Three-dimensional probabilistic maps of the occipital sulci of the human brain in standardized stereotaxic space

Neuroscience 151 (2008) 174 –185

THREE-DIMENSIONAL PROBABILISTIC MAPS OF THE OCCIPITAL SULCI OF THE HUMAN BRAIN IN STANDARDIZED STEREOTAXIC SPACE G. IARIA,a* S. ROBBINSb AND M. PETRIDESb

Zeki, 1969, 1974, 1978a,b; Van Essen and Zeki, 1978). In recent years, developments in functional neuroimaging in normal human subjects, such as functional magnetic resonance imaging (fMRI), have permitted the mapping of several visual areas of the human brain (Sereno and Tootell, 2005). Functional localization of these visual areas includes V1, V2, V3, V3A, V4, V5/MT, and V6 (Anderson et al., 1996; Barton et al., 1996; Bense et al., 2006; Brewer et al., 2005; de Jong et al., 1994; DeYoe et al., 1996; Dougherty et al., 2003; Dumoulin et al., 2000; Dupont et al., 1994; Engel et al., 1997; Hadjikhani et al., 1998; Hasnain et al., 1998; Itoh et al., 2005; Sack et al., 2006; Sereno et al., 1994, 1995; Shipp et al., 1995; Shulman et al., 1998; Stiers et al., 2006; Tootell et al., 1996, 1997; Tootell and Hadjikhani 2001; Vallines and Greenlee, 2006; Walters et al., 2003; Watson et al., 1993; Zeki et al., 1991). The lack of standard terminology and adequate description of the sulcal patterns of the human occipital region, with the exception of the calcarine sulcus that is evident from inspection of any one of several modern standard textbooks of neuroanatomy (e.g. Carpenter, 1996; Nolte, 2002), makes it difficult to establish clear relationships between sulcal landmarks and identified visual areas with functional neuroimaging.

a

Human Vision and Eye Movement Laboratory, Faculty of Medicine, University of British Columbia, VGH Eye Care Center, Section D, 2550 Willow Street, Vancouver, British Columbia, Canada V5Z 3N9

b

Montreal Neurological Institute, McGill University, 3801 University Street, Montreal, Quebec, Canada H3A 2B4

Abstract—Developments in functional neuroimaging in normal human subjects, such as functional magnetic resonance imaging (fMRI), have permitted the mapping of several visual areas of the human brain and have already provided provisional identification of some of the visual areas that were first described in nonhuman primates. However, the lack of a detailed description of the sulcal patterns of the human occipital lobe makes it difficult to establish clear relationships between sulcal landmarks and identified visual areas with functional neuroimaging. In the present study we used magnetic resonance images to investigate the morphological variation of the human occipital sulci in both the left and right hemispheres of 40 normal adult human brains. We identified 11 occipital sulci, the parieto-occipital fissure and the temporo-occipital incisure, and their corresponding gray matter voxels were marked in the magnetic resonance volumes which had been transformed into the Montreal Neurological Institute standard proportional stereotaxic space. Probability maps were then constructed for each occipital sulcus. These probability maps provide a quantitative measure of the variability of the occipital sulci in standard stereotaxic space and are a useful tool to identify the location of voxels of other magnetic resonance imaging images transformed in the same stereotaxic space. © 2008 IBRO. Published by Elsevier Ltd. All rights reserved.

EXPERIMENTAL PROCEDURES Subjects We examined the magnetic resonance imaging (MRI) scans of 40 human brains (both the left and right hemispheres) with the purpose of identifying and marking the occipital sulci. These MRI scans were randomly selected from those collected for the International Consortium for Brain Mapping project (Mazziotta et al., 1995a,b). The sample consisted of 17 females (mean age 25.5 years, S.D. 5.3) and 23 males (mean age 25 years, S.D. 5.3). Participants were right-handed and none had a positive history of neurological or psychiatric disorders. All subjects gave informed consent.

Key words: sulcus, visual-cortex, morphology, lunate, calcarine, atlas.

The existence of multiple visual areas in the cerebral cortex beyond the primary visual cortex (i.e. the striate cortex along the calcarine sulcus) was initially demonstrated in several single neuron recording studies mapping the visual field in monkeys (e.g. Allman and Kaas, 1971; Felleman and Van Essen, 1991; Galletti et al., 1999; Kaas, 2004;

MRI The MRI scans were performed on a Philips Gyroscan 1.5-T superconducting magnet system (Philips Medical System, Best, the Netherlands). A fast-field echo 3-D acquisition sequence was used to collect 160 contiguous 1 mm T1-weighted images (Tr⫽18 ms, Te⫽10 ms, flip angle⫽30°) in the sagittal plane. Each MR volume was transformed into the Montreal Neurological Institute (MNI) standardized stereotaxic space (Evans et al., 1992; Mazziotta et al., 1995a,b), which is based on that of Talairach and Tournoux (1988), to normalize and correct the images for interindividual differences in gross brain size. For each MR volume, the transformation was determined by an automated registration using 3D cross-correlation (Collins et al., 1994) to a target image that was the intensity average of 305 brain volumes previously aligned

