Helmuth Steinmetz 1

Gunter FOrst2

Hans-Joachim Freund1

Received March 12, 1990; revision requested June 5, 1990; revision received July 2, 1990; ac­cepted July 4, 1990.

This work was supported by grants from the Deutsche Forschungsgemeinschaft (SFB 200fZ2).

' Department of Neurology, Heinrich-Heine-Uni­versity, Moorenstr. 5, D-4000 Dusseldorf, F.R.G. Address reprint requests to H. Steinmetz.

2 Department of Diagnostic Radiology, Heinrich­Heine-University, D-4000 Dusseldorf, F.R.G.

0195-6108/90/1106-11 23 © American Society of Neuroradiology

Variation of Perisylvian and Calcarine Anatomic Landmarks Within .Stereotaxic Proportional Coordinates

1123

This investigation describes the variability in location of functionally important peri­sylvian landmarks and of the calcarine sulcus within the Talairach stereotaxic grid, a system frequently used for cortical localization in functional images. Twenty healthy volunteers (40 hemispheres) had MR imaging under stereotaxic conditions. Outlines of the following structures were directly identified on sagittal 5-mm MR sections and marked on individual proportional grid overlays: inferior central sulcus, inferior precentral sulcus, inferior postcentral sulcus, anterior ascending ramus and posterior rami of the sylvian fissure, superior temporal sulcus, and calcarine sulcus. Maximal variation zones for these landmarks were defined by superimposition of the standardized individual data on a standard stereotaxic grid. The sulcal variation zones measured 1.5-2.0 em.

The findings indicate that macroanatomic individuality in the cerebral surface cannot be accounted for adequately by proportional coordinates, and that this method does not allow precise definition of anatomically based regions of interest for functional imaging. Instead, MR mapping of the individual sulcus pattern should be used to generate brain templates.

AJNR 11:1123-1130, November/December 1990

The current revival of stereotaxic brain imaging reflects the need for a precise topographic analysis of structural and functional image data. The Talairach ster­eotaxic proportional grid was originally developed for pneumoencephalography [1] and has received renewed attention since the discovery that MR can provide noninvasive application [2-5]. The anatomic atlas of Talairach et al. [1] is based on this grid system and has recently been used by several investigators for interpretation of CT [6] , MR [3, 4], and positron emission tomography (PET) [7-16]. This interest prompted the publication of a new brain atlas by Talairach and Tournoux [17], which , according to the preface, was "derived from one particular [postmortem] brain, applicable to all other brains under examination ." Drawings of contiguous frontal , coronal, and sagittal sections of this "brain of reference" were displayed with the corresponding grid overlays. Unlike the original work of Talairach et al. [1], interindividual variability of cortical structures was not assessed quanti­tatively in the new atlas. The problem of morphologic individuality, however, is relevant for any atlas-based interpretation of image data. Variability of functionally important perisylvian landmarks (Figs. 1 and 2) and of the calcarine sulcus within the Talairach proportional grid is described in this article, which continues a previous study on the variation of superior hemispheric sulci and of the sylvian fissure [5] . On the basis of the results, the suitability of the proportional grid for image analysis is discussed.

Subjects and Methods

Forty cerebral hemispheres were evaluated in 20 healthy volunteers comprising eight women and 12 men 22-63 years old . Nineteen probands considered themselves right-

1124 STEINMETZ ET AL. AJNR :11 , November/December 1990

Fig. 1.-Standard sulcal arrangement of lateral hemispheric aspect. See key for abbreviations. (Rendering adapted from Brodmann (18].)

10 •

Fig. 2.-Base planes of proportional grid as applied to left (L) and right (R) hemispheres of two different-sized adult brains show consistent loca­tion of sulcus centra lis within reference system. See key for abbreviations. Locations of precentral sulcus (open arrows) and superior temporal sulcus (solid arrows) show perisylvian variability, even within proportional frame. Both sulci are classical landmarks of functionally important regions (pre­central sulcus is posterior border of Broca's area and superior temporal sulcus is inferior border of Wernicke's area). Anterior ascending ramus is the sulcus anterior to the precentral sulcus in both hemispheres. (Reprinted with permission from Talairach and Tournoux [17).)

