c o r t e x 1 3 4 ( 2 0 2 1 ) 2 0 7 e2 2 2

Available online at www.sciencedirect.com

ScienceDirect
Journal homepage: www.elsevier.com/locate/cortex

Research Report

Midlevel visual deficits after strokes involving area

human V4

Karoline Spang a,*, Cathleen Grimsen a, Maren Prass a, Freimuth Brunner b,

Martin Ko€hnlein c, Stefanie Kehrer c, Antje Kraft c, Stephan A. Brandt c and
Manfred Fahle a,1
a
Department of Human Neurobiology, University of Bremen, Bremen, Germany
b
Department of Neurology, Klinikum Bremen-Mitte, Bremen, Germany
c
Department of Neurology, Charite Universita
€tsmedizin Berlin, Berlin-Mitte, Germany

article info abstract

Article history: We present the results of 51 stroke patients with free central visual fields of which about
Received 13 February 2019 half suffer from clear deficits of midlevel vision undetected by standard clinical tests.
Reviewed 11 July 2019 These patients yield significantly elevated thresholds for detection and/or discrimination
Revised 28 September 2019 between forms defined by motion, colour, or line orientation (‘texture’). As demonstrated
Accepted 15 June 2020 by voxel-based lesion-symptom mapping (VLSM) the underlying lesions involve mainly
Action editor H. Branch Coslett area human V4 (hV4) located in the posterior third of the fusiform gyrus and extending into
Published online 3 September 2020 the lingual gyrus.
Patient’s detection thresholds correlate only very weakly between the submodalities
Keywords: tested, indicating partly separate neural networks on mid-level vision for colour, motion,
Midlevel vision and texture detection. Correlations are far stronger for form discrimination tasks, indicating
Patient study partly shared mechanisms for even simple form discrimination of distinct visual sub-
Voxel-based lesion-symptom modalities. We conclude that deficits of visual perception are far more common after
mapping strokes in visual brain areas than is apparent in clinical practice. Our results further clarify
Human V4 the functional organization of midlevel visual cortical areas.
Visual deficit © 2020 Published by Elsevier Ltd.

than 30 modules with differing specialization for visual sub-

1. Introduction: specificity of cortex? modalities such as contrast, colour, or motion perception (Van
Essen, Anderson, & Felleman, 1992). Common sense tells us
Animal and single cell studies have demonstrated that around
that brain tissue is there for a purpose, and loss of chunks of
50% of primate neocortex is concerned with visual perception
this tissue should have negative consequences. Lesions in
(Kandel & Wurtz, 2000) and that visual cortex contains more

* Corresponding author. Department of Human Neurobiology, University of Bremen, Hochschulring 18, D-28359, Bremen, Germany.
E-mail address: [email protected] (K. Spang).
1
Manfred Fahle has passed away (February 2020).
https://doi.org/10.1016/j.cortex.2020.06.006
0010-9452/© 2020 Published by Elsevier Ltd.
208 c o r t e x 1 3 4 ( 2 0 2 1 ) 2 0 7 e2 2 2