*Corresponding author. Tel: ⫹1-604-875-4111x62929; fax: ⫹1-604-8754302. E-mail address: [email protected] (G. Iaria). Abbreviations: ACS, anterior calcarine sulcus; BCS, body of the calcarine sulcus; CSF, cerebrospinal fluid; IOS, inferior occipital sulcus; ISGS, inferior sagittal sulcus; LiS, lingual sulcus; LOS, lateral occipital sulcus; LuS, lunate sulcus; MNI, Montreal Neurological Institute; MRI, magnetic resonance imaging; PCS, posterior collateral sulcus, i.e. the occipital extension of the collateral sulcus; POF, parieto-occipital fissure; RCS, retrocalcarine sulcus; SSGS, superior sagittal sulcus; TO, temporo-occipital incisure; TOS, transverse occipital sulcus.

0306-4522/08$32.00⫹0.00 © 2008 IBRO. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.neuroscience.2007.09.050

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used to determine the upper intensity threshold for voxels of the cerebrospinal fluid (CSF). All voxels were automatically classified according to tissue type (Kollokian, 1996). Initially, the voxels considered to contain CSF between the sulcal banks were marked by the investigator. The gray-matter voxels extending 1 mm on either side of the banks of the sulcus, adjacent to those in the sulcal CSF, were automatically included in the set of voxels constituting the sulcus. See Fig. 1 for a schematic view of the main sulci present on the medial and lateral surfaces of the human occipital lobe.

Gender differences The subjects were split into male and female groups and the variability of the sulci between the two groups was analyzed. For each sulcus in each group, an average sulcus was computed from the subjects’ sulci using the distance mean method (Robbins et al., 2004), which generates an extended (non-zero volume) structure. For each subject, we computed a 90%-trimmed Hausdorff distance (Rucklidge, 1996) between the subject’s sulcus and the mean sulcus. This measures the closeness of two extended structures: 90% of each structure lies within this distance (in millimeters) of the other. The variability within each group is summarized by the median distance to the mean sulcus (see Table 1). The two groups were compared using the distribution-free KolmogorovSmirnov test, and the resulting P-values are reported in Table 1. Overall, the data did not reveal a significant effect of gender showing a similar variability within both female and male groups. The only evidence for group difference appeared in the right body calcarine sulcus (BCS) and left lateral occipital sulcus (LOS), in both cases being less variable in females.

Probability mapping

Fig. 1. Schematic drawings of the main occipital sulci present on the medial (a) and lateral (b) surface of the human occipital lobe.

After labeling the voxels comprising each occipital sulcus, we constructed 3D probability maps of each sulcus separately. For each sulcus, the probability values are displayed by means of a color scale range. The minimum value of each scale is 0.1 (10% of the subjects included in this study). The highest probability value varied for different sulci. The maps were constructed by dividing, at each particular 3D stereotaxic location, the number of times a voxel belonged to the sulcus of interest by the number of subjects examined. These probability values, which are displayed in color-coded maps, thus represent the likelihood that any voxel Table 1. Median distances from mean sulcus and probability values

to the Talairach atlas (Evans et al., 1992). The image data were then re-sampled onto a standard grid with cubical voxels 1 mm wide. The x-coordinates were used to define the mediolateral axis (left–right; positive⫽right hemisphere), the y-coordinates were used to define the rostrocaudal axis (anterior–posterior; positive⫽rostral to anterior commissure), and the z-coordinates were used to define the dorsoventral axis (superior–inferior; positive⫽superior to a horizontal line drawn through anterior and posterior commissures).

Localization of the occipital sulci The occipital sulci were manually identified using DISPLAY, an interactive 3-D imaging software package (MacDonald, 1996), which displays a 3D view of the brain surface as well as sections in the coronal, horizontal, and sagittal planes. The location of the sulcus under investigation was marked while moving from voxel to voxel in any one of the three planes of sections. Movement of the cursor to any point in any section results in automatic updating in all other sections. This automatic updating allows the investigator to identify and mark accurately the extent and direction of a particular sulcus by following the sulcus within its depth and not simply from the surface. DISPLAY also provides the option of generating a histogram of the image intensity values, which is

Sulcus

Left hemisphere Median (mm)

