1 McConnell Brain Imaging Centre, Montréal Neurological Institute, McGill University, Montréal, Canada, , 2 Utrecht University, Utrecht, The Netherlands and , 3 McGill Vision Research Unit, Department of Ophthalmology, McGill University, Montréal, Canada
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Abstract |
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Introduction |
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Functional specialization within the human visual cortex was demonstrated by Zeki et al. (Zeki et al., 1991), who used positron emission tomography (PET) to demarcate cortical areas V4 and V5 (or MT), which they implicated in the processing of color and motion information respectively. In a further PET study, Watson et al. more accurately defined the location of V5 on the ventrolateral occipital cortex, slightly posterior to the junction of the ascending limb of the inferior temporal sulcus (ALITS) and the lateral occipital sulcus (LO) (Watson et al., 1993
). Tootell et al. (Tootell et al., 1995
) studied V5 in humans with functional magnetic resonance imaging (fMRI), and described a similar location in the standard (stereotaxic) space of Talairach and Tournoux (Talairach and Tournoux, 1988
). However, they could not discern a consistent relationship between the region of V5 activation and the sulcal and gyral pattern in this region, except to observe that the activation was usually (but not always) buried within a shallow sulcus, as described by Watson et al. (Watson et al., 1993
).
The parieto-temporo-occipital cortex is one of the most extensively gyrified regions of the cerebral cortex (Zilles et al., 1988), and consequently a high percentage of its surface area is buried within sulci. In addition, the sulcal and gyral pattern in this region is highly variable, evidenced by numerous alternative descriptions and nomenclature systems over the past century, either in relationship with V5 (Watson et al., 1993
; Howard et al., 1995
; McCarthy et al. 1995
; Anderson et al., 1996
) or without (Talairach and Tournoux, 1988
; DeArmond et al., 1989
; Ono et al., 1990
; Carpenter, 1991
; Duvernoy 1991
; Nolte, 1999
).
Since a consistent location of V5 in stereotaxic (Talairach) space has been indicated by several previous studies (Zeki et al., 1991; Watson et al., 1993
; De Jong et al., 1994
; Dupont et al., 1994
; McCarthy et al., 1995
; Tootell et al., 1995
; Anderson et al., 1996
; Uusitalo et al., 1997
; Shulman et al., 1998
), the goal of this study was to describe precisely the location of V5 with respect to the sulcal pattern in the lateral parieto-temporo-occipital cortex, using a set of fully automated registration and sulci extraction techniques. The use of such anatomical methods should result in an improved description and more detailed quantification of this relationship. This study entailed choosing a visual stimulus to activate selectively area V5 with fMRI, and a careful examination and re-classification of the sulcal patterns and landmarks in this region.
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Materials and Methods |
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fMRI was performed in 15 normal subjects, 10 of whom showed significant activations [eight males, two females; one left handed, nine right handed; average age 31 years (range 2444 years)]. All subjects had normal or corrected to normal acuity. These studies were conducted with the subjects lying on their back with a surface-coil (circularly polarized, receive only) centered over their occipital poles. The visual stimuli were presented on a rear-projection screen placed at the end of the bore of the magnet, which was viewed by means of a mirror mounted above the eyes at an angle of ~45°. Head position was fixed by a foam headrest and either by the use of a bite-bar or by a combination of immobilizing hearing protectors and a bar pressing on the bridge of the subject's nose. These constraints reduced head motion and virtually eliminated cumulative head drift during the scanning session.
Multislice T2*-weighted gradient echo (GE) echo-planar imaging images (TR = 3.0 s, TE = 51 ms, flip angle = 90°) were acquired with a Siemens Magnetom Vision 1.5T MRI. A 128 x 128 acquisition matrix was acquired with a 300 x 300 mm rectangular field of view. For this study, 1012 contiguous 46 mm slices were obtained parallel to the calcarine sulcus, and care was taken to include the junction of the inferior temporal sulcus (ITS) and the ALITS. One hundred and twenty measurements (time frames) were acquired, giving a total scanning time of 6 min per dynamic scan. Baseline and activation conditions were alternated every 45 s, resulting in four activation periods and four baseline periods per dynamic scan. Two to four dynamic scans were performed in each session.