different areas should therefore cause a large variety of defi- presented here. We correlated behavioural results of sub-
cits of visual perception. The most frequently reported deficits groups of patients with pathological scores in one or several
are visual field defects that are easily detected using peri- modalities with their anatomical lesion locations by means of
metry. But only relatively few mostly single-case studies re- voxel-based lesion-symptom mapping (VLSM) to allocate
ported deficits of midlevel vision following lesions of visual these visual deficits to specific brain regions. The method of
brain areas in patients with intact visual fields, hence the VLSM (Bates et al., 2003) has been used before to correlate
exact contribution of the more than 30 modules of primate stroke lesions to clinical deficits such a neglect (Beume et al.,
visual cortex is far from clear (Van Essen & Gallant, 1994). 2017; Karnath, Rennig, Johannsen, & Rorden, 2011), somato-
The deficits we investigated are on a level below object sensory deficits (Meyer et al., 2015) and reading and writing
recognition but above luminance discrimination, the so-called (Baldo et al., 2018) but there was no attempt of correlating
midlevel vision including discrimination of simple forms. visual subsystems systematically to anatomical locations.
Deficits on this level between agnosias and visual field defects We hypothesize that a relatively high percentage of pa-
have been termed ‘indiscriminations’ (Fahle, 2003). For tients after strokes of visual areas suffer from (highly) specific
example, Troscianko et al. (1996) and Ruttiger et al. (1999) re- disturbances of visual perception that are not detected by
ported patients suffering from an isolated loss of colour clinical tests. Given the high number of distinct visual cortical
discrimination without visual field loss or apparent deficits in areas, we suppose that submodalities such as colour or mo-
any other visual submodality. Similarly, Zihl et al. and others tion are perceived and processed at several distinct functional
(Vaina, Lemay, Bienfang, Choi, & Nakayama, 1990; Zihl, von and anatomical levels. Hence, detection and discrimination of
Cramon, & Mai, 1983) described rare cases of an isolated simple forms defined by different submodalities may be
strong deficit in motion perception though a later test of the defective relatively isolated from each other. It may be too
‘Zihl’ patient indicated additional simultanagnosia (Gruesser simple to ask whether or not e.g., colour vision is normal since
& Landis, 1991). The relative specificity of these isolated de- colour perception can be disturbed on different levels, repre-
fects of colour or motion perception fits in very well with the sented by separated elements of a neuronal network incor-
traditional view of cortical specificity as put forward, e.g., by porating both bottom up and top down elements (Rumelhart,
Zeki’s ‘colour area’ (V4) or V5/MT’s description as the ‘motion McClelland, & the PDPResearchGroup, 1986; Van Essen et al.,
area’ (Britten, Shadlen, Newsome, & Movshon, 1993; Zeki, 1992; Herzog & Fahle, 1998; Tsotsos, Rodrı́guez-Sa  nchez,
1978). Rothenstein, & Simine, 2008; Bartolomeo, Bachoud-Levi, &
But this view of highly specialized and unitary cortical Thiebaut de Schotten, 2014). This hypothesis would explain
areas that (almost) exclusively perform one type of task e a bit why so few patients show a complete defect of e.g., colour or
like the older view of highly specialized sensory and motor motion perception.
speech areas e has lost part of its appeal due to both imaging
and single-cell studies (Baizer, Ungerleider, & Desimone, 1991;
Freiwald & Tsao, 2010; Moeller, Freiwald, & Tsao, 2008; Van 2. Methods
Essen et al., 1992; Van Essen & Gallant, 1994). Especially, the
scarcity of clinical reports on specific visual deficits argues 2.1. Ethics statement
against this view of a single ‘motion’ or ‘colour’ area. If such
specific areas would exist, quite a number of strokes should The study was conducted in conformity with the declaration
destroy such an area leading to specific deficits of perception. of Helsinki and was approved by the local ethics committees
Patients do not usually show such isolated deficits. Rather in Bremen and Berlin. Written informed consent was obtained
their symptoms are compatible with the existence of small from all participants. They were free to withdraw from the
networks of even more specialized areas subserving different study at any time. All subjects were unaware of the purpose of
aspects of for example face recognition. The same may be the experiments. Participants of the control group were paid
true, we hypothesize, for the perception of colour, motion, and for their participation. Patients were reimbursed for their
other elementary features. One reason that even these highly travelling costs. No part of the study analyses was pre-
specific deficits of post-stroke vision usually remain unde- registered prior to the research being conducted. The data
tected in the clinic (and by the patients themselves) may be have been collected over a period of more than 10 years. In the
their specificity and the lack of appropriate clinical tests to informed consent there was approval of the patients to pub-
detect relatively specific losses and that are missed by using lish anonymized data. Anonymized psychophysical study
qualitative tests presented only centrally. data, presentation and analysis codes are published in https://
To further clarify whether or not cortical specificity goes doi.org/10.5281/zenodo.3479558. As the imaging data cannot
beyond specialization for all aspects of ‘colour’ or ‘motion’, we be fully anonymized for ethical reasons these data cannot be
investigated the specificity of functional loss following stroke publicly archived. Data can be accessed through contact of the
regarding both the detection and discrimination of stimuli corresponding author ([email protected]). Data will be
defined by contrasts in luminance, wavelength, line orienta- released subsequent to requestors meeting the following
tion, or motion direction. Having tested more than one hun- conditions: approval of an ethics committee; pledge of se-
dred patients (Kraft et al., 2014) with anatomical lesions after crecy. Participants.
occipital, occipitotemporal, or occipito-parietal infarction, we In this study psychophysical data of 51 patients are pre-
found 51 patients whose central ten degrees of their visual sented, a subgroup of the 128 patients included in the paper of
fields were intact. Analysis of their behavioural (psycho- Kraft et al. (2014). We report how we determined our sample
physical) results collected at least two months after stroke is size, all data exclusions, all inclusion/exclusion criteria,
 c o r t e x 1 3 4 ( 2 0 2 1 ) 2 0 7 e2 2 2 209

