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Vision Research 41 (2001) 1459–1474
Sustained extrastriate cortical activation without visual awareness
revealed by fMRI studies of hemianopic patients
Rainer Goebel
a,
*, Lars Muckli
b
, Friedhelm E. Zanella
c
, Wolf Singer
b
, Petra Stoerig
d
a
Department of Cogniti6e Neuroscience,Faculty of Psychology,Maastricht Uni6ersity,Postbus
616
,NL-
6200
MD Maastricht,The Netherlands
b
Max Planck Institute for Brain Research,Deutschordenstr.
46
,D-
60528
Frankfurt a.M., Germany
c
Klinikum der Johann Wolfgang Goethe-Uni6ersita¨t,Institut fu¨r Neuroradiologie,
60528
Frankfurt a.M., Germany
d
Institute of Experimental Psychology II,Heinrich-Heine -Uni6ersity,Uni6ersita¨tsstr.
1
,D-
40225
Du¨ sseldorf,Germany
Received 23 January 2001; received in revised form 15 February 2001
Abstract
Patients with lesions in the primary visual cortex (V1) may show processing of visual stimuli presented in their field of cortical
blindness even when they report being unaware of the stimuli. To elucidate the neuroanatomical basis of their residual visual
functions, we used functional magnetic resonance imaging in two hemianopic patients, FS and GY. In the first experiment, a
rotating spiral stimulus was used to assess the responsiveness of dorsal stream areas. Although no response was detectable within
denervated or destroyed early visual cortex, motion-sensitive areas (hMT+/V5) ipsilateral to the lesion showed a strong sustained
hemodynamic response. In GY, this activation was at least as strong as that of his contralesional hMT+/V5 to the stimulus in
the normal hemifield. In the second experiment, coloured images of natural objects were used to assess the responsiveness of
ventral stream areas. Again, no activity was detectable in ipsilesional early visual areas, but extrastriate areas in the lateral
occipital cortex (hMT+/V5 and LO) and within the posterior fusiform gyrus (V4/V8) showed a robust sustained hemodynamic
response. In both experiments, we observed that ipsilesional areas responded to stimuli presented in either hemifield, whereas the
normal hemisphere responded preferentially to stimuli in the sighted hemifield. As only one subject occasionally noticed the onset
of stimuluation in the impaired field, the unexpectedly strong sustained activity in ipsilesional dorsal and ventral cortical areas
appears to be insufficient to generate conscious vision. © 2001 Elsevier Science Ltd. All rights reserved.
Keywords
:
Cortical blindness; Blindsight; Hemianopia; Visual cortical areas; Visual awareness; fMRI; Lesion
www.elsevier.com/locate/visres
1. Introduction
The term ‘blindsight’ describes the ability of neuro-
logical patients with postgeniculate lesions to detect,
localise and discriminate visual stimuli in blind parts of
the visual field, although they do not consciously per-
ceive them (Weiskrantz, Warrington, Sanders, & Mar-
shall, 1974). These residual visual functions must be
mediated by those parts of the visual system that retain
visual responsiveness despite the lesion that destroys or
denervates primary visual cortex (V1) and causes corti-
cal blindness. Data from monkeys have shown that
despite retrograde degeneration of projection cells in
the dorsal lateral geniculate nucleus (dLGN) and the
retina (Van Buren, 1963; Cowey, Stoerig, & Perry,
1989), subcortical retinorecipient nuclei continue to re-
ceive visual input from the parts of the retinae that
represent the cortically blind visual field (for a recent
review, see Stoerig & Cowey, 1997). Some of these
nuclei project directly to extrastriate visual cortex,
which consists of cytoarchitectonically distinct areas
that subserve specific visual functions (Zeki, 1974; Zilles
& Clarke, 1997). Evidence indicates that these areas are
organized within two main visual pathways (Mishkin,
Ungerleider, & Macko, 1983): a ventral stream or
‘what’ system devoted to the fine-grained analysis of the
visual scene, including processing of shape and colour
and a dorsal stream or ‘where’ system, which processes
spatial characteristics of the visual scene and analyses
motion. Emphasizing that the latter pathway is also
involved in visuomotor transformations, Milner and
* Corresponding author. Tel.: +49-69-96769471; fax: +49-69-
96769327.
E-mail address
:
r.goebel@psychology.unimaas.nl (R. Goebel).
0042-6989/01/$ - see front matter © 2001 Elsevier Science Ltd. All rights reserved.
PII: S0042-6989(01)00069-4
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Vision Research
41 (2001) 1459–1474
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Goodale (1995) proposed to distinguish between ‘vision
for perception’(ventral pathway) and ‘vision for action’
(dorsal pathway). The two pathways originate in areas
V1 and V2 and extend into the temporal (the ‘what’
system) and parietal (the ‘where’system) lobe, respec-
tively. With brain imaging techniques, they have been
convincingly demonstrated in the normal human brain
(e.g. Haxby et al., 1991) and several specialized areas
have been identified on the basis of their stimulus
preference profiles.