Key to Abbreviations Used in Figures

AAR AGPG

AHR GaGp GALGS GS IFS IPS MS

PAR PDR

PHR POGS PRGS SF STS VAG

Vca Vcp VPG

anterior ascending ramus of sylvian fissure bicommissural plane that runs tangent to up­

per margin of anterior commissure and to lower margin of posterior commissure

anterior horizontal ramus of sylvian fissure same as AGPG calcarine sulcus central sulcus inferior frontal sulcus intraparietal sulcus marginal sulcus (terminal ascending ramus

of cingulate sulcus) posterior ascending ramus of sylvian fissure posterior descending ramus of sylvian fis-

sure posterior horizontal ramus of sylvian fissure postcentral sulcus precentral sulcus sylvian fissure superior temporal sulcus plane perpendicular to bicommissural plane

and to midsagittal plane and tangent to posterior margin of anterior commissure

same as VAG same as VPG plane perpendicular to bicommissural plane

and to midsagittal plane and tangent to anterior margin of posterior commissure

handed. Methodologic principles of the proportional grid system were described in a previous study of 15 probands [5) who were also included in this investigation. Following orthomorphic alignment of the brain (Fig. 3A), sagittal T1-weighted spin-echo (SE) images (Figs. 3B-3F) were obtained from the whole brain with the use of a 0.35-T superconductive magnet. The technical factors were 500/40/4 (TR/ TEfexcitations), 256 x 256 image matrix, and 5-mm-thick contiguous slices. For each of the 40 hemispheres an individual proportional grid was constructed on a transparent overlay on the sagittal images (Figs. 3B-3F). Identical orientation of the overlay on images not in the midplane was facilitated by the scanner's millimetric grid on the images serving as a fixed ·:external" reference (the grid is not dis­played in Figs. 3B-3F). Image distortions within the field of interest were excluded, as also described previously [5). For the current study the following sulci were identified directly on each hemisphere and their course was marked on the overlay (see below for anatomic criteria): inferior central sulcus , inferior precentral sulcus, inferior postcentral sulcus , anterior ascending sylvian ramus , posterior hori­zontal sylvian ramus, posterior ascending sylvian ramus, and hori­zontal segment of the superior temporal sulcus (see Fig . 1 for "standard" perisylvian topography). The calcarine sulcus was outlined on the medial hemispheric surface. The callosal sulcus was deter­mined on the midsagittal section. Except for the callosal sulcus all sulci were evaluated separately for left and right hemispheres.

Inferior Central, Precentral, and Postcentral Sulci

The inferior central and pre- and postcentral sulci were identified directly by using the following procedure [19) : The central sulcus was

AJNR:11, November/December 1990 STEREOTAXY OF CORTICAL LANDMARKS 1125

identified at the superior hemispheric margin, where it is constantly found as the next sulcus anterior to the marginal sulcus (5 , 19-21]. From there, the central sulcus takes an unbroken course (21 , 22] toward its inferior end. By using a real-time cinematographic display mode on an off-line image-processing workstation (Mipron, Kontron Bildanalyse, Eching, F.R.G.), we traced the bottom of the central sulcus progressing from medial to lateral MR slices. The course of the inferior central sulcus on the external hemispheric surface as determined from the two or three most lateral sagittal images of each hemipshere was marked on the individual grid overlay. The next sulci running anterior and posterior to the inferior central sulcus were identified and marked as the inferior pre- and postcentral sulci, respectively (Figs. 3C-3E).

Anterior Ascending, Posterior Horizontal, and Posterior Ascending Sylvian Rami and Superior Temporal Sulcus