whether inclusion/exclusion criteria were established prior to min were presented additionally in the remaining visual field
data analysis, all manipulations, and all measures in the quadrants. The midpoints of stimuli were placed at an ec-
study. Patients were chosen based on the site of lesion ac- centricity of 5
(deg) from the central fixation point. In both
cording to the following criteria: unilateral lesion of the oc- conditions the subject’s task was to indicate the location of
cipital and/or temporal and/or parietal cortex; lesion onset the circle via a button press (4-alternative-forced-choice task;
older than two months; no aphasia; no neglect (tested by three 4 AFC). The subject’s response initiated the next trial after a
paper and pencil tests); no dementia; no visual field defects delay of 500 msec.
within the central 10
in standard perimetry; no psychiatric or For both conditions (localisation based on detection or else
ophthalmological disorders. In addition, luminance contrast (form) discrimination) perceptual thresholds (62.5% correct
detection in the target quadrant had to be within normal responses) were defined in each experimental run for each
limits. Patients were tested between 2 and 12 months after the visual field quadrant using the adaptive staircase procedure
stroke, i.e., in a ‘chronic’ state after visual reorganization QUEST (Quick Estimation by Sequential Testing; Watson &
processes had time to restore function (Thiel & Kolmel, 1991). Pelli, 1983) yielding separate threshold values for each quad-
Controls (N ¼ 61) were included if they reported no neuro- rant. After a short training with some clearly suprathreshold
logical, psychiatric, or ophthalmological disturbances. All presentations the sequence of the four independent staircases
subjects had normal or corrected to normal visual acuity. For was organized in randomized order within each experimental
demographical data of patients and controls see Table 1. run. Subjects completed 30 trials per visual field quadrant, i.e.,
120 trials per run. Each visual submodality (luminance,
2.2. Stimuli, task and procedure texture, motion, and colour) and task (shape localisation
based on detection vs form discrimination) was tested in a
The stimuli, task, and procedure are illustrated in Fig. 1. separate run resulting in 8 experimental runs. The sequence
Stimulus details were already described in Kraft et al. (2010). of tasks was held constant across subjects. Subjects first per-
Stimuli were displayed on a 21” CRT monitor with a spatial formed the shape localisation tasks based on detection in the
resolution of 1600  1200 pixels and a refresh rate of 75 Hz order luminance, texture, motion, and colour. Subsequently
controlled by a PC. A software programme developed in-house the shape localisation tasks based on form discrimination
served to present stimulus displays and to collect perfor- were conducted in the same order.
mance data. Subjects were seated 60 cm from the screen. To In a 4AFC task the theoretical probability of guessing for
minimize head movements and to ensure a constant viewing each response is 25%. A response bias in favour of one visual
distance the head was stabilized by a chin rest and brow bar. field quadrant could mimic a lower threshold. Therefore, we
Participants were instructed to fixate a central fixation point controlled the distribution of button presses over the four
(diameter 12 arcmin) presented during all experiments. quadrants for each subject in every testing run eliminating
All experimental tasks were performed binocularly. During strong response biases.
each trial the stimulus array was presented for only 200 msec
(Fig. 1). The short presentation time prevented artefacts from 2.3. Submodality-specific stimuli
scanning eye movements. For the detection task a single circle
with a diameter of 210 arc min was presented in one of the For the submodality luminance 20 000 white dots (maximal
four visual field quadrants in pseudorandom order. For the luminance, 108 cd/m2) with a diameter of 5.6 arcmin each
discrimination task based on form discrimination between were presented against a grey background (54 cd/m2). The
circle and square, three squares with a side length of 186 arc difference between white dots and background was defined as
100% luminance contrast and served as the starting point for
the adaptive staircase procedure. QUEST modulated the dif-
Table 1 e Medical and demographic data of patients and ference between target and background in percent luminance
controls. difference.
For the submodality texture 20 arcmin long and 1.4 arcmin
Patients Controls
wide lines were presented on a virtual grid with an inter-line
N 51 61 distance of 14 arcmin, randomly jittered by up to 2 arcmin.
Age Mean ± SD in years 59.2 ± 12.1 49.3 ± 16.8 Background rotation of line elements was 45 deg. Starting
Range 20e76 21e79
orientation of target lines was 135 deg, resulting in a target-
Gender Male 31 60.8% 32 52.5%
background difference of 90 deg. QUEST modulated the
Female 20 39.2% 29 47.5%
Handiness Right 46 90.2% 55 90.2% orientation difference between target lines versus background
Left 3 05.9% 4 06.6% lines.
unknown 2 03.9% 2 03.3% For the submodality motion 20 000 black dots (5.6 arcmin,
N % z 3 cd/m2) moving at a velocity of 3 deg/s were presented on a
grey background (54 cd/m2). Background dots moved contin-
Time since lesion 2e6 months 21 41.2%
6e12 months 13 25.5%
uously to the right whereas the target dots moved to the left,
12 months 17 33.3% hence motion direction difference was 180 at the beginning of
Hemisphere Left 26 51.0% the staircase procedure. QUEST modulated the difference be-
Right 25 49.0% tween target and background motion directions.
Relation Calcarina Above 26 51.0% For the submodality colour an Ishihara-like setup was
Below 25 49.0%
created. Dots were presented on a virtual grid with an inter-
210 c o r t e x 1 3 4 ( 2 0 2 1 ) 2 0 7 e2 2 2

Fig. 1 e A Temporal sequence of task. B Stimuli used. They were defined by differences in luminance, colour, orientation, or
motion. In the detection task a circle was presented in one of the four visual field quadrants. For the discrimination task three
squares were presented additionally to the circle in the remaining visual field quadrants. Subject’s task was to indicate the
location of the circle via a button press (4-alternative-forced-choice task; 4 AFC). The subject’s response initiated the next
trial after a delay of 500 msec.
 c o r t e x 1 3 4 ( 2 0 2 1 ) 2 0 7 e2 2 2 211