ACS BCS IOS ISGS LiS LOS LuS PCS POF RCS SSGS TO TOS

Male

Female

3.7 4.9 9.0 7.5 6.3 13 12 7.6 6.5 6.5 7.8 9.0 10

4.1 5.5 8.6 8.8 6.5 8.4 14 7.6 5.5 6.7 9.4 9.6 12

Right hemisphere P-value

0.95 0.99 0.49 0.47 0.98 0.0023* 0.076 0.6 0.62 0.64 0.96 0.83 0.76

Median (mm) Male

Female

3.3 5.9 7.8 5.9 7.3 10 13 9.2 5.9 7.1 7.1 9.8 9.0

3.9 3.9 9.0 7.3 5.7 9.6 11 8.2 5.5 6.5 6.5 6.5 10

P-value

0.62 0.0075* 0.39 0.83 0.28 0.53 0.88 0.99 0.33 0.95 0.52 0.086 0.89

Data are reported for each sulcus in both left and right hemispheres according to female and male gender groups. * Indicates statistically significant difference.

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Fig. 2. Probability maps on coronal sections of the POF, RCS (retro-calcarine sulcus) and LOS. The probability maps of the sulci are superimposed on the average brain of the MNI (Evans et al., 1992) and the coordinates provided are within the MNI standard proportional stereotaxic space.

in MNI space will be classified as part of the sulcus. For example, if the value at the given x, y, z location is 0.6 for a particular sulcus, then this location was occupied by a voxel that belong to that sulcus in 60% of the subjects examined. The probability maps are then superimposed on the intensity-averaged target image of 305 brains (Evans et al., 1992) that have been transformed in MNI space and the stereotaxic x, y, z coordinate values are provided in the MNI standard proportional space.

RESULTS In a previous study, we identified and described in detail 11 occipital sulci, the parieto-occipital fissure (POF) and the temporo-occipital incisure (TO) (Iaria and Petrides, 2007). In most cases, we adopted a nomenclature that was consistent with both the classical and contemporary investigations. When the nomenclature of a certain sulcus was not consistently used, we adopted the term that in our opinion was most appropriate for that specific sulcus (Iaria and Petrides, 2007). The probability maps of the POF and TO are available in coronal (POF, Fig. 2; TO, Fig. 4) and horizontal (POF, Fig. 8; TO, Fig. 10) sections. The calcarine sulcus is the main sulcus on the medial part of the occipital lobe, extending from just below the splenium of the corpus callosum all the way to the occipital

pole. The POF extends from the dorsal surface of the hemisphere all the way down, in an oblique direction, to join the anterior part of the calcarine sulcus, thus delimiting the upper part of the medial occipital lobe known as the cuneus. In the present description, we refer to the anterior part, which extends in an antero-ventral direction in front of the point of intersection with the POF, as the anterior calcarine sulcus (ACS). The probability maps of the ACS are provided in coronal (Fig. 4) and horizontal (Fig. 10) sections. The most posterior tail of the calcarine sulcus, which often fans out into an upper and lower part, is referred as the retrocalcarine sulcus (RCS). The probability maps of the RCS is provided in coronal (Fig. 2) and horizontal (Fig. 8) sections. We refer to the remaining main part of the calcarine sulcus as the BCS. The probability maps of the BCS is provided in coronal (Fig. 3) and horizontal (Fig. 9) sections. The inferior sagittal sulcus (ISGS) of the cuneus is located just dorsal to the BCS and runs, more or less, parallel to it. The term has been adopted by Economo and Koskinas (1925) to distinguish it from another somewhat less frequent superior sagittal sulcus of the cuneus (SSGS). In the present study, we have adopted the terminology of Economo and Koskinas (1925) for both the sulci of the

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Fig. 3. Probability map on coronal sections of the BCS and IOS. The probability maps of the sulci are superimposed on the average brain of the MNI (Evans et al., 1992) and the coordinates provided are within the MNI standard proportional stereotaxic space.

cuneus. The probability maps of the ISGS and SSGS are provided in coronal (ISGS, Fig. 4; SSGS, Fig. 5) and horizontal (ISGS, Fig. 10; SSGS, Fig. 11) sections. The posterior branch of the collateral sulcus (PCS) is located in the inferior part of the occipital lobe (below the calcarine sulcus), running, more or less, parallel to the BCS, thus delimiting the lingual gyrus. Within the lingual gyrus, occasionally, there is a sulcus running, more or less, parallel to the BCS, dividing it into a superior and an inferior lingual gyrus. This sulcus has been referred to as the lingual sulcus (LiS) in the classical literature (e.g. Economo and Koskinas, 1925) and, more recently, as the intralingual sulcus (Ono et al., 1990). Here, we have retained the classical term LiS. The probability maps of the PCS and the LiS are available in coronal (PCS, Fig. 5; LiS, Fig. 6) and horizontal (PCS, Fig. 11; LiS, Fig. 12) sections. The lunate sulcus (LuS) is a dorso-ventrally oriented sulcus that lies at the most caudal part of the lateral occipital lobe, often forming a concavity directed toward the occipital pole. In MRI images, it is very hard to identify this sulcus both because of its shape and its location on the lateral to medial curvature of the occipital pole. The probability maps of the LuS are provided in coronal (Fig. 6) and horizontal (Fig. 12) sections. The LOS is a horizontally oriented sulcus that can be identified immediately anterior to the LuS (Duvernoy, 1991; Eberstaller, 1890; Economo and Koskinas, 1925; Ono et al., 1990). This sulcus usually blends, more or less, with the middle part of the LuS and divides the lateral surface of the occipital lobe into a superior and an inferior part. The probability maps of the LOS are provided in coronal (Fig. 2) and horizontal (Fig. 8) sections.

