
3829
-
3837
)
Dum
RP
Strick
PL
Vogt
B
Gabriel
M
Cingulate motor areas
Neurobiology of cingulate cortex and limbic thalamus: a comprehensive handbook
 , 
1993
Boston
Birkhäuser
(pg. 
415
-
441
)
Dum
RP
Strick
PL
The origin of corticospinal projections from the premotor areas in the frontal lobe
J Neurosci
 , 
1991
, vol. 
11
 (pg. 
667
-
689
)
Dum
RP
Strick
PL
Spinal cord terminations of the medial wall motor areas in macaque monkeys
J Neurosci
 , 
1996
, vol. 
16
 (pg. 
6513
-
6525
)
Dum
RP
Strick
PL
Motor areas in the frontal lobe of the primate
Physiol Behav
 , 
2002
, vol. 
77
 (pg. 
677
-
682
)
Fornito
A
Wood
SJ
Whittle
S
Fuller
J
Adamson
C
Saling
MM
Velakoulis
D
Pantelis
C
Yucel
M
Variability of the paracingulate sulcus and morphometry of the medial frontal cortex: associations with cortical thickness, surface area, volume, and sulcal depth
Hum Brain Mapp
 , 
2008
, vol. 
29
 (pg. 
222
-
236
)
Friston
KJ
Frith
CD
Frackowiak
RS
Turner
R
Characterizing dynamic brain responses with fMRI: a multivariate approach
Neuroimage
 , 
1995
, vol. 
2
 (pg. 
166
-
172
)
Friston
KJ
Frith
CD
Turner
R
Frackowiak
RS
Characterizing evoked hemodynamics with fMRI
Neuroimage
 , 
1995
, vol. 
2
 (pg. 
157
-
165
)
Friston
KJ
Holmes
AP
Poline
JB
Grasby
PJ
Williams
SC
Frackowiak
RS
Turner
R
Analysis of fMRI time-series revisited
Neuroimage
 , 
1995
, vol. 
2
 (pg. 
45
-
53
)
Galea
MP
Darian-Smith
I
Multiple corticospinal neuron populations in the macaque monkey are specified by their unique cortical origins, spinal terminations, and connections
Cereb Cortex
 , 
1994
, vol. 
4
 (pg. 
166
-
194
)
Grafton
ST
Woods
RP
Mazziotta
JC
Within-arm somatotopy in human motor areas determined by positron emission tomography imaging of cerebral blood flow
Exp Brain Res
 , 
1993
, vol. 
95
 (pg. 
172
-
176
)
He
SQ
Dum
RP
Strick
PL
Topographic organization of corticospinal projections from the frontal lobe: motor areas on the medial surface of the hemisphere
J Neurosci
 , 
1995
, vol. 
15
 (pg. 
3284
-
3306
)
Hutchins
KD
Martino
AM
Strick
PL
Corticospinal projections from the medial wall of the hemisphere
Exp Brain Res
 , 
1988
, vol. 
71
 (pg. 
667
-
672
)
Jurgens
U
The neural control of vocalization in mammals: a review
J Voice
 , 
2009
, vol. 
23
 (pg. 
1
-
10
)
Koski
L
Paus
T
Functional connectivity of the anterior cingulate cortex within the human frontal lobe: a brain-mapping meta-analysis
Exp Brain Res
 , 
2000
, vol. 
133
 (pg. 
55
-
65
)
Luppino
G
Matelli
M
Camarda
RM
Gallese
V
Rizzolatti
G
Multiple representations of body movements in mesial area 6 and the adjacent cingulate cortex: an intracortical microstimulation study in the macaque monkey
J Comp Neurol
 , 
1991
, vol. 
311
 (pg. 
463
-
482
)
MacDonald
AW
3rd
Cohen
JD
Stenger
VA
Carter
CS
Dissociating the role of the dorsolateral prefrontal and anterior cingulate cortex in cognitive control
Science
 , 
2000
, vol. 
288
 (pg. 
1835
-
1838
)
Makris
N
Kaiser
J
Haselgrove
C
Seidman
LJ
Biederman
J
Boriel
D
Valera
EM
Papadimitriou
GM
Fischl
B
Caviness
VS
Jr
, et al.  . 
Human cerebral cortex: a system for the integration of volume- and surface-based representations
Neuroimage
 , 
2006
, vol. 
33
 (pg. 
139
-
153
)
Mitz
AR
Godschalk
M
Eye-movement representation in the frontal lobe of rhesus monkeys
Neurosci Lett
 , 
1989
, vol. 
106
 (pg. 
157
-
162
)
Morecraft
RJ
Schroeder
CM
Keifer
J
Organization of face representation in the cingulate cortex of the rhesus monkey
Neuroreport
 , 
1996
, vol. 
7
 (pg. 