dot distance of 14 arcmin jittered with a Gaussian distribution (Qbr) which represented the ‘average’ quadrant for compari-
of 1.5 arcmin resulting in a dot radius between 4 and 10 arcmin sons between healthy controls and the patient group.
(on average around 7 arcmin) and starting point for QUEST
was 650 nm (corresponding to red; Minolta Color Analyzer CA- 2.7. Lesion mapping
100RT). To avoid discrimination between target and back-
ground on the basis of luminance differences random lumi- Details of image acquisition are described in the paper of Kraft
nance noise (between 0% and 40% of maximum luminance) et al. (2014). Patients’ T2 weighted images served as the basis
was introduced to each stimulus dot. QUEST modulated the for lesion delineation because they offered the best contrast
difference between target and background colour hues. for subacute brain lesions. Only in one patient CT scans were
used because MRI’s were not available. Lesions were manually
2.4. Data analysis drawn onto the 24 slices of the T2-weighted MRI scan using
MRIcron (http://www.cabiatl.com/mrico/mricon/stats.html).
Controls were divided into three age groups: 20e39 yrs, Accuracy of lesion delineation was inspected visually at each
40e59 yrs., and 60þ yrs. of about equal size. Individual slice by comparing the lesion to the corresponding diffusion
patient’s results were compared to the corresponding age weighted images. Each lesion was spatially coregistered and
group. normalized to the FLAIR template (n ¼ 366; Winkler AM,
Kochunov P, Glahn DC; Available at http://brainder.org) using
2.5. Logarithmization, normalization, and statistics the Clinical Toolbox of SPM5 (Rorden, Bonilha, Fridriksson,
Bender, & Karnath, 2012) resulting in 51 lesion volumes (Voi-
As the expected psychophysical response distributions espe- volume of interest). Lesions in the right hemisphere were
cially for contrast and motion vision follow a logarithmic flipped to the left to increase statistical power. In a first step
characteristic, we logarithmized all results of controls and maps individual ROIs were combined to generate lesion
patients. overlap maps and subtraction maps. To further relate lesions
In addition, in order to correct for age we normalized each and behavioural data we used the voxel-based lesion-symp-
individual threshold by the following equation: tom mapping (VLSM) approach of the MRICron Software
package (Rorden et al., 2007). The binarized psychophysical
thresholdindividual  mean thresholdagematched controls scores of the target quadrant QI of all 51 patients were used for
Thresholdnorm ¼
SDagematched controls calculation separately for each modality (detection and
discrimination of texture, motion, and colour as well as
The mean thresholds of the age matched controls are discrimination of luminance, each as a single predictor). By
defined as the mean of the four quadrants of the visual field. means of the Liebermeister test, uncorrected z values for each
An individual normalized threshold represents the number of submodality resulted in seven statistical maps. Voxels
standard deviations (SD) from the age mean. We define more damaged in less than 15% of patients were ignored. The crit-
than three SD’s above the mean of controls as pathological. ical cut-off z values for p ¼ .05 were calculated after correction
All statistical data analyses were carried out with SPSS for multiple comparisons by using false discovery thresh-
software (Version 23). For each visual submodality correlation olding as implemented in the software package. Statistical
analyses (Spearman Rho rank order) were conducted between maps of significant voxels (p < .05) were overlaid onto the AAL
shape localisation based on detection and form discrimina- atlas brain (Tzourio-Mazoyer et al., 2002) for visualization and
tion using the individual threshold values of each subject and descriptive statistics calculated to indicate the number of
visual field quadrant. significant voxels in the different anatomical areas. Please
note, that all the lesions were restricted to the posterior part of
2.6. Topographical sequencing the brain because of our selection criteria including only le-
sions in “visual areas”. In addition we did not control for lesion
We first defined for each patient the visual field quadrant size. This means that the results are to be judged with care.
expected to be most affected based on the position of the
lesion in the MRI/CT scan. Depending on the side and whether
the lesion was above or below the calcarine fissure, we chose 3. Results
the contra-lesional visual field and either the lower or else
upper (contra-lesional) quadrant of the visual field. This 3.1. Behavioral data
quadrant was considered the target quadrant (QI). Its com-
panion on the same (contra-lesional) side was QII since we We tested the perception ability of both stroke patients and
expected deficits to spread on the same cortical hemisphere controls for four submodalities of vision, both for detection
more than to the opposite side. The quadrant mirror- and form discrimination, based on a) luminance contrast; b)
symmetrical to QI was defined as QIII since it is connected differences in texture; c) differences in motion direction; d)
to QI via callosal fibres. The quadrant least expected to show differences in wave length composition (‘colour’).
deficits in visual performance was defined as QIV. In cases
where the lesion extended both above and below the calcarine 3.2. General effects
sulcus, we chose the more lesioned portion of the hemisphere.
All four visual quadrants of the healthy controls yielded Mean thresholds for the form discrimination tasks are highly
roughly similar results. We chose the bottom right quadrant significantly lower than discrimination thresholds (values are
212 c o r t e x 1 3 4 ( 2 0 2 1 ) 2 0 7 e2 2 2