An extensively studied area in the ventral stream is
area V4, which in the macaque, appears to be involved
in the processing of chromatic and shape information
(see Cowey, 1994 for a review). It has been reported to
mediate colour constancy, but nevertheless, its necessity
for colour vision is debated on the grounds that abla-
tion of this area does not produce marked deficits in
colour discrimination (Heywood & Cowey, 1987). In
man, the colour complex has been located in the
fusiform gyrus (Lueck et al., 1989; Hadjikhani, Liu,
Dale, Cavanagh, & Tootell, 1998), in a region that is
generally compromised in patients with achromatopsia
(Meadows, 1974) and is often referred to as V4 (McK-
eefry & Zeki, 1997; Zeki, McKeefry, Bartels, & Frack-
owiak, 1998) or V8 (Hadjikhani et al., 1998); we shall
refer to it here as the ‘colour complex’or V4/V8. Other
areas located in close proximity to area V4/V8 have
been characterized, including the fusiform face area
(FFA, Kanwisher, Dermott, & Chun, 1997) and several
overlapping regions sensitive to different object cate-
gories (e.g. Ishai, Ungerleider, Martin, Schouten &
Haxby, 1999). Less specialized, with respect to object
categories but responsive to common objects, abstract
sculptures and famous faces is a more dorsal area in a
region at the lateral-anterior aspect of the occipital lobe
that Malach et al. (1995) called LO (lateral occipital
complex).
Of the dorsal stream areas, those that are specialized
for motion processing have received particular atten-
tion. In monkey cortex, the motion-selective area MT
(middle temporal area) is located in the middle tempo-
ral sulcus, close to the junction of the occipital, tempo-
ral and parietal lobes (Van Essen, Maunsell & Bixby,
1981). Its cells are responsive to the direction and speed
of moving stimuli (Snowden, Treue & Andersen, 1992)
and their inactivation causes deficiencies in motion
direction discrimination. Area MT is easily identified in
histological sections because of its high myelination and
it is surrounded by several other specialized areas
(‘satellites’) that process higher-order aspects of stimu-
lus motion. The human visual cortex contains an area
that is likely to correspond to monkey area MT and is
located in the occipito-temporo-parietal pit. Bilateral
lesions, that include this area, cause a severe impair-
ment in detecting the movement of objects (cortical
akinetopsia, see Zeki, 1991). Imaging studies have
shown that metabolism and blood flow in that region
increases more in response to moving than to stationary
stimuli, indicating preferential involvement of this area
in the processing of motion information (e.g. Watson et
al., 1993; Tootell et al., 1995; Goebel, Khorram-Sefat,
Muckli, Hacker, & Singer, 1998a). As functional imag-
ing studies have not yet convincingly differentiated
between the human homologue of area MT and its
satellites, this motion-selective region is generally re-
ferred to as the ‘human motion complex’(hMT+)or
as V5.
Although area MT receives its major input directly
or indirectly from the primary visual cortex (V1), de-
struction or temporary inactivation of V1 in monkeys
does not eliminate its visual responsiveness (Rodman,
Gross & Albright, 1989). Although the responses were
markedly reduced, a large part of the neuronal popula-
tion remained visually responsive and even retained
directional tuning. Accordingly, one might expect resid-
ual visual responsiveness in the motion complex of
human patients who have suffered lesions to the pri-
mary visual cortex, and indeed, functional imaging
studies in patients with lesions of the optic radiation or
primary visual cortex have confirmed its continued
responsiveness to moving or flickering stimuli (Barbur,
Watson, Frackowiak, & Zeki, 1993; Stoerig, Goebel,
Muckli, Hacker, & Singer, 1997; Zeki & ffytche, 1998).
In contrast to dorsal stream areas, neurons in the
monkey’s ventral stream become unresponsive to stim-
uli in the blind field after V1 lesions (Girard, Salin &
Bullier, 1991; Bullier, Girard & Salin, 1993). Thus, one
would expect little, if any, activity in areas of the
ventral stream in patients with lesions to the primary
visual cortex. However, in a recent imaging study of
two hemianopic patients, we have found that presenta-
tion of images of natural objects in the cortically blind
visual field can lead to strong sustained activity in the
ventral pathway without any detectable activity in pri-
mary visual cortex (Goebel et al., 1998b; Goebel,
Muckli, Zanella, Singer, & Stoerig, submitted).
In the present study, we compare the responsiveness
of dorsal and ventral (Goebel et al., submitted) stream
areas after blind field stimulation in the two hemianopic
patients, GY and FS, as measured by echoplanar func-
tional magnetic resonance imaging. To activate dorsal
stream areas, a rotating spiral stimulus was presented in
the cortically blind visual field. We used a rotating
spiral instead of translational motion (Sahraie et al.,
1997; Zeki & ffytche, 1998) because it restricts motion
to a limited region of space for prolonged stimulation
epochs (e.g. 30 s). This allowed us to separate the
hemodynamic response to stimulus onset, which GY
can be aware of (see Barbur, Ruddock, & Waterfield,
1980) from the sustained response to the rotatory mo-
tion. For activation of ventral stream areas, coloured
images of natural objects (fruit and vegetables) were
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Vision Research
41 (2001) 1459–1474
1461
used (Goebel et al., submitted). Both stimulus types
were also presented in the sighted visual field of the
patients to allow for a direct within-subject comparison
of the hemodynamic response to stimulation in the
cortically blind and in the intact visual field. As a
further control, the same experiments were conducted
with two healthy subjects. In addition, retinotopic map-
ping experiments were performed to describe the precise
spatial layout of the functional responsiveness of early
visual areas in the normal and lesioned hemisphere.
2. Methods
2
.