Anatomical MRI Scanning
T1-weighted anatomical MRI (aMRI) images were acquired with the surface-coil in place, prior to the commencement of the functional scans. Thus, if no head movement occurred, the anatomical and functional surface-coil MRI images were aligned. This aMRI utilized a 3-D GE sequence (TR = 22 ms, TE = 10 ms, flip angle 30°) and yielded ~80 256 x 256 sagittal images with a thickness of 2 mm. The signal intensity of a surface-coil aMRI decreases as a function of the distance from the coil. This intensity gradient interferes with most of the automatic algorithms used. Therefore, in all subjects, T1-weighted global MRI images were acquired with a head-coil (circularly polarized, transmit and receive), also using a 3-D GE sequence, yielding ~170 256 x 256 sagittal images comprising 1 mm3 voxels. The surface-coil aMRI was aligned with the head-coil scan, thereby allowing an alignment of the functional data with a head-coil aMRI. All studies were performed with the informed consent of the subjects and were approved by the Montreal Neurological Institute Research Ethics Committee.
Visual Stimulus
The visual stimulus was generated on a Macintosh Powerbook 160 using a modified program from the Video Toolbox (Pelli, 1997), and displayed with an LCD projector (NEC-MT). The visual display was 36 cm in both height and width, corresponding to 15° at a viewing distance of 135 cm. The activation condition consisted of random checkerboard patterns (see Fig. 1
), which were replaced by fresh random checkerboard patterns at a frequency of ~2 Hz, i.e. two checkerboard patterns per second. Each check of the checkerboard pattern subtended ~0.06°, and was randomly assigned a lighter (Lmax) or darker (Lmin) luminance value than the mean background luminance (435 cd/m2). The contrast, defined as (Lmax Lmin)/ (Lmax + Lmin), was 3%. The baseline condition comprised a stationary random checkerboard pattern, otherwise identical to that in the activation condition. A black fixation dot (0.3°) was affixed to the center of the visual display.
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Data Analysis
The images were analyzed on SGI workstations using purpose-built software developed in the Neuroimaging Laboratory at the Montreal Neurological Institute. The global aMRI scans were corrected for intensity non-uniformity (Sled et al., 1998) and automatically registered (Collins et al., 1994
) into a stereotaxic space (Talairach and Tournoux, 1988
) using a stereotaxic average model of 305 brains (Evans et al., 1992
). The surface-coil anatomical scans were aligned with the head-coil anatomical scans using an automated script combining correction for the intensity gradient (Sled et al., 1998
) and intra-subject registration (Collins et al., 1994
; Maes et al., 1997
). The functional data were blurred with a 3-D full-widthhalf-maximum (fwhm) filter of 6 mm to increase signal-to-noise by attenuating high frequency noise, and analyzed using a Spearman rank order statistical test for each voxel. The acquired t-statistic map was transformed into the standard Talairach space by combining the transformation files from the previous two steps. Only t-statistical maps with a group of adjacent voxels whose t-statistical values corresponded, after correcting for multiple comparisons, to P-statistical values smaller than 0.001 (t = 5.4) were included in this study. Using the P < 0.001 criterion, regions of activations were identified. The location of V5 has been correlated with the parieto-temporo-occipital cortex (Zeki et al., 1991
; Watson et al., 1993
; McCarthy et al., 1995
; Tootell et al., 1995
); therefore, the location of the voxel with the most significant t-statistical value in this region was taken to be V5. This identification process of V5 was similar to that used by Watson et al. (Watson et al., 1993
). Sulcal regions were identified using automated algorithms which extract the cortical surface (MacDonald et al., 1994
, 1998
) and then identify sulcal zones using curvature criteria (Le Goualher et al., 1996
, 1998
). Those in the region of interest were manually identified (Ono et al., 1990
), using a 3-D interactive display program (MacDonald, 1996
). The voxels with the t-statistical values above a certain threshold and all sulci were displayed on an extracted cortical surface (MacDonald et al., 1994
, 1998
). Cortical unfolding was then performed to aid the visualization of functional activation deep within the sulci (MacDonald, 1998
).