listed in Supplementary Table 1). Thresholds in controls in- The total number of pathological results is clearly higher
crease as a function of age, except for colour. We find that 7 of for the patients as compared to the normal controls. This is
our 61 controls yield performance three SD’s above the mean also true for the other quadrants QII- IV (see Supplementary
for one submodality in the right lower quadrant (Fig. 2, left Fig. 1-3). There are no pathological results for the luminance
side; the other quadrants yield similar results, not shown). detection in this quadrant because this was one of our
Results more than three SD’s above the mean of controls are exclusion criteria (see 2.2). Form discrimination yields more
defined as pathological both in controls and patients. pathological results than detection. For example concerning
The individual results of the 51 patients included in our discrimination, 41% of patients are disturbed in one or more
study are presented as deviations from the results of the submodalities as compared to 8% of controls, hence 92% of
corresponding task of normal observers for the target quad- controls have “0” pathological result in any submodality (Fig. 3
rant I in Fig. 2 right side (see Supplementary Fig. 1-3 for the right part “Discrimination”).
results of the other quadrants). Fig. 2 shows that we did Figs. 2 and 3 demonstrate that deficits of visual perception
choose relevant tests: Almost half of patients yield patholog- even without visual field defects are a common symptom after
ical results in at least one test and no patient fails all subtests strokes in visual cortical areas. While around 90% of controls
indicating that all patients understood the task. Except for have normal performance in all tests, in patients 22% (detec-
luminance detection (caused by ‘elimination’ of pathological tion) and 28% (discrimination) yield pathological results in one
results as outlined above), we find at least one patient with subtest and further 6% (detection) and almost 14% of patients
pathological results for each of our subtests. (discrimination) show deficits in more than one subtest.

Fig. 2 e Individual results of controls (N ¼ 61) and patients (N ¼ 51). Left two columns: Normalized data of all controls in the
right lower quadrant for detection (left column) and discrimination tasks (right column) Right two columns: Normalized data
of all patients in the contralesional quadrant (¼ target quadrant I), for the other quadrants see Supplementary Fig. 1-3;
green: normal range, red: normalized threshold more than three standard deviations above the means of controls, grey:
data missing.
 c o r t e x 1 3 4 ( 2 0 2 1 ) 2 0 7 e2 2 2 213

3.3.2. Texture (orientation contrast)

The significant decrease of patient’s detection of orientation
differences in QI is accompanied by a decrease of performance
in the remaining (even ipsilesional) quadrants (Fig. 4B). Still,
the loss of performance is significant only in the contralesional
hemifield. The results on form discrimination based on orien-
tation differences follow a very similar pattern, with a highly
significant loss in QI and less pronounced losses in QII and non-
significant losses in the ipsilesional quadrants (Fig. 4F).

3.3.3. Motion (motion direction)

As in the previous submodalities, results in the expected
quadrant QI are decreased more so for discrimination than for
detection (Fig. 4C, G). This is true in comparison with both the
controls and the ipsilesional quadrants e with the latter
showing almost normal performance. Performance is signifi-
cantly impaired only for the discrimination task.
Fig. 3 e Percentage of pathological results of patients (red)
and controls (grey). Percentage of results in the 3.3.4. Colour (‘wavelength contrast’)
contralesional quadrant (I, patients) or right lower In colourebased contour detection and form discrimination
quadrant (controls). Abscissa indicates the number of patients show a significant decrease of performance
submodalities with pathological results (>3SD) in either expressed as an increase in thresholds in the expected
no, one, or else more than one submodality. Hence, more quadrant (QI), and, surprisingly, in the second contralesional
than 90% of controls have no pathological result (“0”) in quadrant (QII). This holds true both in comparison to the
any of the Submodalities and none has pathological results ipsilesional quadrants and in comparison, to the results of
in more than 1 submodality. healthy controls. The deficits are comparable for detection
and discrimination (Fig. 4D, H).

3.3. Detection versus discrimination 3.4. Correlations between submodalities

Fig. 2 shows a double dissociation between detection and The rank orders obtained for each control subject between re-
discrimination in each submodality, with several patients sults for the different submodalities show only weak correla-
yielding pathological results for discrimination while normal tions (with two exceptions) for detection and discrimination
results for detection or, more important, the other way round. (Fig. 5 A, B, grey colour). This is to say that there exists only a
The average results of the 51 patients with free visual fields relatively low tendency in normal subjects to be a gifted ‘viewer’
for all four submodalities, both for detection and discrimina- in general but that good results in one submodality are not a very
tion in all four visual field quadrants are shown in Fig. 4. Re- good indicator for good performance in other submodalities
sults are expressed as standard deviations above (or rarely except for motion-based tests. In patients the correlations be-
below) those of the age matched controls. As expected, the tween detection modules are even weaker. Correlation co-
means are always lower, i.e., better in the ipsilesional quad- efficients are-with one exception-far more random than in
rants (QIII, QIV) as compared to the contralesional quadrants controls indicating further ‘disintegration’ between sub-
(QI, QII) except for luminance. Except for luminance all modalities caused by the lesion (Fig. 5A, orange colour). For
discrimination results in QI and II differ significantly from zero, discrimination, however (Fig. 5B, orange colour), the opposite
which is the mean level of the controls. Detection in QI and II holds true, meaning that a deficit in any of the submodalities of
deviate significantly from zero only for texture and colour, not form discrimination indicates a tendency for discrimination in
for motion (see Supplementary Fig. 4-7 for distributions of another submodality to be impaired with three out of six
patients and controls). possible correlations being significant on the .01% level.