The sylvian fissure is classically divided into five segments [21 , 23] . These are the main horizontal stem (posterior horizontal ramus) and two anterior (anterior ascending and anterior horizontal rami) and two posterior (posterior ascending and posterior descend­ing rami) branches (see Fig . 1 ). The anterior and posterior ascending rami constitute functionally important landmarks. The anterior as­cending ramus divides the posterior inferior frontal gyrus into the pars opercularis (between precentral sulcus and anterior ascending ramus) and pars triangularis (between anterior horizontal ramus and anterior ascending ramus). The anterior ascending ramus is thus centered in the anterior speech area on the dominant hemisphere. The posterior ascending ramus cuts into the supramarginal gyrus, which is part of the inferior parietal lobule (and posterior speech region). The anterior ascending ramus was directly identified with MR by using the follow­ing criteria (19]. The anterior ascending ramus originates in the depth of the insular cistern , where it is continuous with the so-called circular (periinsular) sulcus. From there, the anterior ascending ramus was traced laterally on the 5-mm sagittal MR sections by using the aforementioned fast display mode. The anterior ascending ramus cuts through the whole depth of the frontal operculum and thus can be discerned from other anterior perisylvian sulci. The posterior ascending ramus was identified as the terminal , upswinging portion of the posterior sylvian fissure (Fig . 1 ). The posterior horizontal ramus was outlined between the points of origin of the anterior and posterior ascending rami. The superior temporal sulcus was identified as the next sulcus running inferior and parallel to the posterior horizontal ramus (Figs. 3D-3F).

Calcarine and Callosal Sulci

The calcarine sulcus is centered in the striate cortex (18, 24] and originates about 2 em posterior to the splenium of the corpus cal­losum from a common stem with the inferior parietooccipital sulcus [20, 23]. From there, the calcarine sulcus takes a slightly curved course toward the occipital pole. It has a sulcal depth of 14-20 mm [20, 25]. Accordingly, the calcarine sulcus was identified and marked on immediate paramedian MR sections (Fig. 3C). The callosal sulcus was determined as the outer r:nargin of the corpus callosum on the midsagittal image.

Standardization Procedure

All sulcal markings on the individual overlays referred to midpoints between opposed gyral lips at the external hemispheric surface. To obtain statistical graphic summations of the individual data, all over­lays were magnified proportionally and projected stepwise, rectangle by rectangle, on a standard grid (Figs. 4-7).

Results

Inferior Central, Precentral, and Postcentral Sulci

The variation zones of the right and left inferior central and pre- and postcentral sulci measured between 1.5 and 2 em in the anteroposterior axis (Figs. 4 and 5). As gyral widths were of the same order, only minimal overlap occurred be­tween the sulcal zones. The location and variation of the inferior central sulci corresponded to that derived by Talairach et al. [1] from their study of 20 postmortem hemispheres. No clear left-right asymmetries were seen for the central or precentral sulcus. The inferior postcentral sulcus was more variable and tended to be located farther posteriorly on the left than contralaterally (Fig. 5). The inferior pre- and postcen­tral sulci had not been investigated by Talairach et al. [1 ].

Sylvian Rami and Superior Temporal Sulcus

The vertical variation of the posterior horizontal ramus and superior temporal sulcus and the anteroposterior variation of the anterior and posterior ascending rami also ranged be­tween 1.5 and 2 em (Figs. 4 and 6). The variation zone of the posterior horizontal ramus extended more posteriorly in the left than in the right hemispheres, thus producing a larger left parietal operculum in the majority of cases. The latter finding agrees with several anatomic reports [21, 23, 26-31 ]. Also, distribution of the posterior end points of the posterior hori­zontal ramus was more scattered on the left than contralat­erally, so that the location of the posterior ascending ramus was more variable among left hemipsheres (Fig . 6). No left­right asymmetries were observed for the anterior ascending ramus and superior temporal sulcus.

In six right hemispheres, a direct transition of the posterior ascending ramus into the inferior postcentral sulcus was seen , which explains the considerable overlap between these vari­ation zones (compare Figs. 5A and 6A). In five left hemi­spheres, a posterior ascending ramus could not be identified, which explains the posterior extension of the posterior hori­zontal ramus zone beyond that of the posterior ascending ramus in Figure 68.

Calcarine Sulcus

The variation zone of the calcarine sulcus measured almost 2 em in the vertical axis {Fig. 7). It corresponded exactly to that indicated by Talairach et al. [1] in their pneumoenceph­alographic study of 30 hemispheres. There were no left-right asymmetries.