1
.Patients
FS and GY, who participated in this study, have
long-standing post-geniculate lesions of the left hemi-
sphere (see Fig. 1). FS, born in 1937, suffered a severe
craniocerebral trauma when he was 42 years of age.
GY, born in 1956, was involved in a traffic accident
when he was 8 years, and his left primary visual cortex
was almost completely destroyed by a vascular incident.
The visual field defects that resulted from the lesions
are shown in Fig. 2. The wedge-shaped region in FS’s
right hemifield (black) is absolutely blind, while GY’s
hemianopia is relative and allows conscious detection of
salient visual events. Over many years, GY and FS
have participated in studies of their residual visual
functions (e.g. for GY: Barbur et al., 1980; Blythe,
Bromley, Kennard, & Ruddock, 1986; Brent, Kennard,
& Ruddock, 1994; Weiskrantz, Barbur, & Sahraie,
1995; Morland, Ogilvie, Ruddock, & Wright, 1996;
Finlay, Jones, Morland, Ogilvie, & Ruddock, 1997;
Marcel, 1998; Guo, Benson, & Blakemore, 1998; Ben-
son, Guo, & Blakemore, 1998; Kentridge, Heywood, &
Weiskrantz, 1999 and for FS: Po¨ppel, 1985, 1986; Sto-
erig, 1993; Stoerig & Cowey, 1997; Stoerig, Klein-
schmidt, & Frahm, 1998).
The lesions were visualized by MR-imaging (Fig. 1)
using a high-resolution T1-weighted 3D FLASH se-
quence (voxel size 1×1×1 mm) recorded with a 1.5 T
scanner (Siemens Magnetom Vision). FS’s extensive
lesion primarily affects the temporal lobe and includes
the optic radiation in the vicinity of the LGN. In GY,
the medial occipital lobe of the left hemisphere is
destroyed, including most of V1, as well as surrounding
extrastriate visual cortex and the underlying white mat-
ter, but sparing the occipital pole.
2
.
2
.Tasks
2
.
2
.
1
.Retinotopic mapping
The responsiveness and delineation of early visual
areas V1, V2, V3, VP, V3A, V4v and V4d was investi-
gated with retinotopic mapping scans (cf. Sereno, Dale,
Reppas, Kwong, Belliveau, Brady, Rosen, & Tootell,
1995), sampling 12 contiguous slices approximately in
parallel to the calcarine fissure. Eccentricity and polar
angle mapping experiments were performed in the same
recording session (for details see Linden, Kallenbach,
Heinecke, Singer, & Goebel, 1999). For eccentricity
mapping, a ring-shaped configuration of black and
white contrast-reversing (8 Hz) checkers was presented
centered around the fixation point. The ring started
with a radius of 1°visual angle and expanded to a
radius of 12°within 96 s. For polar angle mapping, the
same pattern was configured as a wedge subtending
22.5°in polar angle with the tip at the fixation cross.
The wedge started at the left horizontal meridian and
slowly rotated clockwise for a full cycle of 360°within
96 s. Each mapping experiment consisted of four repeti-
tions of a full expansion and a full rotation.
2
.
2
.
2
.Mapping of the motion complex
Motion-selective areas were identified by comparing
the hemodynamic response during presentation of a
moving stimulus with the response during presentation
of a stationary control stimulus. We used a flowfield
stimulus, consisting of 400 white dots moving radially
outward on a black background (visual field: 28°wide
by 20°high, dot size: 0.06×0.06°, dot velocity: 3.6 –
14.4°/s). It was contrasted with a stationary dot display
to produce a clear response of motion-sensitive areas
(Tootell et al., 1995).
2
.
2
.
3
.Motion experiment
(
Experiment
1)
While the flowfield stimulated both hemifields simul-
taneously, the main stimulus was presented 6.8°off-axis
in one hemifield at a time. It consisted of a blue-and-
red (run 1) or black-and-white (run 2) checkered spiral
(Fig. 2A,C), 7°in diameter, rotating counter-clockwise
around its centre (180°/s). Each stimulation block
lasted for 30 s and was repeated four times within each
run. In an additional condition, a stationary spiral was
shown four times in four blocks of 30 s. All stimulation
blocks were separated by fixation blocks of equal
length. The stimulus was presented on a grey back-
ground to prevent light scatter from the stimulus into
the sighted hemifield. A schematic drawing of the stim-
ulus configuration is shown in Fig. 2(A,C).
2
.
2
.
4
.Object experiment
(
Experiment
2)
Coloured images of natural objects (fruit and vegeta-
bles) subtending 5.2×5.2°were presented in the left
(normal) or right (impaired) upper visual field, 7°off-
axis (Fig. 2B). Each stimulation block lasted for 30 s
and was repeated four times within each recording
session. Stimulation blocks were separated by fixation
blocks of equal length. Within a stimulation block, an
image was shown for 1 s and then replaced by the next
image without an interstimulus interval. Images con-
R.Goebel et al.
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Vision Research
41 (2001) 1459–1474
1462
Fig. 1. Lesions of patients GY (A) and FS (B). (A) Slices of an anatomical T1-weighted MRI scan showing the V1 lesion of GY. The small cross
in (1–3) indicates the 3D position of the selected slices, the yellow curve delineate the extend of the lesion within the respective slices. (1) Sagittal
slice through the lesion. (2) Axial slice through the lesion. (3) Coronal slice through the lesion. (4) Surface rendering of GYs reconstructed head
(yellow) and of the boundary of the V1 lesion (red). The rendered head was partially opened to reveal the size and position of the lesion. (B)
Rendering of the reconstructed cortical surface at the boundary between grey and white matter of the affected left hemisphere of patient FS. An
image containing a single slice running through the lesion is also shown.