3.3.1. Luminance (luminance contrast) 3.5. Correlations between hemispheres and between
Testing of the visual field in static and kinetic perimetry is detection and discrimination tasks
based on detection of luminance differences in the visual field.
This task is similar to the detection of luminance contrast in Mean correlations between target QI from the visual field of
our test. We excluded all patients showing deficits in either the lesioned hemisphere and its mirror-symmetrical QIII
perimetry or luminance detection to ensure intact visual fields representing the ‘healthy’ visual field are highly significant
(Fig. 4A). both for patients and for controls (Fig. 5C, D). We find sig-
We were less sure what to expect for the results on form nificant correlations between both quadrants for each and
discrimination, i.e., finding the circle among squares. Perfor- every of the tests for controls and with one exception for
mance is slightly below the mean of healthy observers in the patients. This is to say that while both patients and controls
contralesional quadrants, but not significantly changed show weak correlations between the results in different
(Fig. 4E). submodules (see Fig. 5A, B), they do have stable correlations
214 c o r t e x 1 3 4 ( 2 0 2 1 ) 2 0 7 e2 2 2

Fig. 4 e AeH Mean performance and standard error of patients (N ¼ 51) for all submodalities; A-D detection tasks and E-H
discrimination tasks. Abscissa indicates the quadrant tested according to the topographical sequencing (see methods);
ordinate indicates normalized threshold in standard deviations relative the results of age-matched controls. Asterisks
indicate means differing significantly from zero as revealed by a t-test (uncorrected); *p < .05; **p < .01. Involvement of the
ipsilesional visual field (III, IV) varies somewhat but not significantly between submodalities.

within each submodule between the right and left hemi- occipital regions (Fig. 6). In 26 of the 51 patients the left
sphere represented by the quadrants QI and QIII and there- hemisphere is affected but to increase statistical power right
fore between the lesioned and intact hemispheres (of lesions are flipped to the other side. Patients with bilateral
patients). Correlations for the entire hemifields conform to lesions were a priori excluded from the study except for one
the results of the quadrants mentioned above (data not patient with a very small lesion on the opposite side or in
shown). You may be good at motion detection and discrimi- unrelated portions of the opposite cortex (n ¼ 2) and especially
nation while not for wavelengths, but if you are good at the cerebellum (4 patients). Twenty-six patients (15 have an
motion detection in your right visual field, you are also good original left lesion) have a pathological score (þ3 SDs) in at
in your left visual field weaker in the patients while still sig- least one submodality in the target quadrant I (Fig. 2) and are
nificant except for colour. in the following labelled “PS patients”. We first compared the
Correlations between the results for detection and anatomical distribution of lesions of the 26 PS patients with
discrimination within the same submodality exist in controls those of the 25 patients with normal scores, called “NS pa-
for luminance and to a lesser degree for colour (Fig. 5 E). In tients”. The lesion overlap of the normalized imaging results
patients the correlation between the results for detection and of 25 patients without any pathological scores in the visual
discrimination is significant only for texture and less so for tests as displayed in Fig. 6A and Fig. 6B shows the lesion
luminance. It is important here that stimuli for discrimination overlap of the remaining 26 patients with pathological scores
are presented far above thresholds for detection; hence even irrespective of submodality (a subtraction plot is presented in
an impaired detection system might detect the stimuli and the Supplementary Fig. 10). While there is hardly any overlap
hence allow discrimination. in the NS patients, we find an area of substantial overlap in the
Scatter plots of the data used for correlation analysis PS patients located in the posterior third of the fusiform gyrus
including linear regression lines are presented in the extending into the lingual gyrus.
Supplementary Figs. 8A and B and 9 to illustrate the distri- To better characterize this area of overlap we performed a
bution of individual results and to enable the comparison of binary voxel-based lesion-symptom mapping analysis (VLSM)
thresholds of patients and controls. of each submodality as a single predictor, resulting in seven
statistical maps (three for detection; four for discrimination).
3.6. Imaging results Three out of the seven maps revealed a significant link be-
tween lesioned voxels and pathological perception, namely
Stroke lesions of the 51 patients included in this study are for detection and discrimination of texture as well as the
distributed over a wide range of temporal, parietal, and detection of colour (Table 2). This is to say that we find voxels
 c o r t e x 1 3 4 ( 2 0 2 1 ) 2 0 7 e2 2 2 215

Fig. 5 e AeE Spearman Rho rank order correlations in patients (red) and controls (grey). A, B Correlations between
submodalities for detection (A) or discrimination (B) in the contralesional quadrant for patients and the right lower quadrant
for controls; numbers in the right upper part indicate the corresponding absolute p-values; C,D Correlations between the
ipsilesional quadrant and the contralesional quadrant for patients and left lower quadrant versus right lower quadrant in
controls of each submodality for detection (C) and discrimination (D); E Correlations between detection and discrimination
tasks of the same submodality in the ipsilesional quadrant for patients and the right lower quadrant for controls. Numbers
in bold font indicate significant results (p < .01).
216 c o r t e x 1 3 4 ( 2 0 2 1 ) 2 0 7 e2 2 2

Fig. 6 e Overlay lesion plots A) of the patients with a normal behavioral score (NS; n ¼ 25) and B) of the patients with a
pathological score irrespective of submodality (PS; n ¼ 26). Colour code represents the number of overlapping lesions from
pink (n ¼ 1) to red (n ¼ 25 or 26). MNI Z-coordinates are indicated below each of the nine horizontal sections. The upper
three squares show the overlap regions in higher detail, they have a different colour code from pink (n ¼ 1) to red (n ≥ 8) and
mark the region almost exclusively involved in PS patients, at the border area between the lingual and fusiform gyri.