The inferior occipital sulcus (IOS) is located in the inferior part of the occipital region, close to the base of the hemisphere. The caudal end of the IOS runs close to the most ventral part of the LuS. The probability maps of the IOS are provided in coronal (Fig. 3) and horizontal (Fig. 9) sections. The transverse occipital sulcus (TOS) can be identified in the superior part of the occipital region (Elliot Smith, 1904a; Duvernoy, 1991). This sulcus, which is more or less dorso-ventrally oriented, lies caudal to the POF and joins the occipital extension of the intraparietal sulcus. The probability maps of the TOS are available in coronal (Fig. 7) and horizontal (Fig. 13) sections.

DISCUSSION In a previous study, we identified and described in detail the patterns formed by the sulci found in the occipital lobe of the human brain (Iaria and Petrides, 2007). Here, we marked the voxels occupied by these sulci on MRI volumes transformed into the MNI standardized proportional stereotaxic space in order to create probability maps of the occipital sulci. These probability maps provide a quantitative measure of the variability in location of the occipital sulci in standardized stereotaxic proportional space and are a useful tool to identify the location of voxels of other MRI images transformed in the same stereotaxic space. Thus, the availability of these maps should help in the identification of the occipital sulci and facilitate the study of the relation of the various visual areas identified with functional MRI to particular sulci of the human brain. The relation of the calcarine sulcus to the striate cortex has been the subject of intense investigation

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Fig. 4. Probability map on coronal sections of the ACS, ISGS and TO. The probability maps of the sulci are superimposed on the average brain of the MNI (Evans et al., 1992) and the coordinates provided are within the MNI standard proportional stereotaxic space.

since the beginning of the 20th century. anatomical studies (e.g. Bolton, 1900; 1904a), the ACS, i.e. the extension of sulcus anterior to the point of intersection

In the classic Elliot Smith, the calcarine with the POF,

is described as the border between the limbic cortex lying on the isthmus and the striate cortex found only on the ventral bank of the calcarine sulcus. Caudal to the point of intersection of the POF with the calcarine sul-

Fig. 5. Probability map on coronal sections of the SSGS and PCS. The probability maps of the sulci are superimposed on the average brain of the MNI (Evans et al., 1992) and the coordinates provided are within the MNI standard proportional stereotaxic space.

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Fig. 6. Probability map on coronal sections of the LiS and LuS. The probability maps of the sulci are superimposed on the average brain of the MNI (Evans et al., 1992) and the coordinates provided are within the MNI standard proportional stereotaxic space.

cus, i.e. on the BCS, the striate cortex extends on both banks of the calcarine sulcus (e.g. Bolton, 1900; Elliot Smith, 1904a; Brodmann, 1909; Antoni, 1914; Economo and Koskinas, 1925). Further caudally, the striate cortex extends outside the calcarine sulcus almost reaching the occipital pole. According to Elliot Smith (1904a,b), in about 70% of the brains, the striate cortex extends around the occipital pole to reach the lateral surface of the occipital region and is limited, more or less, by the LuS. Note that unlike the brain of the macaque monkey where the LuS is always the border of area V1 with area

V2, the striate cortex in the lateral part of the human occipital pole may be close to the LuS (as in the macaque monkey) or it may stay behind it (e.g. Elliot Smith, 1904a). In other words, area V2 which in the monkey lies always within the posterior bank of the LuS may spread outside the posterior bank of the LuS onto the occipital pole. In a recent study, Amunts and colleagues (2000) examined 10 human brains in order to investigate the relation of the striate cortex (Brodmann’s area 17) to the calcarine sulcus. The authors reported that, in all cases, area 17 (i.e.

Fig. 7. Probability map on coronal sections of the TOS. The probability maps of the sulci are superimposed on the average brain of the MNI (Evans et al., 1992) and the coordinates provided are within the MNI standard proportional stereotaxic space.

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Fig. 8. Probability map on horizontal sections of the POF, RCS (retro-calcarine sulcus) and LOS. The probability maps of the sulci are superimposed on the average brain of the MNI (Evans et al., 1992) and the coordinates provided are within the MNI standard proportional stereotaxic space.