R.Goebel et al.
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41 (2001) 1459–1474
1463
Fig. 2. Plots of visual field sensitivity (A,B) which are based on a combination of static and dynamic perimetry (target: 116’, 320 cyc deg
−1
m
−2
,
background: 10 cyc deg
−1
m
−2
; white: normal field, black: absolutely blind field; grey: relatively blind region, see text). (A) Visual field sensitivity
plot with indicated position of the moving spiral stimulus for GY (left) and FS (right). (B) Visual field sensitivity plot with indicated stimulation
position in the objects experiment for GY (left) and FS (right). Stimuli were shown in separate blocks in either the left or the right visual field.
(C) Stimulus size and location in the spiral experiment (left) and in the objects experiment (right).
R.Goebel et al.
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41 (2001) 1459–1474
1464
sisted of coloured drawings of natural objects (fruit and
vegetables, Corel Draw clip art gallery). The stimuli
were presented on a white background to minimize
stray light falling into the sighted hemifield. A sche-
matic drawing of the stimulus configuration is shown in
Fig. 2(B,C).
In order to assess whether the subjects were aware of
the stimuli presented in the cortically blind hemifield,
we asked them to respond by button press when they
detected anything in the right visual hemifield.
2
.
3
.MRI acquisition
Functional magnetic resonance imaging was per-
formed at 1.5 T (Siemens Magnetom Vision) using the
standard head coil and a gradient echo EPI sequence.
The Siemens Magnetom gradient overdrive allowed
functional scans with high spatial and temporal resolu-
tion (TE=69 ms, TR =3000 ms, FA =90°, FOV =
200×200 mm
2
, matrix size: 128×128, voxel size:
1.6×1.6 ×3–5mm
3
). A T1-weighted 3D MP RAGE
scan lasting 8 min was performed in the same session
(voxel size 1×1×1mm
3
). An additional T1-weighted
3D data set tuned to optimize the contrast between
gray and white matter was recorded in a separate
recording session lasting 24 min (FLASH sequence).
The intrasession MP RAGE 3D data set was automati-
cally aligned with the extrasession T1 FLASH data set.
Visual stimuli were delivered under computer control
(Digital DECpc Celebris XL 590) to a high-luminance
LCD projector (EIKI LC-6000). The image was back-
projected onto a frosted screen positioned at the foot of
the scanner. Visual stimuli were generated using the
Microsoft DirectX graphics library and a Matrox Mys-
tique graphics board.
2
.
4
.Data analysis
FMRI data analysis was performed using BrainVoy-
ager 3.×/2000 (Brain Innovation, Maastricht, The
Netherlands, www.BrainVoyager.com) and included re-
moval of low-frequency drifts, 3D motion detection
and correction, determination of Talairach coordinates,
multiple regression analysis, cortex reconstruction,
inflation and flattening. For the retinotopic mapping
experiments, cross-correlation analysis was applied (for
details see Linden et al., 1999). The eccentricity and
polar angle represented by a given cortical site was
determined by finding the lag value maximizing the
cross-correlation. The obtained lag values at each
voxel, corresponding to the eccentricity or polar angle
of optimal stimulation, were encoded in pseudocolours
on slices as well as on surface patches (triangles) of the
reconstructed cortical sheet (see below). Pixels were
included into the statistical map if the obtained cross-
correlation value rwas \0.4 (PB0.0001, uncorrected).
In order to detect weak activity within and surrounding
the lesioned or denervated regions, retinotopic mapping
experiments were also analysed with a lowered correla-
tion threshold of r\0.2. Based on the polar angle,
mapping the boundaries of retinotopic cortical areas
V1, V2, V3, VP, V3A and V4v were estimated on the
flattened cortical surface maps (see below) of each
patient’s non-lesioned hemisphere and of both hemi-
spheres in each control subject. The motion complex
mapping experiment was analysed with a simple corre-
lation analysis contrasting the flowfield stimulus with
the stationary control stimulus.
The two main experiments were analysed with a
multiple regression model consisting of two predictors,
one for the presentation of the stimulus (moving spiral/
images of natural object) in the left and one for the
presentation of the stimulus in the right visual field.
The overall model fit was assessed using an Fstatistic.
The obtained P-values were corrected for multiple com-
parisons using a cortex-based Bonferroni adjustment,
i.e. the number of voxels included for correction was
limited to grey matter voxels (Goebel & Singer, 1999).
The relative contribution of each of the two predictors
RC=(b
1
−b
2
)/(b
1
+b
2
) was visualised with a red-yel-
low-green pseudocolour scale. Statistical maps were
superimposed on the original functional scans and in-
corporated into the high-resolution 3D MRI data sets
through interpolation to the same resolution (voxel size:
1×1×1 mm). Since the 2D functional and 3D struc-
tural measurements were acquired in the same record-
ing session, coregistration of the respective data sets
could be performed on the basis of the Siemens slice
position parameters of the T2*-weighted measurement
(number of slices, slice thickness, distance factor, Tra-
Cor angle, FOV, shift mean, offcenter read, offcenter
phase, in-plane resolution) and the T1-weighted 3D MP
RAGE measurement (number of sagittal partitions,
shift mean, offcenter read, offcenter phase, resolution).