Table 2 e Results of the VLSM analysis. Z-values (uncorrected and cutoff z values after false discovery thresholding of the
Liebermeister test for the three submodalities with significant results including the number of patients (affected patients)
used for calculation The complete results for the remaining submodalities not reaching significance level are listed in the
Supplementary Table 2.

Submodality Range Cutoffa N (affected) Center of massb

X Y Z
Detection Texture 4,062 1,882 48 (10) 24,90 68,01 7,64
Discrimination Texture 3,019 2,195 48 (11) 23.80 71.01 6.73
Detection Colour 3,808 1,766 36 (7) 23.42 69.81 7.11
a
FDR p < .05.
b
MNI coordinates.

whose lesion is significantly correlated with a specific visual discrimination the least (TexDis 829). The distribution and
deficit. extend of significant voxels (based on the AAL Atlas of MRi-
The overlay of significant voxels of these three maps is cron) for these three maps is listed in Table 3. All three maps
shown in Fig. 7. There is only one patch of significant voxels reveal significant voxels in the border area between the
in these three modalities plotted for texture detection in the lingual and fusiform gyrus with a larger proportion in the
first row, for texture discrimination in the second row, and lingual gyrus.
colour detection in the last row. The location of this patch Since pathological scores for both texture detection and
does not vary much between these three modalities. Colour discrimination yield significant voxels, we further evaluated
detection has the greatest number of significant voxel (ColDet lesion locations for the subgroup of patients with any deficit in
3561), texture detection fewer (TexDet 1734), and texture texture processing by overlaying lesions. Four patients score
 c o r t e x 1 3 4 ( 2 0 2 1 ) 2 0 7 e2 2 2 217

Fig. 7 e Plots of the significant voxels (p < .05) of the voxel based statistical analysis for modalities texture detection, texture
discrimination, and colour detection from top to bottom. Colours code the z-values corrected for multiple comparisons using
the false discovery rate. Significant voxels do not differ much in location between these modalities.

Table 3 e Distribution of significant voxels in the AAL atlas brain. Numbers of significant voxels (p < .05) in the left lingual
and fusiform gyrus including the individual z-scores and center of mass coordinates for the three submodalities TexDet,
TexDis and ColDet. Significant voxels that did cover less than .1% of an area (rest of brain; cerebellum; calcarine fissure and
surrounding cortex, middle and inferior occipital lobes) are not listed.

Area TexDet TexDis ColDet

N voxel X Y Z z N voxel X Y Z z N voxel X Y Z z
Total 1734 829 3561
Lingual 865 25 77 12 4.1 504 29 65 3 3 2013 20 80 12 3.8
Fusiform 788 25 75 13 4.1 279 27 74 6 3 1356 24 74 13 3.8

pathologically in both texture detection and discrimination up individual thresholds (three for detection and four for
and their summary overlay is shown in the upper panel of discrimination in the target quadrant (QI) compared to the
Fig. 8. The subtraction analysis of patients with isolated individual companion contralesional quadrant (QII). (The sum
pathological scores in either texture detection (n ¼ 6) or of the 26 deficit scores was 321.3 in Q I, 183.2 in Q II, 132.8 in Q
discrimination (n ¼ 7) is plotted in the lower panel of Fig. 8. It is III and 90.4 in Q IV for the sorting based on lesion site indi-
striking that the lesions of the four patients with a more cating that elevated perceptual thresholds were often not
general deficit in texture processing are strongly overlapping. restricted to a single quadrant and even affected the ipsile-
On the other hand, the subtraction plot in the lower panel sional side. We cannot exclude a small influence of neglect
indicates that the processing of texture detection lies more here in spite of the fact that we had excluded all patients with
posteriorly and therefore nearer to the primary visual cortex pathological results in paper and pencil tests). Eight of the 26
while the discrimination task is processed more anteriorly as patients (in contrast to expectation) performed worse in QII
expected from the known hierarchy of processing visual ob- than QI. Half of the 26 patients had their lesion above, the
jects in vision. other half below the calcarine fissure. Irrespective of lesion
Finally (in contrast to the topographical sequencing used site, nine patients performed worse in the upper contrale-
so far for the previous analysis of the data depending on lesion sional hemifield and 17 patients in the lower contralesional
location), we sorted the 26 patients with pathological scores hemifield. To that end, we calculated summary overlay plots
(PS patients) according to their perceptual deficit by summing of patient’s lesions based on whether the upper or else the
218 c o r t e x 1 3 4 ( 2 0 2 1 ) 2 0 7 e2 2 2

lower quadrant of their contralesional hemifield yielded most elevated perceptual thresholds. As can be seen in Fig. 9, lesion