Discussion

The distinction between direct and indirect techniques of cerebral localization is fundamental to brain stereotaxy [1 , 17]. Direct localization means recognition of characteristic cerebral landmarks. Indirect localization, such as with the proportional grid, relies on coordinate systems constructed in reference to (directly identified) landmarks. Errors are inherent in any indirect method owing to interindividual variability of the spatial relation between targets and references. Direct

1126 STEINMETZ ET AL. AJNR:11 , November/December 1990

A

D E F

AJNA :11 , November/December 1990 STEREOTAXY OF CORTICAL LANDMARKS 1127

identification is therefore preferable, but until now has re­mained restricted to only a few morphologically unique struc­tures.

Our evaluation of the (indirect) proportional grid system using techniques of direct sulcus mapping revealed variation zones for all major sulci of 1 .5-2 em measured on the external brain surface (Figs. 4-7). Similar spatial variability must be assumed for deeply located parts of the sulci . The inaccuracy of the proportional grid system was the same in the antero­posterior and vertical axes and increased with the distance between the target and the inner reference points of the anterior and posterior commissures. Variation of the callosal sulcus (Fig. 7), for example, was about half that of the central sulcus, posterior horizontal ramus, or calcarine sulcus, which corresponds to about double the distance of the latter sulci to the anterior or posterior commissure. Significant overlap­ping between variation zones was observed only for the posterior suprasylvian landmarks. The sulcal zones may therefore provide a guide for the identification of individual sulci visible on high-resolution images. Structural regions of interest based on proportional coordinates, however, would be unreliable for an anatomically based data analysis. The individual sulcus pattern was too unpredictable to allow focal distinctions between, for instance, precentral or postcentral, supra- or infrasylvian, and parietal opercular or angular loca­tions by means of Talairach atlas coordinates (see Figs. 4-7). In fact, variability of the central sulcus or posterior hori­zontal ramus within the proportional grid was not less than within the standard system for electroencephalographic scalp electrode placement, which is based solely on the external cranial landmarks of the nasion, inion, and preauricular points [32).

These conclusions clearly depend on the ability to confi­dently identify the individual sulci with our MR technique. It is no problem to recognize the rami of the sylvian fissure or the superior temporal , calcarine, or callosal sulci on 5-mm sagittal sections. It is more difficult to outline the inferior extension of the central sulcus. The central sulcus was identified at the superior hemispheric margin, where it is always found imme­diately in front of the so-called marginal sulcus; that is, the terminal ascending ramus of the cingulate sulcus [5, 19, 21,

33). From there, the central sulcus was traced inferiorly by using a cinematographic image display mode [19]. Since the course of the central sulcus is unbroken through its entire length [21 , 22] , the procedure left no doubt among the authors that the sulcus named was actually the inferior central sulcus in each individual. Therefore, identification of the inferior pre­and postcentral sulci was self-evident. It should be noted that almost no overlap occurred between the variation zones of these three sulci (Figs. 4 and 5). Thus , if any false identifica­tions had occurred , the present investigation would have actually underestimated anatomic variability. Strong evidence against any misinterpretation of the suprasylvian sulcus pat­tern is provided by the original Talairach atlas (plate 154 of Talairach et al. [1 ]), which shows the same location and variation of the inferior central sulcus derived from 20 post­mortem hemispheres.

Several studies used the Talairach atlas [1) to correlate PET with anatomic structures [7 -1 6]. Fox et al. reported highly focal cerebral blood flow (CBF) responses of the pri­mary sensory cortices to cutaneous tacti le vibration [11) or retinal field stimulation [1 0, 12). The following anteroposterior and vertical mean coordinates and standard deviations were found for the primary somatosensory projection areas in eight healthy subjects [11) (positive values were superior to the estimated bicommissural line (ACPC) or anterior to the esti­mated midcommissuralline (MC) [11 ); MC would be equidis­tant to lines VAG and VPC in Figures 4-7 [11 ]):

1. Lip area, right hemisphere: MC, +0.2 ± 0.5 em (range, +1.2 to -0.4 em); ACPC, +2.7 ± 0.6 em.

2. Finger area, right hemisphere (digits 1-4): MC, -0.8 ± 0.6 em (range, +0.1 to -1.9 em); ACPC, +4.8 ± 0.3 em.

3. Toe area, midsagittal plane (digits 1 and 2, bilateral stimulation): MC, -1 .1 ± 1.1 em (range, +0.6 to -3.0 em); ACPC, +5.1 ± 0.4 em.