Identification of Sulci
The anatomical MRI images were initially examined in the sagittal plane for major sulci (Fig. 2). The Sylvian fissure and the superior temporal sulcus were identified, followed by the often discontinuous ITS, running parallel to the above-mentioned sulci. The posterior end of the ITS was traced to the formation of the ventrodorsally oriented sulcus, which has been previously referred to as the ALITS (Watson et al., 1993
). At this junction, the ITS usually extended horizontally into the occipital lobe, and when it did not reach the occipital pole we labeled it the posterior continuation of the ITS (PCITS). In cases where this horizontal sulcus reached the occipital pole it was termed the posterior continuation/ lateral occipital sulcus (PCITS/LO). Often there was a horizontal sulcus dorsal to the PCITS or PCITS/LO, which extended to the occipital pole, the LO (Ono et al., 1990
).
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Results |
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The acquired t-statistical map contained several t-statistical peaks. The P < 0.001 criterion usually revealed only one activation region in each hemisphere, situated in the general location where V5 (or MT) has been previously reported, i.e. the parietotemporo-occipital cortex (Zeki et al., 1991; Watson et al., 1993
; De Jong et al., 1994
; Dupont et al., 1994
; Cheng et al., 1995
; McCarthy et al., 1995
; Tootell et al., 1995
; Uusitalo et al., 1997
; Shulman et al., 1998
). For examples see Figures 4 and 5a
. In a few cases two activation points were found in the region of interest. These points, however, were always located within the same sulcus and could, based on the anatomical dimensions of V5 (Tootell and Taylor, 1995
), still arise from the same area. The criterion sometimes revealed more activation points. These, however, had lower peak t-statistical values and were never located within the parieto-temporo-occipital cortex.
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The average coordinates and standard deviations in stereotaxic Talairach space of V5 for the left hemisphere (x = 47 ± 3.8, y = 76 ± 4.9, z = 2 ± 2.7; n = 10) and for the right hemisphere (x = 44 ± 3.3, y = 67 ± 3.1, z = 0 ± 5.1; n = 9) were similar to the ones found by Watson et al. (Watson et al., 1993) (x = 41 ± 5.6, y = 69 ± 6.0, z = 2 ± 5.3 and x = 41 ± 3.7, y = 67 ± 4.7, z = 2 ± 3.2 for the left and right hemisphere respectively; n = 12) and Tootell et al. (Tootell et al., 1995
) (x = ± 45 ± 3.6, y = 76 ± 7.5, z = 3 ± 2.5; n = 6) [see also (Zeki et al., 1991
; De Jong et al., 1994
; Dupont et al., 1994
; McCarthy et al., 1995
; Uusitalo et al., 1997
; Shulman et al., 1998
)]. No significant differences between the activation foci in the left and right hemispheres was observed with respect to the peak t-statistical values or the total volumes of significant activation (P > 0.05).
The Sulcal Pattern
We found a fairly consistent sulcal pattern in the region of interest (the parieto-temporo-occipital cortex), enabling us to describe a generic model of the sulcal pattern (Fig. 3). Variations in this model are produced by the absence or presence of the LO, the PCITS and the PCITS/LO. In all cases (19 hemispheres) the posterior end of the ITS gave rise to a roughly ventrodorsally oriented sulcus, the ALITS. At this junction the ITS extended posteriorly in 89% (17/19) of the cases. This extension was in 47% (9/19) defined as the PCITS and in the remaining 42% (8/19) the PCITS/LO. The LO was identified in 69% (13/19). In 58% (11/19) the LO was located dorsal to the PCITS (37%) or PCITS/LO (21%) without a meeting point to either of the above-mentioned sulci. In the remaining 11% (2/19) the LO connected to the ALITS, in which case there was neither a PCITS nor a PCITS/LO.