In order to compare activated brain regions across
sessions, anatomical and functional 3D data sets were
transformed into Talairach space (Talairach & Tour-
naux, 1988). Results were visualised by superimposing
3D statistical maps on reconstructions of each patient’s
cortical sheet. Areas were identified based on their
anatomical position and Talairach coordinates.
The recorded high-resolution T1-weighted 3D
recordings were used for surface reconstruction of both
cortical hemispheres of the control subjects and patients
(for details see Linden et al., 1999; Kriegeskorte &
Goebel, submitted). The white/grey matter border was
segmented with a region-growing method preceded by
inhomogeneity correction of signal intensity across
space. The border of the resulting segmented subvol-
ume was tessellated to produce a polygon-mesh surface
reconstruction of each cortical hemisphere. The tessella-
tion of the white/grey matter boundary of a single
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41 (2001) 1459–1474
1465
hemisphere typically consists of :250000 triangles. An
iterative 3D morphing algorithm (Goebel et al., 1998a)
was used to move the vertices outward along the sur-
face normals into the grey matter. Through visual
inspection, this process was halted when the surface
reached the middle of the gray matter corresponding
approximately to layer 4 of the cortex. The resulting
surface was used as the reference mesh for projecting
functional data on folded, inflated or flattened repre-
sentations. A morphed surface was always linked to its
folded reference mesh, so that functional data could be
shown at the correct location of an inflated or flattened
representation. This link was also used to minimize
geometric distortions during inflation and flattening
(Goebel, 2000) by inclusion of a morphing force that
keeps the distances between vertices of each triangle of
the morphed surface as close as possible to the respec-
tive values of the folded reference mesh.
3. Results
Results from a control subject of the retinotopic
mapping, motion complex mapping and objects experi-
ment are shown in Fig. 3. Results of the two patients
are shown in Figs. 4–6.
3
.
1
.Retinotopic mapping
The topography of the early visual areas is shown in
Fig. 3(A) for a normal observer. In the patients, the
contralesional V1 appeared normal, but no visual re-
sponsiveness was seen in its lesioned (GY) or dener-
vated (FS) counterpart (r`0.4, PB0.00001). Only a
small region at the occipital pole was activated in GY
(Fig. 5(A), see also Baseler, Morland, & Wandell,
1999). This is in agreement with GY’s visual field
perimetry that shows a 3°macular sparing in the lower
quadrant of the hemianopic right visual field (Barbur et
al., 1980).
3
.
2
.Motion complex mapping
The comparison of the flowfield stimulus with the
stationary dot stimulus revealed several motion-selec-
tive areas in both hemispheres including the motion
complex, area V3A and an area at the border between
occipital and parietal lobes (Fig. 3B). In GY, the mo-
tion complex in the ipsilesional hemisphere is located
more posteriorly and more ventrally than in the con-
tralesional hemisphere. The position of the motion
complex in both patients (Table 1) agrees with previous
reports in normal observers (Tootell et al., 1995; Goe-
bel et al., 1998a).
3
.
3
.Motion experiment
In the control subjects, the foci of activation in the
lateral occipital cortex produced by passive viewing of
the moving spiral were functionally identified as
hMT+/V5 because they overlapped with the regions
activated by the flowfield stimulus (not shown). When
the moving spiral stimulus was presented in the corti-
cally blind (right) visual field of the patients, the ipsile-
sional (left) motion complex was strongly activated
(Fig. 4) despite the fact that there was no detectable
activation within and around the lesioned or dener-
vated region. A weaker but significant response was
also observed in the contralesional motion complex.
When the spiral stimulus was presented in the left
(sighted) hemifield, both the contralesional motion
complex, as well as the ipsilesional motion complex,
responded strongly (see Fig. 4). Thus, the motion com-
plex at the ipsilesional side responded equally strong
(FS) or stronger (GY) to the moving spiral presented in
the cortically blind visual field, whereas the response of
the contralesional motion complex was stronger to the
spiral in the sighted (left) visual field in both patients.
In B20% of the presentations of the rotating spiral
in the cortically blind hemifield, GY pressed the button
for a short duration following the onset of the spiral,
indicating that he was aware of a stimulus change. An
analysis of the data restricted to the first 15 s of the 30-s
stimulation epochs produced almost identical results as
the analysis restricted to the last 15 s. FS never indi-
cated awareness when stimuli were presented in his
blind visual field.
In GY, the comparison of the hemodynamic response
to the presentation of the moving spiral in the cortically
blind visual field and the sighted visual field revealed
that the extent of the functionally defined motion com-
plex in the lesioned hemisphere was greater than in the
intact hemisphere (Table 2). Interestingly, this differ-
ence was more pronounced in the black-white spiral
experiment than in the red-blue spiral experiment. The
red-blue spiral, although not isoluminant, possessed
much less luminance contrast than the black-white spi-
ral. We quantified the observation of an extended ip-
silesional motion complex in GY using the number of
activated voxels as well as the maximal correlation
values in the obtained statistical maps (Table 2). Dur-
ing presentation of the moving spiral in the cortically
blind visual field, the maximum single-voxel correlation
value was r
max
=0.62 (black-white spiral) and r
max
=
0.61 (red-blue spiral) and located in the ipsilesional
motion complex. With a fixed single-voxel correlation
value of r\0.4 (PB0.00001, uncorrected), the cluster
size (CS=number of activated voxels) was CS
r\0.4
=
93 (black-white spiral) and CS
r\0.4
=61 (red-blue spi-
ral). During presentation of the moving spiral in the
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41 (2001) 1459–1474
1466
sighted visual hemifield, the maximum single-voxel cor-
relation value was r
max
=0.55 (black-white spiral) and
r
max
=0.60 (red-blue spiral) and located in the contrale-
sional motion complex. With a value of CS
r\0.4
=40,
the cluster size was also larger for the red-blue than the
black-white spiral (CS
r\0.4
=26), indicating that in the
normal hemisphere, chromatic contrast is more effec-
tive than in the lesioned one.