Location and width of the sensory lip area are compatible with the MR localization of the inferior postcentral gyrus (Figs. 4 and 5; it must be taken into account that the inferior central sulcus has a slightly oblique, anterolateral to posteromedial , depth orientation , which influences the location of the sensory CBF activation). Midsagittal CBF responses to toe vibration , however, were dislocated anteriorly by Fox et al. [11] com-

Fig. 3.-Stereotaxic MR evaluation of perisylvian and calcarine sulci. See key for abbreviations. A, Axial and coronal T1-weighted images (SE 500/30/1, 1-cm slice thickness) show orthomorphic position within field of view. 8-F, Sagittal T1-weighted images (SE 500/40/4, 5-mm slice thickness) with individually constructed proportional grid overlays at 0 (8), 5 (C), 45 (0),

50 (E), and 55 (F) mm from midsagittal plane. C, Direct identification of central (white curved arrow) and calcarine (black curved arrow) sulci. Marginal sulcus (straight arrow). D and E, Direct identification of anterior (white open arrows) and posterior (solid arrows) ascending rami. Bottom of central sulcus (black open arrows)

has been traced in 5-mm lateral steps from C. Sulci anterior and posterior to central sulcus are pre- and postcentral sulci. F, Image showing most lateral portion of posterior horizontal ramus of sylvian fissure (white open arrow) and superior temporal sulcus (black open

arrow). In this subject, perisylvia[l sulci were mapped in the following fashion: Portions of the central and pre- and postcentral sulci visible on E were drawn on the individual overlay. The upper ends of these outlines were connected with those points on D where the central and pre- and postcentral sulci open onto the external brain surface. Outlines of the anterior and posterior ascending rami were drawn as visible on E. Lateral-most portions of posterior horizontal ramus and superior temporal sulcus were drawn as visible on F and connected with their anterior and posterior continuations on E. This procedure gives a very close estimate of superficial course of sulci.

1128 STEINMETZ ET AL. AJNR:11 , November/December 1990

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B Fig. 4.-A and 8, Perisylvian variation of right (R) and left (L) central and superior temporal sulci as obtained from sagittal MR imaging in 20 probands.

See key for abbreviations. Shaded areas represent variation zones of posterior horizontal ramus of sylvian fissu re measured between points of origin of anterior and posterior ascending rami. Zones of variation of central sulcus, posterior horizontal ramus, and superior temporal sulcus measure 1.5-2 em. Note farther backward extension of zone of posterior horizontal ramus on left compared with right. Sulcal outlines at superior hemispheric convexity represent superomedial central sulcus as identified on immediate paramedian sections, serving as starting points from which course of central sulcus was traced laterally.

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A B Fig. 5.-A and 8, Perisylvian variation of right (R) and left (L) pre- and postcentral sulci as obtained by sagittal MR imaging in 20 probands. See key for

abbreviations. Shaded areas represent variation zones of posterior horizontal ramus of sylvian fissure. Variation zones of pre- and postcentral sulci measure 1.5-2 em. Outlines of postcentral sulcus on left are more scattered throughout their band of variation and tend to lie more posterior than those in right hemispheres.

pared with the MR localization of the bottom of the central sulcus at the medial hemispheric aspect, which in our study was found at an MC coordinate of -2.1 ± 0.6 em (range, -1 .2 to -3.4 em) (Fig . 4). The difference is statistically signif­icant (p < .05; t test). The sensory toe representations indicated by Fox et al. [11] extended up to 1.8 em anteriorly. The increased range of variation may be due to their technique of estimating the individual ACPC lines from the glabella-inion line on lateral skull radiographs [8, 9]. Variable tilts of the estimated ACPC line thus may have added to the inaccuracy of the proportional grid system. In the studies on the primary visual projection , Fox et al. [1 0, 12] applied checkerboard stimuli to restricted parts of the retina. The findings were summed up from six normal subjects and confirmed retino-

tropy on the medial occipital lobe. However, the reported coordinates of the CBF peak responses [1 0 , 12] differ from the MR location (Fig. 7) and from the Talairach atlas coordi­nates of the calcarine sulcus [1 , 17] , which harbors most of the striate cortex [18, 24]: Stimulation of the macula and perimacula, for instance, produced maximal midsagittal acti­vation below the estimated ACPC line: for macula, ACPC =