Fig. 9. Probability map on horizontal sections of the BCS and IOS. The probability maps of the sulci are superimposed on the average brain of the MNI (Evans et al., 1992) and the coordinates provided are within the MNI standard proportional stereotaxic space.

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Fig. 10. Probability map on horizontal sections of the ACS, ISGS and TO. The probability maps of the sulci are superimposed on the average brain of the MNI (Evans et al., 1992) and the coordinates provided are within the MNI standard proportional stereotaxic space.

Fig. 11. Probability map on horizontal sections of the SSGS and PCS. The probability maps of the sulci are superimposed on the average brain of the MNI (Evans et al., 1992) and the coordinates provided are within the MNI standard proportional stereotaxic space.

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Fig. 12. Probability map on horizontal sections of the LiS and LuS. The probability maps of the sulci are superimposed on the average brain of the MNI (Evans et al., 1992) and the coordinates provided are within the MNI standard proportional stereotaxic space.

V1) was located mainly in the depth of the calcarine sulcus, extending onto the free surface in the most caudal sections, and area 18 (V2) surrounded area 17 dorsally and ventrally. In order to localize the boundary between V1 and V2, Clarke and Miklossy (1990) studied the location of callosal connections in the human occipital cortex. These investigators showed that area 17 (V1) occupies both banks of the calcarine sulcus and posteriorly (i.e. toward the occipital pole) extends onto both lips of the calcarine sulcus. The boundary of area 17 (V1) and area 18 (V2) extends in an antero-posterior direction close to the SSGS, dorsally, and the LiS ventrally. In addition, below the LiS and still on the lingual gyrus, the ventral part of area V3 (also known as VP) can be established on the basis of callosal connections (Clarke and Miklossy, 1990). The primary visual cortical area (V1) that is found along the calcarine sulcus in human brains has also been identified by several functional neuroimaging studies (e.g. Sereno et al., 1995; DeYoe et al., 1996; Tootell

et al., 1997; Hadjikhani et al., 1998). These studies showed that, proceeding dorsally within the cuneus, strips of cortex running in an anteroposterior direction along the calcarine sulcus can be identified as the dorsal part of V2, V3 and V3A (accessory V3) (Sereno et al., 1995; DeYoe et al., 1996; Tootell et al., 1997; Hadjikhani et al., 1998). All these strips extend beyond the cuneus onto the superior–lateral surface of the occipital lobe. The most dorsal area, V3A, runs along the TOS on the superior–lateral surface of the occipital lobe (Tootell et al., 1997). Recently, Pitzalis and co-authors (2006) have shown that, in the dorsalmost part of the parieto-occipital sulcus of the human brain, the contralateral visual hemifield could be mapped anterior and medial to areas V2, V3 and V3A. It has been suggested that this newly mapped area may be the human homologue of macaque area V6 (Galletti et al., 1996, 1999). Within the lingual gyrus, below the calcarine sulcus, a series of anteroposterior strips of cortex have been

Fig. 13. Probability map on horizontal sections of the TOS. The probability maps of the sulci are superimposed on the average brain of the MNI (Evans et al., 1992) and the coordinates provided are within the MNI standard proportional stereotaxic space.

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linked with the ventral part of V2 and V3 (the latter is also known as VP) (Sereno et al., 1995; DeYoe et al., 1996; Tootell et al., 1997; Hadjikhani et al., 1998). The identification of areas that lie further ventrally, however, has generated considerable debate. Initially, a visual area related to the processing of color was identified close to the collateral sulcus and extending lateral to it on the fusiform gyrus (Lueck et al., 1989; Zeki et al., 1991). This color-related area was interpreted as the homologue of macaque monkey area V4 (Zeki et al., 1991), but others have argued that it may not be area V4, but rather a separate area that was referred to as area V8 (Hadjikhani et al., 1998). Some neuroimaging studies have located the ventral part of area V4 (V4v) immediately after ventral area V3 and medial to the color area, which was originally found on the fusiform gyrus (Sereno et al., 1995; DeYoe et al., 1996; Tootell et al., 1997; Hadjikhani et al., 1998). Recently, Brewer et al. (2005) re-examined the organization of the visual areas on the ventral occipital region and demonstrated the existence of a hemifield map (V4) adjacent and anterior to the ventral portion of area V3. In addition, these investigators demonstrated two new hemifield maps, anterior to ventral V4, that were named areas VO-1 and VO-2. All three areas responded well to color stimulation, but VO-1 and VO-2 (but not area V4) responded preferentially to objects compared with faces. Recall that area V3A (i.e. area V3 accessory) which in the monkey lies in the dorsal prestriate region between areas V3 and V4 (Van Essen and Zeki, 1978; Zeki, 1978b), has been identified in the human brain in the dorsal prestriate region along the TOS (Tootell et al., 1997), i.e. just posterior to the location of dorsal area V4 on the dorsal part of the LOS (Tootell and Hadjikhani, 2001). If these interpretations are correct, then the superior lateral occipital cortex that lies above the LOS includes the dorsal parts of areas V2, V3 and V4 and the complete contralateral representation of area V3A. This would make this region of the human occipital cortex comparable to the cortex that is hidden in the LuS and extends onto the prelunate gyrus in the macaque monkey where areas V2, V3, V3A and V4 can be found. The ventral parts of areas V2, V3 (VP) lie on the lingual gyrus. Anterior to the TOS lies the anterior occipital sulcus, which has also been referred to as the posterior ascending branch of the second temporal sulcus (Eberstaller, 1890; Economo and Koskinas, 1925) or the posterior ascending branch of the inferior temporal sulcus (Cunningham, 1892; Watson et al., 1993). Functional neuroimaging studies (Zeki et al., 1991; Watson et al., 1993; Dumoulin et al., 2000) suggested that the cortical region close to the point of intersection of the anterior occipital sulcus and the LOS is the locus of the human homologue of the visual cortical motion area demonstrated in the rhesus monkey by Zeki (1974) and named V5, and in the owl monkey by Allman and Kaas (1971) and named MT. In a recent study, Malikovic and co-authors (2007) have shown a distinct architectonic area in this region of the cortex that is located most often in the depth of the