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Relation of Area V5 to the Sulcal Pattern
In 95% of all cases, V5 was located within the depth of a sulcus. The one activation peak (5%) that was not located within a sulcus was positioned on the gyrus directly posterior to the ALITS. As shown in Figure 3, 53% of the activations were found in the ALITS, 11% in the ITS, and 26% in the PCITS and PCITS/LO (5% was located in the PCITS and 21% in the PCITS/LO). No activation peaks were found in the LO. The remaining location of V5 (5%) was in the descending limb of the superior temporal sulcus. Fourteen V5 locations are shown in Figures 4 and 5
. In Figure 4
the t-statistical maps and labelled sulci are shown in a sagittal slice chosen to visualize both the V5 locations and labelled sulci. In Figure 5
, the V5 locations are displayed on a cortical surface and an unfolded cortical surface. The unfolded surfaces are shown for the parieto-occipito-temporal junction. In the latter case, the identified sulci are displayed with different labels.
Landmarks
The average stereotaxic Talairach coordinates and standard deviations of two possible anatomical landmarks for the position of V5 were determined, i.e. the LO (and PCITS/LO) and ALITS (LOALITS) as defined by Watson et al. (Watson et al., 1993) and the junction of the ITS and ALITS (ITSALITS) (see Fig. 5
). These coordinates were x = 47 ± 3.5, y = 71 ± 5.0, z = 2 ± 3.7 (n = 10) and x = 45 ± 3.2, y = 74 ± 5.3, z = 2 ± 3.4 (n = 8) respectively for the left hemisphere. For the right hemisphere the respective coordinates were x = 46 ± 2.9, y = 66 ± 5.8, z = 2 ± 7.7 (n = 9) and x = 46 ± 2.4, y = 63 ± 4.1, z = 6 ± 7.3 (n = 7). As shown in Table 1
, these landmarks were 4 ± 4.6 mm (n = 8) apart in the left hemisphere and 7 ± 6.5 mm (n = 7) apart in the right hemisphere.
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The ITSALITS junction was present in all cases. For the ITSALITS junction this average distance corresponded to 9 ± 4.2 (n = 10) and 10 ± 5.1 mm (n = 9) for the left and right hemisphere respectively.
To estimate the variability of the position of V5, the distances from the individual V5 coordinates to the average V5 position were determined. The average absolute value of the distance and standard deviation were 6.4 ± 2.4 (n = 10) and 6.5 ± 2.8 mm (n = 9) for the left and right hemisphere respectively. To determine whether inter-subject registration of the anatomical landmarks would decrease the variability of the position of V5, the same distances were computed after substraction of the individual landmark coordinates from the corresponding coordinates of V5. These distances after subtraction of the ITSALITS coordinates were 6.3 ± 2.6 (n = 10) and 10.4 ± 5.0 mm (n = 9) for the left and right hemisphere respectively. The distances after substraction of the LOALITS coordinates were 6.6 ± 3.5 (n = 8) and 9.3 ± 4.2 mm (n = 7) for the left and right hemisphere respectively. None of these distances differ significantly from each other (P > 0.05).
Methodological Issues
The functional data were not corrected for head movement; however, the head restraints minimized motion. To estimate the amount of movement of a given point on the cortex, functional scans of six different subjects were analyzed with the AIR package (Woods et al., 1992, 1998
; Jiang et al., 1995
). The average amount of motion of a point on the surface of the brain was 0.27 mm (n = 702), with a maximum displacement of 1.1 mm. All these estimates were calculated with absolute values, i.e. the direction of motion was not taken into account and was assumed to always be the same. Therefore these estimates represent the worst case scenario.
The intra-subject registration error after transformation from the surface-coil aMRI to the head-coil aMRI was determined by selecting, in four subjects, six or seven specific anatomical landmark points in the head-coil aMRI and surface-coil aMRI. The landmark points of the surface-coil aMRI were mapped into the same space as the head-coil aMRI, both with the automatic procedure and by a landmark-based procedure. In the landmarkbased procedure the distances between the surface-coil landmarks and the head-coil landmarks were minimized. The average distance and standard deviation between the landmark points of the head-coil aMRI and the corresponding ones of the surface-coil aMRI mapped into the same space through the landmark-based registration was 0.74 ± 0.43 mm (n = 27). The corresponding value for the automatic registration was 1.01 ± 0.96 mm (n = 27). These average values also contain the average identification error for the landmark points. Even though this difference in group mean is significant, we note that the landmark-based registration result is optimized for the given set of landmarks. Therefore we conclude that the results for the automatic procedure are at least comparable to the manual landmark-based registration.