-0.50 em and MC = -6.86 em; for perimacula, ACPC =

-0.12 em and MC = -6.29 em; for retinal periphery, ACPC = +0.64 em and MC = -5.96 em. Mean values are from Table 2 of Fox et al. [12]. (Compare with Fig. 7 or with atlas plates [1 , 17].) Taken together, the findings of Fox et al. [1 0-12] suggest displacement of the CBF responses with respect to the primary sensory cortices in two directions: anterior shift

AJNR:11 , November/December 1990 STEREOT AXY OF CORTICAL LANDMARKS 1129

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in 20 probands. See key for abbreviations. Shaded areas represent variation zones of posterior horizontal ramus of sylvian fissure. Variation zones of anterior and posterior ascending rami measure 1.5-2 em. Zone of left posterior ascending ramus is broader and extends farther posteriorly than contralaterally, so that left parietal operculum is longer than its mate in most cases.

of the toe response and downward shift of the visual re­sponse, each on the order of 1 em. With our current MR material , we tested their method to estimate the ACPC line from the glabella-inion line [8). The estimated midcommissural point was found at 4.8 mm superior to 4.5 mm inferior (mean, 0.83 mm superior; SD = 2.49 mm) and at 1.5-7.3 mm posterior (mean, 4.06 mm posterior; SD = 1.36 mm) to the true midcommissural point (perpendicular measurements from the true ACPC and MC on midsagittal MR slices). The inclination of the estimated ACPC with respect to the true ACPC ranged from -4.0° to +11 .8° (-0.06 ± 3.64° ; positive values correspond to anterior elevation of the estimated ACPC). Nevertheless, this only partly explains the discrep­ancies between functional localization in the studies of Fox et al. [1 0-12] and direct anatomic localization.

Several groups proposed other methods to match PET with structural standard templates [34-42]. Of these, Bajcsy et al. [34] , Bohm et al. [35, 37 , 42] , and Dann et al. [41] described the computerized superimposition of digitized, transformable postmortem brain atlases on individual tomographic data. Brain surface and ventricles served as main reference struc­tures. These systems allow global transformations of scale, rotation , and translation in x, y, and z axes as well as elastic deformation of the atlas structures. They are superior to the proportional grid method [42]. However, they do not solve the principal problem of indirect localization ; that is, the com­parison of individual brains under study with one standard reference organ . Furthermore, changes of surface profile or ventricular contours cannot b~ excluded in postmortem atlas brains . Vice versa, structural abnormalities may be present in patients. These issues were also addressed by Herholz et al. [38] and Evans et al. [40] . In a comprehensive approach, Evans et al. [ 40] developed a standard region-of-interest (ROI) atlas derived from an in vivo MR data set. To account for morphologic variability , they used an interactive procedure to correct and redefine single standard ROis according to indi­vidual brain contours seen on MR, thus combining indirect with direct localization.

----f.-- ~

~ ~ /

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~ ~ \

I

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\ ~ ~\I \~

~~\

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Fig. 7.-Variations of calcarine and callosal sulci as obtained by MR imaging in 20 probands (pooled data from 40 hemispheres). See key for abbreviations. Variation zone of callosal sulcus measures less than 1 em. With increasing distance from center of reference system, sulcal variation zones become broader (compare Figs. 4-6 and calcarine with callosal sulcus).

Further improvement of direct localization will come from gradient-echo MR volume measurements yielding isotropic data matrices [43, 44). Direct MR identification and mapping of cortical landmarks will thus allow the generation of individ­ual brain templates and improved accuracy of structural ROI placement. Although computationally expensive and user­intensive, the intraindividual three-dimensional matching of such MR data with PET appears to provide the most reliable way for studies of structural-functional relationships in normal and abnormal conditions [45]. It also renders identical repo­sitioning unnecessary. Our group is currently validating an intermodal surface-fitting method similar to that described by Pelizzari et al. [46] .

1130 STEINMETZ ET AL. AJNR:11 , November/December 1990

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