Fig. 3. Results of a control subject of the retinotopic mapping experiment (A), motion complex mapping experiment (B) and objects experiment
(C). (A) Boundaries of retinotopic cortical areas were determined through field sign map computations (cf. Sereno et al., 1995) based on
eccentricity and polar angle mapping. (B) Lateral view of the reconstructed cortical sheet. The statistical map comparing the flowfield condition
with the stationary dots condition is projected on the surface revealing motion-selective areas including V3A and hMT+/V5. (C) Lateral and
ventral view of ‘inflated’cortical hemispheres. Activated regions responding solely to objects presented in the left visual field are coloured green;
regions responding solely to objects presented in the right visual field are coloured red. Areas responding with equal strength to stimuli in either
hemifield are shown in yellow (for graded values, see colour scale).
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Fig. 4.
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41 (2001) 1459–1474
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3
.
4
.Object experiment
In the control subjects, activated regions in early
visual areas responded solely to objects presented in the
contralateral visual field (Fig. 3C). With increasing
distance from V1, visual areas responded also to stimuli
in the ipsilateral visual field as indicated in Fig. 3(C) by
the change from red to yellow color (left hemisphere)
and green-to-yellow color (right hemisphere). Regions
responding equally well to stimuli in both visual fields
(yellow) were more extended in the right hemisphere.
The human motion complex, which is known to re-
spond not only to motion but also to flickering stimuli
(Tootell et al., 1995) also responded strongly to the
presentation of the images. The motion complex in
either hemisphere responded to stimuli in both visual
fields albeit with a stronger response to the respective
contralateral hemifield.
The normal hemisphere in the patients responded to
stimuli in the normal hemifield with a similar activation
pattern as that seen in the control subjects, and includes
early visual areas, the lateral occipital cortical region
and a region in the fusiform gyrus (Fig. 5(B) and Fig.
6(B), right hemisphere). Activity in the lesioned hemi-
sphere caused by stimuli in the normal field (Fig.
5(B,C) and Fig. 6(B,C), green curves) was less extended
than in the controls, but in GY, the region in the
fusiform gyrus responded as well as it did to stimuli in
the normal hemifield. Much to our surprise, ventral
areas in the lesioned hemishere responded quite
strongly to images presented in the impaired (right)
hemifield (Fig. 5C and Fig. 6C, red curves),. In GY,
both a region in the fusiform gyrus and the lateral
occipital region were activated. These foci presumably
correspond to V4/V8 and area LO, respectively, as their
Talairach coordinates (Table 1) closely match those
reported in the literature (Malach et al., 1995; Had-
jikhani et al., 1998). Time courses show that the ipsile-
sional response strength in area V4/V8 is nearly the
same for stimuli in the blind and sighted field, but the
response of area LO is weaker for stimuli in the blind
field (Fig. 5C). In FS, the lateral occipital region in the
lesioned hemisphere responded roughly half as strong
to images in the impaired hemifield compared to the
response after sighted field stimulation (Fig. 6C), but
there was only little activation in V4/V8. In both sub-
jects, some activation was also seen in hMT+/V5. In
Table 1
Talairach coordinates (x,y,z) of regions hMT+/V5, LO, and V4/V8
in the left (LH) and right (RH) hemisphere of patients GY and FS.
FS LHGY RH FS RHGY LH
−36, −67, 1hMT+/V5 47, −63, 0 −48, −76, 0 47, −64, −3
45, −65, −20LO −38, −67, −8−39, −73, −15 43, −65, −16
22, −62, −21V4/V8 −35, −62, −18−25, −65, −12 28, −53, −17
Table 2
Two measures characterizing the response strenght in hMT+/V5 in
the left, lesioned hemisphere after blind field stimulation and in the
right hemisphere after stimulation in the sighted hemifield: maximum
observed correlation value (r
max
) and cluster size (number of con-
nected, activated pixels) at a specified correlation value of r=0.4
(CS
r=0.4
)
Black-white spiral Red-blue spiral
r
max
CS
r=0.4
r
max
CS
r=0.4
26 0.60 40RH 0.55
610.6193LH 0.62
GY, bilateral hMT+/V5 activity was observed after
stimulation in either hemifield (Fig. 5B,C), but in FS,
only stimulation of the normal hemifield elicited bilat-
eral hMT+/V5; no significant activity was observed
after stimulation in the blind visual field (Fig. 6B,C).
Throughout, the normal hemisphere showed very little
activation in response to stimuli in the impaired field,
indicating that the coactivation of corresponding areas
commonly seen in higher extrastriate cortical areas is
compromised. In contrast to control subjects, no activ-
ity was observed anterior to V4/V8 in the left, lesioned
hemisphere in either patient.