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Discussion |
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The position of V5 (or MT) in stereotaxic Talairach space as determined here is consistent with previous studies (Zeki et al., 1991; Watson et al., 1993
; De Jong et al., 1994
; Dupont et al., 1994
; McCarthy et al., 1995
; Tootell et al., 1995
, Uusitalo et al., 1997
; Shulman et al., 1998
). In most cases, V5 was selectively activated, i.e. only one activation peak was determined in each hemisphere. This activation peak was always situated in the parieto-temporo-occipital cortex. In some cases other visual areas were also activated, though with lower t-statistical values. These activation sites were, based on their position, probably V3/V3A, VP and less often V1/V2 (Sereno et al., 1995
; DeYoe et al., 1996
; Tootell et al., 1996
; Engel et al., 1997
; Tootell et al., 1997
). These points were never located in the parieto-temporooccipital cortex. This result is consistent with the notion that V5 receives its input mainly from the M-pathway and thus is relatively sensitive to low contrast and high temporal frequency (Tootell et al., 1995
).
Suppose, however, that there were a number of nearby areas, all M-cell driven and responsive to high temporal frequencies, but varying in relative strength of their activation in response to our stimulus. This situation would result in different areas being identified as V5 in different subjects; in some proportion of the cases, two or more spatially distinct t-statistical peaks would then be present in the region of interest. Such an outcome was never observed, except for a few cases where the distance between the peaks, always located within the same sulci, was small enough to have been produced by the same V5 area (Tootell and Taylor, 1995). These results confirm the selectivity of this visual stimulus for eliciting V5 responses.
The Sulcal Pattern
The sulcal patterns on the lateral surface of the occipital lobe are variable, and its gyri are often simply referred to as lateral occipital gyri (DeArmond et al., 1989; Carpenter, 1991
; Nolte, 1999
). Several different systematic descriptions have been given. One description distinguishes three occipital gyri, the inferior, middle (or lateral) and superior occipital (Talairach and Tournoux, 1988
; Duvernoy, 1991
). According to Duvernoy, these gyri are separated by the inferior and superior occipital sulci, and the inferior occipital sulcus is frequently absent (Duvernoy, 1991
). In the latter case only two gyri can be distinguished. The lateral occipital sulcus is considered to be an intermediate sulcus subdividing the middle occipital gyrus (analogous to the middle frontal sulcus). Others only distinguish two gyri, the superior and lateral (or inferior) occipital (Chusid, 1973
; DeGroot, 1991
); however, the lateral occipital gyrus may have further subdivisions. These two gyri are separated by the lateral occipital sulcus, of which there are often two (Ono et al., 1990
). These lateral sulci (Ono et al., 1990
) correspond to Duvernoy's inferior and lateral occipital sulci. These sulci were of interest to our study as they are correlated with the location of V5 (Watson et al., 1993
). All horizontally oriented occipital sulci located in the vicinity of V5 were defined as the lateral occipital sulcus (Ono et al., 1990
). We differentiate between two types of lateral occipital sulci, the LO and the PCITS/LO. This distinction was based on the observation that the ITS often extended into the occipital lobe where it became the lateral occipital sulcus (PCITS/LO) (Ono et al., 1990
). This distinction proved useful because V5 was never located in one type, the LO, but was in some cases positioned in the PCITS/LO and sometimes in the PCITS. The posterior end of the highly interrupted ITS gave rise to a ventrodorsally oriented sulcus, the ALITS (Watson et al. 1993
). This sulcus, which Duvernoy (Duvernoy, 1991
) referred to as the anterior occipital sulcus, separates the occipital and temporal lobes. Watson et al. also referred to the ALITS as the posterior continuation of the inferior temporal sulcus. This is different from our definition of the PCITS, which is the horizontally oriented extension of the ITS that does not reach the occipital pole and therefore is not referred to as PCITS/LO. Thus the definitions of the sulci used in this paper (see Fig. 2
) are consistent with most other descriptions given for the sulcal patterns in our region of interest.