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sulci, i.e. the posterior bank of the anterior occipital sulcus and the ventral bank of the LOS. These investigators consider this distinct architectonic area as the putative human visual motion area, i.e. the homologue of monkey V5/MT. The use of retinotopic mapping techniques during functional MRI have begun demonstrating the visual areas of the occipital region of the human brain. Hasnain et al. (2001) have examined the quantitatively the value of sulcal landmarks for predicting functional areas in relation to some occipital sulci and found a number of significant spatial covariances. Further studies should combine the use of these techniques with more precise localization of the occipital sulci provided in the present study in order to clarify the relation between occipital sulcal patterns and functional visual areas. Acknowledgments—This study was supported by Canadian Institute of Health Research (CIHR), grant number MOR 14620. G.I. is supported by the Michael Smith Foundation for Health Research (MSFHR) and Alzheimer Society of Canada (ASC).

REFERENCES Allman JM, Kaas JH (1971) A representation of the visual field in the caudal third of the middle temporal gyrus of the owl monkey (Aotus trivirgatus). Brain Res 31:85–105. Amunts K, Malikovic A, Mohlberg H, Schormann T, Zilles K (2000) Brodmann’s areas 17 and 18 brought into stereotaxic space: Where and how variable? Neuroimage 11:66 – 84. Anderson SJ, Holliday IE, Singh KD, Harding GF (1996) Localization and functional analysis of human cortical area V5 using magnetoencephalography. Proc Biol Sci 263:423– 431. Antoni NRE (1914) Ausbreitung und Flächenbeziehungen der Area striata im menschlichen Gehirn. Folia Neurobiol 8:265–279. Barton JJ, Simpson T, Kiriakopoulos E, Stewart C, Crawley A, Guthrie B, Wood M, Mikulis D (1996) Functional MRI of lateral occipitotemporal cortex during pursuit and motion perception. Ann Neurol 40:387–398. Bense S, Janusch B, Schlindwein P, Bauermann T, Vucurevic G, Brandt T, Stoeter P, Dieterich M (2006) Direction-dependent visual cortex activation during horizontal optokinetic stimulation (fMRI study). Hum Brain Mapp 27:296 –305. Brewer AA, Liu J, Wade AR, Wandell BA (2005) Visual field maps and stimulus selectively in human ventral occipital cortex. Nat Neurosi 8(8):1102–1109. Bolton JS (1900) The exact histological localization of the visual area of the human cerebral cortex. Phil Trans R Soc Lond B 193: 165–222. Brodmann K (1909) Vergleichende Lokalisationslehre der Grosshirnrinde in ihren Prinzipien dargestellt auf Grund des Zellenbaues. Leipzig: Barth. Carpenter MB (1996) Core text of neuroanatomy. New York: Williams & Wilkins. Clarke S, Miklossy J (1990) Occipital cortex in man: Organization of callosal connection, related myelo- and cytoarchitecture, and putative boundaries of functional visual areas. J Comp Neurol 298:188 –214. Collins DL, Neelin P, Peters TM, Evans AC (1994) Automatic 3D intersubject registration of MR volumetric data in standardized Talairach space. J Comp Assist Tomogr 18:192–205. Cunningham DJ (1892) Contribution to the surface anatomy of the cerebral hemispheres. Academy House, Dublin. de Jong BM, Shipp S, Skidmore B, Frackowiak RS, Zeki S (1994) The cerebral activity related to the visual perception of forward motion in depth. Brain 117:1039 –1054.