In B10% of the presentations of the objects in the
cortically blind hemifield, GY pressed the button for a
short duration following the onset of the image se-
quence, indicating that he was aware of a stimulus
change. An event-related analysis of ‘aware’versus
‘unaware’epochs produced almost identical results. As
in the motion experiment, FS never indicated awareness
when stimuli were presented in his blind visual field.
Fig. 4. Multiple regression results of the black-and-white spiral experiment of patient GY (A) and patient FS (B), shown on inflated representation
of the cortical sheet. Activated regions responding solely to the spiral presented in the left visual field are coloured green; regions responding solely
to the spiral presented in the right visual field are coloured red. Areas responding with equal strength to the spiral in either hemifield are shown
in yellow (for graded values, see colour scale). (A) Activated regions in the right hemisphere are dominated by green colors whereas regions in
the lesioned left hemisphere are dominated by yellow colors. The extent of the functionally defined motion complex is greater in the ipsilesional
hemisphere than in the intact hemisphere. Time courses of left and right hemispheric motion complex (hMT+/V5) for left hemifield stimulation
(green curves) and right hemifield stimulation (red curves). (B) Activated regions in the right hemisphere are dominated by green colors whereas
regions in the lesioned left hemisphere are dominated by yellow colors.
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41 (2001) 1459–1474
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Fig. 5. Multiple regression results of object experiment of patient GY. Dark red regions in (A) and (B) correspond to the boundary of the cortex
and the lesion; LH=left hemisphere, RH=right hemisphere. (A) Folded (small insets) and flattened representation of the reconstructed cortical
sheet with superimposed results of eccentricity mapping; foveal to peripheral visual field representations are coded in colour from red to yellow
to blue to green. (B) Results of the object experiment superimposed on a subpart of the flattened cortex representation of each hemisphere as
indicated with white rectangles in (A). Activated regions responding solely to objects presented in the left visual field are coloured green, regions
responding solely to objects presented in the right visual field are coloured red. Areas responding with equal strength to stimuli in either hemifield
are shown in yellow (for graded values, see colour scale); FG=fusiform gyrus. (C) Time courses of right hemispheric area V1/V2 and left and
right hemispheric areas hMT+/V5, presumed LO and presumed V4/V8 for left hemifield stimulation (green curves) and right hemifield
stimulation (red curves); location of plotted areas are indicated by numbers 1–4in(B).
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Fig. 6. Multiple regression results of object experiment of patient FS. Dark red regions in (A) and (B) correspond to the boundary of the cortex
and the lesion; LH=left hemisphere, RH=right hemisphere. (A) Folded (small insets) and flattened representation of the reconstructed cortical
sheet with superimposed results of the main experiment. (B) Results of the object experiment superimposed on a subpart of the flattened cortex
representation of each hemisphere as indicated with white rectangles in (A). Activated regions responding solely to objects presented in the left
visual field are coloured green, regions responding solely to objects presented in the right visual field are coloured red (for graded values, see colour
scale); FG=fusiform gyrus. (C) Time course plots of areas of interest as in Fig. 5; location of plotted areas are indicated by numbers 1–4in(B).
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4. Discussion
4
.
1
.Summary
We studied activation patterns in dorsal and ventral
cortical areas in response to a rotating spiral and to
images of natural objects presented in the intact and
cortically blind fields of two hemianopic patients. We
found surprisingly strong responses to blind-field stimu-
lation in ipsilesional extrastriate areas including the
motion complex, but also in ventral areas, which prob-
ably correspond to area LO and V4/V8. There was no
detectable activity in the early visual cortical areas of
the lesioned hemisphere and with the exception of GY’s
occasional button press at stimulus onset, the patients
indicated no awareness of the stimuli. In addition, the
data revealed an unexpected asymmetry: the areas of
the intact hemisphere responded well to stimulation of
the contralateral, sighted hemifield but very little to
stimulation of the impaired hemifield. In contrast, the
corresponding areas in the lesioned hemisphere re-
sponded to stimulation of either hemifield.
4
.