Relation of Area V5 to the Sulcal Pattern
In agreement with the observations of Watson et al. (Watson et al., 1993) and Tootell et al. (Tootell et al., 1995
), V5 was mostly found within a sulcus. This finding may be explained by the extensive gyrification in this area, i.e. relatively more cortex is buried within sulci (Zilles et al., 1988
; Tootell et al., 1995
). The sulcus in which V5 was located was variable but mainly limited to three sulci, i.e. ALITS, ITS and the posterior extension of the ITS (PCITS and PCITS/LO). V5 was most commonly located in the ALITS. Watson et al. found the position of V5 to be close to the junction point (actual or interpolated) of the lateral occipital sulcus (LO and PCITS/LO) and the ALITS (Watson et al., 1993
). Our results show that the position of V5 is located, on average, 1 cm from this junction point. This average distance to V5 is the same for another anatomical landmark, i.e. the junction between the ITS and the ALITS. Realignment of the results to either landmark did not significantly alter the variation of the V5 locations. However, the latter was always present in our study and interpolation was unnecessary. Also, V5 was usually located within a sulcus intersecting with this junction, making it a more reliable V5 landmark.
Methodological Issues
Misregistration between the functional and anatomical data could potentially be an explanation for the variability between those data. These potential registration errors may have their origin in two processes, both relating to the short (surface-coil) aMRI taken before each functional scanning session. This aMRI was assumed to be in the same position as the functional scans taken immediately afterwards. A potential source of a registration error could occur due to movement of the subject during the scanning session, thus making our assumption false. Though we did not correct for movement the head constraints minimized motion and virtually eliminated cumulative head drift. The absolute movement values for a point on the surface of a brain are (~30 times) smaller than the variations between functional and anatomical data. Other registration errors may occur due to misregistration of the surface-coil aMRI with the head-coil aMRI. However, these registration errors are also (~10 times) smaller than the variations of our data. Therefore we conclude that misregistration issues do not play a significant role in the explanations of our results.
Variable fMRI responses could also potentially be an explanation for the variability between functional and anatomical data. However, the reproducibility of fMRI results is very good (Ramsey et al., 1996b; Casey et al., 1998
) and correlates highly with PET (Dettmers et al., 1996
; Ramsey et al., 1996a
). The reproducibility of the stereotaxic coordinates of area V5 has been indicated by several previous studies using a variety of imaging techniques (Zeki et al., 1991
; Watson et al., 1993
; De Jong et al., 1994
; Dupont et al., 1994
; McCarthy et al., 1995
; Tootell et al., 1995
; Anderson et al., 1996
; Uusitalo et al., 1997
; Shulman et al., 1998
). Studies of the cytoand myeloarchitecture of the visual cortex have identified V5 within the ITS, within the dorsal arm of the ITS (ALITS) (Tootell and Taylor, 1995
) and on the lateral occipital gyri specifically in the lateral (occipital) sulcus (Clarke and Miklossy, 1990
; Clarke, 1993
). These cytoand myeloarchitectural results are in agreement with our findings. Therefore we conclude that the variability of fMRI responses does not play a significant role in the explanation of our results.
Implications for Brain Imaging
Rademacher et al. (Rademacher et al., 1993) found that the prominent variability of primary cytoachitectonical areas is closely predictable from gross anatomical morphology of the brain [see also (Stensaas et al., 1974
; Gilissen and Zilles, 1996
)]. Based on these observations, Rademacher et al. suggested that a direct reference to the landmarks that frame these areas may be a more reliable basis for functional mapping. The stereotaxic space as defined by Talairach and Tournoux (Talairach and Tournoux, 1988
) exhibits variations in gross anatomical features (Steinmetz et al., 1989
, 1990
, 1991
; Hunton et al., 1996
). Noninear alignment of gross anatomical structures would reduce this kind of variability (Collins et al., 1996
) (Collins et al., submitted for publication). Our results show that, for human area V5, a linear alignment with two possible landmarks did not improve the alignment of the individual V5 positions. This suggests that even after alignment of gross cortical features, residual variability might still arise from the variability between gross anatomical features and functional areas.
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Conclusion |
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Notes |
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Address correspondence to Serge Dumoulin, McConnell Brain Imaging Centre, Montreal Neurological Institute, 3801 University Street, Webster 2B, Montréal, Québec, Canada H3A 2B4. Email: serge{at}bic.mni.mcgill.ca.
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