184

G. Iaria et al. / Neuroscience 151 (2008) 174 –185

DeYoe EA, Carman GJ, Bandettini P, Glickman S, Wieser J, Cox R, Miller D, Neitz J (1996) Mapping striate and extrastriate visual areas in human cerebral cortex. Proc Natl Acad Sci U S A 9:2382–2386. Dougherty RF, Koch VM, Brewer AA, Fischer B, Modersitzki J, Wandell BA (2003) Visual field representations and locations of visual areas V1/2/3 in human visual cortex. J Vis 3:586 –598. Dumoulin SO, Bittar RG, Kabani NJ, Baker CL Jr, Le Goualher G, Pike GB, Evans AC (2000) A new anatomical landmark for reliable identification of human area V5/MT: a quantitative analysis of sulcal patterning. Cereb Cortex 10:454 – 463. Dupont P, Orban GA, De Bruyn B, Verbruggen A, Mortelmans L (1994) Many areas in the human brain respond to visual motion. J Neurophysiol 72:1420 –1424. Duvernoy H (1991) The human brain: surface, three-dimensional sectional anatomy and MRI. Wien: Springer-Verlag. Eberstaller O (1890) Das Stirnhirn. Ein Beitrag zur Anatomie der Oberflache des Grosshirns. Wien: Urban and Schwarzenberg. Economo C, Koskinas GN (1925) Die Cytoarchitektonik der Hirnrinde des erwachsenen Menschen. Vienna: Springer. Elliot Smith G (1904a) Studies in the morphology of the human brain with special reference to that of the Egyptians. No. I: The occipital region. Rec Egyptian Government School Med 2:123–173. Elliot Smith G (1904b) The morphology of the occipital region of the cerebral hemisphere in man and the apes. Anat Anz 24:436 – 451. Engel SA, Glover GH, Wandell BA (1997) Retinotopic organization in human visual cortex and the spatial precision of functional MRI. Cereb Cortex 7:181–192. Evans AC, Collins DL, Milner B (1992) An MRI-based stereotactic brain atlas from 300 young normal subjects. Proceedings of the 22nd Annual Symposium of the Society for Neuroscience. Anaheim, CA, 408. Felleman DJ, Van Essen DC (1991) Distributed hierarchical processing in the primate cerebral cortex. Cereb Cortex 1:1– 47. Galletti C, Fattori P, Battaglini PP, Shipp S, Zeki S (1996) Functional demarcation of a border between areas V6 and V6A in the superior parietal gyrus of the macaque monkey. Eur J Neurosci 8:30 –52. Galletti C, Fattori P, Gamberini M, Kutz DF (1999) The cortical visual area V6: Brain location and visual topography. Eur J Neurosci 11:575–582. Hadjikhani N, Liu AK, Dale AM, Cavanagh P, Tootell RBH (1998) Retinotopy and color sensitivity in human visual cortical area V8. Nat Neurosci 1:235–241. Hasnain MK, Fox PT, Woldorff MG (1998) Intersubject variability of functional areas in the human visual cortex. Hum Brain Mapp 6:301–315. Hasnain MK, Fox PT, Woldorff MG (2001) Structure-function spatial covariance in the human visual cortex. Cereb Cortex 11(8): 702–716. Iaria G, Petrides M (2007) Occipital sulci of the human brain: Variability and probability maps. J Comp Neurol 501(2):243–259. Itoh K, Fujii Y, Kwee IL, Nakada T (2005) MT⫹/V5 activation without conscious motion perception: a high-field fMRI study. Magn Reson Med Sci 4:69 –74. Kaas JH (2004) Early visual areas: V1, V2, V3, DM, DL, and MT. In: The primate visual system (Kaas JH, Collins CE, eds), pp 139 – 159. Boca Raton: CRC Press. Kollokian V (1996) Performance analysis of automatic techniques for tissue classification in magnetic resonance images of the human brain. MS thesis, Computer Science, Concordia University, Montreal, Canada. Lueck CJ, Zeki S, Friston KJ, Deiber MP, Cope P, Cunningham VJ, Lammertsma AA, Kennard C, Frackowiack RS (1989) The colour centre in the cerebral cortex of man. Nature 340: 386 –389. MacDonald D (1996) Program for display and segmentation of surfaces and volumes. Montreal, Quebec: McConnell Brain Imaging Center, Montreal Neurological Institute. Software available from http://www.bic.mni.mcgill.ca.