2
.Extrastriate cortical acti6ation without V
1
A strong and sustained activity in extrastriate areas is
not what one would have expected on the basis of
previous monkey experiments which showed that re-
sponses of neurons in MT, while still present, are
markedly reduced (Rodman et al., 1989) and that neu-
rons in ventral stream areas become unresponsive to
visual stimuli presented in the affected hemifield
(Girard et al., 1991; Bullier et al., 1993). It appears
unlikely that the observed activation is mediated by
only partially damaged V1 tissue (Fendrich, Wessinger,
& Gazzaniga, 1992; Wessinger, Fendrich, & Gazzaniga,
1997) since several other functional imaging studies
have also shown an absence of detectable activation in
the lesioned cortex in GY (see Barbur et al., 1993;
Sahraie et al., 1997; Zeki & ffytche, 1998; Baseler,
Morland, & Wandell, 1999; Kleiser, Wittsack, Niedeg-
gen, Goebel, & Stoerig, 2001) and the denervated re-
gion in FS (Stoerig et al., 1998; Kleiser et al., 2001)
after blind field stimulation. Nevertheless, of the two
findings, the dorsal activation of hMT+is less surpris-
ing. It has been reported before (Barbur et al., 1993;
Sahraie et al., 1997; Stoerig et al., 1997; Zeki & ffytche,
1998) and it agrees well with psychophysical data show-
ing that ‘dorsal’functions, such as localization (Po¨ppel,
Frost & Held, 1973; Weiskrantz et al., 1974) and mo-
tion processing (Barbur et al., 1980; Po¨ppel, 1985;
Blythe et al., 1986; Perenin, 1991; Benson et al., 1998)
can be demonstrated in cortically blind fields. In view
of the physiological results from monkey studies (Rod-
man, Gross & Albright, 1990), it is likely that the
information reaches hMT+via the colliculo-pulvino-
extrastriate cortical pathway. What is unexpected is the
extent of ipsilesional hMT+activation in GY, which,
different from FS, is actually as pronounced as that of
the motion complex in the intact hemisphere when it is
stimulated from the normal hemifield. The strength of
activation runs counter the reduction seen in the physi-
ological data from monkeys with ablated or cooled V1
and may indicate plastic changes of the system compen-
sating for the loss of V1 which is normally the major
(direct and indirect) source of hMT+input. When
compared to FS, in whom the activation was weaker on
the lesioned side, one may suggest that GY’s much
earlier lesion allowed for better reorganization. That it
is luminance rather than chromatic contrast that reveals
the extent of GY’s hMT+activation could be seen as
a consequence of the degenerative effects of a V1 lesion
on the colour-opponent retino-geniculo-striate cortical
system that originates in the Pb-ganglion cells of the
retina (Cowey et al., 1989): The magnocellular lumi-
nance- and motion-processing system feeding into the
dorsal pathway is much less compromised.
In view of the data from monkeys, whose V1 had
been deactivated (Bullier et al., 1993), the activation of
ventral cortical areas from stimulation of the impaired
field is most unexpected. In the absence of V1, the
information could reach the ventral areas either via
direct subcortical projections, as those from the degen-
erated lateral geniculate nucleus (Yukie & Iwai, 1981;
Cowey & Stoerig, 1989), or it could arise via lateral
dorso-ventral connections. Our data do not allow refu-
tation of either hypothesis, although the latter is ren-
dered somewhat less likely by the weakness of the
object-induced activity seen in hMT+. Preliminarily,
we have attributed this hMT+activation to the image
presentation frequency of 1 Hz which represents a slow
flicker. ‘Ventral’functions, such as chromatic (Po¨ppel,
1986; Stoerig, 1987; Stoerig & Cowey, 1992; Brent et
al., 1994) and shape discrimination (Weiskrantz et al.,
1974; Weiskrantz, 1987; Marcel, 1998; Stoerig, in
preparation, 1998) have also been demonstrated in cor-
tically blind visual fields, although they are generally
more difficult to elicit than the dorsal functions, and
require more testing to reveal weaker, albeit sometimes
highly significant, results. Our results indicate that it
may be the human colour complex V4/V8 that mediates
the residual processing of chromatic information, as
chromatic information activates this region (Lueck et
al., 1989; Hadjikhani et al., 1998) and its destruction
entails achromatopsia (Meadows, 1974). This assump-
tion fits well with findings showing good chromatic
processing in GY (Brent et al., 1994 Barbur et al., 1999
Stoerig, in preparation), but poorer processing in FS
(Stoerig, 1987; in preparation) whose V4/V8 was not
detectably activated during blind field stimulation. The
ipsilesional lateral occipital area LO that responded in
both subjects could be involved in residual form pro-
R.Goebel et al.
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41 (2001) 1459–1474
1472
cessing, although the psychophysical predictions sug-
gested by the response properties of LO —better
response to objects than textures, comparable responses
to faces, objects, and abstract sculptures (Malach et al.,
1995), and reduction of activity in response to scram-
bled natural objects (Grill-Spector et al., 1998) —have
not yet been tested.
4
.
3
.Asymmetry of extrastriate cortical acti6ation
While we found that each hemisphere was activated
by its contralateral visual hemifield, activation by the
ipsilateral hemifield was asymmetrical for the two hemi-
spheres. Though this pattern was less obvious in dorsal
areas, the ventral foci of the intact hemisphere re-
sponded much less to stimulation of the impaired
hemifield than did those of the lesioned hemisphere to
stimulation of the normal hemifield. In addition, the
activation in the lesioned ventral areas is quite focal: it
does not extend forward or backward as it does in the
intact hemisphere. It is possible that these extrastriate
areas, while able to respond to stimuli in the impaired
field, are incapacitated with respect to conveying activ-
ity forward, backward, or to the other hemisphere.
Such an inability to effectively transmit signals to other
areas might be caused by inactivation of recurrent
loops between higher and early visual areas. Recurrent
loops can organize neuronal activity into stable reso-
nant states, which have been proposed as the neural
correlate of conscious vision (e.g. Tononi & Edelman,
1998; Grossberg, 1999; Engel & Singer, 2001). As we
found sustained and pronounced cortical activity in
both subjects without awareness of the presented stim-
uli, our data are in agreement with such ‘resonance’
theories, but not with simple ‘activation threshold theo-
ries’(Palmer, 1999), which assume that any cortical
neural activity sufficiently strong or lasting will produce
conscious experience of the content it represents.
Acknowledgements
It is a pleasure to thank FS and GY for participation
in this study. We thank Claudia I. Goebel for her help
in performing this study and Niko Kriegeskorte for
helpful comments on the manuscript. This work was
supported by the Max Planck Society and a Human-
Capital and Mobility network grant from the European
Community.
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