1343
-
1348
)
Morecraft
RJ
Van Hoesen
GW
Cingulate input to the primary and supplementary motor cortices in the rhesus monkey: evidence for somatotopy in areas 24c and 23c
J Comp Neurol
 , 
1992
, vol. 
322
 (pg. 
471
-
489
)
Moschovakis
AK
Gregoriou
GG
Ugolini
G
Doldan
M
Graf
W
Guldin
W
Hadjidimitrakis
K
Savaki
HE
Oculomotor areas of the primate frontal lobes: a transneuronal transfer of rabies virus and [14C]-2-deoxyglucose functional imaging study
J Neurosci
 , 
2004
, vol. 
24
 (pg. 
5726
-
5740
)
Nachev
P
Kennard
C
Husain
M
Functional role of the supplementary and pre-supplementary motor areas
Nat Rev Neurosci
 , 
2008
, vol. 
9
 (pg. 
856
-
869
)
Pardo
JV
Pardo
PJ
Janer
KW
Raichle
ME
The anterior cingulate cortex mediates processing selection in the Stroop attentional conflict paradigm
Proc Natl Acad Sci USA
 , 
1990
, vol. 
87
 (pg. 
256
-
259
)
Paus
T
Primate anterior cingulate cortex: where motor control, drive and cognition interface
Nat Rev Neurosci
 , 
2001
, vol. 
2
 (pg. 
417
-
424
)
Paus
T
Koski
L
Caramanos
Z
Westbury
C
Regional differences in the effects of task difficulty and motor output on blood flow response in the human anterior cingulate cortex: a review of 107 PET activation studies
Neuroreport
 , 
1998
, vol. 
9
 (pg. 
R37
-
47
)
Paus
T
Otaky
N
Caramanos
Z
MacDonald
D
Zijdenbos
A
D'Avirro
D
Gutmans
D
Holmes
C
Tomaiuolo
F
Evans
AC
In vivo morphometry of the intrasulcal gray matter in the human cingulate, paracingulate, and superior-rostral sulci: hemispheric asymmetries, gender differences and probability maps
J Comp Neurol
 , 
1996
, vol. 
376
 (pg. 
664
-
673
)
Paus
T
Petrides
M
Evans
AC
Meyer
E
Role of the human anterior cingulate cortex in the control of oculomotor, manual, and speech responses: a positron emission tomography study
J Neurophysiol
 , 
1993
, vol. 
70
 (pg. 
453
-
469
)
Paus
T
Tomaiuolo
F
Otaky
N
MacDonald
D
Petrides
M
Atlas
J
Morris
R
Evans
AC
Human cingulate and paracingulate sulci: pattern, variability, asymmetry, and probabilistic map
Cereb Cortex
 , 
1996
, vol. 
6
 (pg. 
207
-
214
)
Picard
N
Strick
PL
Activation of the supplementary motor area (SMA) during performance of visually guided movements
Cereb Cortex
 , 
2003
, vol. 
13
 (pg. 
977
-
986
)
Picard
N
Strick
PL
Imaging the premotor areas
Curr Opin Neurobiol
 , 
2001
, vol. 
11
 (pg. 
663
-
672
)
Picard
N
Strick
PL
Motor areas of the medial wall: a review of their location and functional activation
Cereb Cortex
 , 
1996
, vol. 
6
 (pg. 
342
-
353
)
Shima
K
Aya
K
Mushiake
H
Inase
M
Aizawa
H
Tanji
J
Two movement-related foci in the primate cingulate cortex observed in signal-triggered and self-paced forelimb movements
J Neurophysiol
 , 
1991
, vol. 
65
 (pg. 
188
-
202
)
Vogt
BA
Nimchinsky
EA
Vogt
LJ
Hof
PR
Human cingulate cortex: surface features, flat maps, and cytoarchitecture
J Comp Neurol
 , 
1995
, vol. 
359
 (pg. 
490
-
506
)
Vogt
BA
Vogt
L
Farber
NB
Bush
G
Architecture and neurocytology of monkey cingulate gyrus
J Comp Neurol
 , 
2005
, vol. 
485
 (pg. 
218
-
239
)
Wang
Y
Matsuzaka
Y
Shima
K
Tanji
J
Cingulate cortical cells projecting to monkey frontal eye field and primary motor cortex
Neuroreport
 , 
2004
, vol. 
15
 (pg. 
1559
-
1563
)
Wang
Y
Shima
K
Sawamura
H
Tanji
J
Spatial distribution of cingulate cells projecting to the primary, supplementary, and pre-supplementary motor areas: a retrograde multiple labeling study in the macaque monkey
Neurosci Res
 , 
2001
, vol. 
39
 (pg. 
39
-
49
)
Wu
CW
Bichot
NP
Kaas
JH
Converging evidence from microstimulation, architecture, and connections for multiple motor areas in the frontal and cingulate cortex of prosimian primates
J Comp Neurol
 , 
2000
, vol. 
423
 (pg. 
140
-
177
)