Malikovic A, Amunts K, Schleicher A, Mohlberg H, Eickhoff SB, Wilms M, Palomero-Gallagher N, Armstrong E, Zilles K (2007) Cytoarchitectonic analysis of the human extrastriate cortex in the region of V5/MT⫹: A probabilistic, stereotaxic map of area hOc5. Cereb Cortex 17:562–574. Mazziotta JC, Toga AW, Evans A, Fox PT, Lancaster J (1995a) A probabilistic atlas of the human brain: Theory and rationale for its development. Neuroimage 2:89 –101. Mazziotta JC, Toga AW, Evans A, Fox PT, Lancaster JL (1995b) Digital brain atlases. Trend Neurosci 18:210 –211. Ono M, Kubik S, Abernathey CD (1990) Atlas of the cerebral sulci. Stuttgart: Thieme. Nolte J (2002) The human brain: An introduction to its functional anatomy. New York: Mosby. Pitzalis S, Galletti C, Huang RS, Patria F, Committeri G, Galati G, Fattori P, Sereno MI (2006) Wide-field retinotopy defines human cortical visual area V6. J Neurosci 26:7962–7973. Robbins S, Whitesides S, Evans AC (2004) Localization volume: A new measure for capturing neuroanatomical variability. 10th International Conference on Functional Mapping of the Human Brain. Rucklidge W (1996) Efficient visual recognition using the Hausdorff distance. Lecture notes in computer science Vol. 1173. Springer. Sack AT, Kohler A, Linden DE, Goebel R, Muckli L (2006) The temporal characteristics of motion processing in hMT/V5⫹: combining fMRI and neuronavigated TMS. Neuroimage 29:1326 –1335. Sereno MI, McDonald CT, Allman JM (1994) Analysis of retinotopic maps in extrastriate cortex. Cereb Cortex 4:601– 620. Sereno MI, Dale AM, Reppas JB, Kwong KK, Belliveau JW, Brady TJ, Rosen BR, Tootell RB (1995) Borders of multiple visual areas in humans revealed by functional magnetic resonance imaging. Science 268:889 – 893. Sereno MI, Tootell RBH (2005) From monkeys to humans: what do we now know about brain homologies? Curr Opin Neurobiol 15:135–144. Shipp S, Watson JDG, Frackowiak RSV, Zeki S (1995) Retinotopic maps in human prestriate visual cortex: the demarcation of areas V2 and V3. Neuroimage 2:125–132. Shulman GL, Schwarz J, Miezin FM, Petersen SE (1998) Effect of motion contrast on human cortical responses to moving stimuli. J Neurophysiol 79:2794 –2803. Stiers P, Peeters R, Lagae L, Van Hecke P, Sunaert S (2006) Mapping multiple visual areas in the human brain with a short fMRI sequence. Neuroimage 29:74 – 89. Talairach J, Tournoux P (1988) Co-planar stereotaxic atlas of the human brain. New York: Thieme. Tootell RBH, Dale AM, Mendola JD, Reppas JB, Sereno MI (1996) fMRI analysis of human visual cortical area V3A. Neuroimage 3: S358. Tootell RBH, Hadjikhani N (2001) Where is “dorsal V4” in human visual cortex? Retinotopic, topographic and functional evidence. Cereb Cortex 11:298–311. Tootell RBH, Mendola JD, Hadjikhani NK, Ledden PJ, Liu AK, Reppas JB, Sereno MI, Dale AM (1997) Functional analysis of V3A and related areas in human visual cortex. J Neurosci 17:7060 –7078. Vallines I, Greenlee MW (2006) Saccadic suppression of retinotopically localized blood oxygen level-dependent responses in human primary visual area V1. J Neurosci 26:5965–5969. Van Essen DC, Zeki SM (1978) The topographic organization of rhesus monkey prestriate cortex. J Physiol (Lond) 277:193– 226. Walters NB, Egan GF, Kril JJ, Kean M, Waley P, Jenkinson M, Watson JD (2003) In vivo identification of human cortical areas using high-resolution MRI: an approach to cerebral structure-function correlation. Proc Natl Acad Sci U S A 100:2981–2986. Watson JD, Myers R, Frackowiak RS, Hajnal JV, Woods RP, Mazziotta JC, Shipp S, Zeki S (1993) Area V5 of the human brain: evidence from a combined study using positron emission

G. Iaria et al. / Neuroscience 151 (2008) 174 –185 tomography and magnetic resonance imaging. Cereb Cortex 3:79 –94. Zeki S, Watson JDG, Lueck CJ, Friston KJ, Kennard C, Frackowiak RSJ (1991) A direct demonstration of functional specialization in human visual cortex. J Neurosci 11:641– 649. Zeki SM (1969) Representation of central visual fields in prestriate cortex of the monkey. Brain Res 34:19 –35.

185

Zeki S (1974) Functional organization of a visual area in the posterior bank of the superior temporal sulcus of the rhesus monkey. J Physiol 236:549 –573. Zeki SM (1978a) Functional specialization of the visual cortex of the rhesus monkey. Nature 274:423– 428. Zeki SM (1978b) The third visual complex of rhesus monkey prestriate cortex. J Physiol (Lond) 277:245–272.

(Accepted 4 October 2007) (Available online 28 November 2007)