Fig. 8 e Upper panel: Overlay summary plots of the four patients with pathological scores in both texture detection and
discrimination (n ¼ 4). Colour code represents the number of overlapping lesions from pink (n ¼ 1) to red (n ¼ 4). Lower
panel: Subtraction plot Texture Detection (n ¼ 6) minus Texture Discrimination (n ¼ 7). Colour coding indicates the
percentage of overlapping lesions, increasing from yellow to red (1e35%). These voxels are damaged more frequently in
patients with a pathological score in texture detection than in patients with a pathological score in texture discrimination.
Colour codes from green to blue (¡1 to ¡35%) indicate regions damaged more frequently in Texture Discrimination than in
Texture Detection. MNI Z-coordinates are indicated below each of the nine transverse sections.

Fig. 9 e Overlay plot of lesions of patients (PS patients; n ¼ 26) sorted according to their perceptual thresholds summed over
all tests. Lesions of patients with thresholds more strongly elevated in the upper contralesional hemifield (n ¼ 9) are shown
in the upper row, those of patients with dominant deficits in the lower hemifield (n ¼ 17) are overlaid in the lower row. The
lesions of the patients in the upper row tend to be more medially and in lower slices that the ones in the lower row. Colour
code represents the number of overlapping lesions from pink (n ¼ 1) to red (n ¼ 6).
 c o r t e x 1 3 4 ( 2 0 2 1 ) 2 0 7 e2 2 2 219

positions differed between those two groups of patients in the patient group. This finding indicates that there is no
indicating a topographical organization of “midlevel” visual significant “spill-over” of deficits in one submodality to other
cortical areas. submodalities-since otherwise correlations should increase
rather than decrease in patients.
Discrimination thresholds, on the other hand, are far closer
4. Discussion correlated in patients than in controls with (far) higher sig-
nificance levels in all cases (Fig. 5B). The increased correla-
We investigated the effects of strokes involving the occipital, tions we find in patients indicate that the mechanisms for
occipito-temporal and occipito-parietal parts of the brain on discrimination are incorporated at more closely related neural
detection and discrimination of visual forms defined by networks in the visual cortices than those for detection are. If
luminance, colour, motion, and texture and tested correla- this common system of form discrimination suffers a defect,
tions with the underlying cortical lesions. The results show form discrimination based on several submodalities is
that almost half of patients suffer from specific deficits un- impaired, introducing a correlation between the results for
detected by clinical tests in spite of free visual fields. The different submodalities.
cortical lesions underlying these perceptual deficits involve
predominantly area hV4 and its surroundings. 4.2. Correlations between hemispheres and between
detection and discrimination
4.1. Correlations between deficits of different
submodalities of vision Normal subjects yield high correlations between results in
both hemifields for each individual submodality for both
The highly selective and varied pattern of pathological results detection and discrimination but show only minor correla-
(Fig. 2) indicates that patients did indeed understand the tasks tions between performances for different submodalities
and were able to perform within the normal range for those (Fig. 5C, D). In other words, good results in one hemifield for
submodalities not disturbed (Fahle, 2003; Kraft et al., 2014). any given submodality are usually associated with good re-
The fact that they had normal visual fields assures that the sults in the other hemifield for the same submodality (but not
optic tract and visual areas V1, V2, V3 were intact since lesions necessarily for others). The results of patients show some-
there produce scotoma (Horton & Hoyt, 1991; Inouye, 1909). what lower correlations between the two hemifields, espe-
Deficits we found do not produce very pronounced symptoms cially for colour discrimination (Fig. 5C, D). This finding
subjectively since they involve the contralesional hemifield reflects the impact of the lesion that slightly decreases the
and not all submodalities. Moreover, our tests primarily correlation between hemispheres present in normal controls.
concern the ventral stream (Merigan & Maunsell, 1993). Finally, correlations between the results for detection and
Deficits appear in all four submodalities tested most often discrimination within each submodality reach significance in
for texture and colour and various types of combinations be- normal controls only for luminance (and almost for colour)
tween the deficits in detection and discrimination exist. There differences while for line orientation (texture) in patients
are patients with elevated thresholds in just one submodality (Fig. 5E). We have argued above that discrimination and
and others with two and more indicating the existence of detection rely indeed on partly different neuronal mecha-
(partly) separated neuronal networks. nisms, with clearly differing thresholds, so one does not have
We find patients suffering exclusively from problems in to expect the same high correlations between detection and
detecting forms while there are others who demonstrate only discrimination as between hemifields, and this is what we
elevated thresholds for discriminating forms demonstrating a find. Still, given the fact that we test correlations between two
double dissociation between form detection and discrimina- types of thresholds of the same submodality, a certain
tion (Fig. 2). (Of course there are also patients who suffer from amount of correlation is not surprising.
problems with both detection and discrimination). Please note Our suggestion of ‘early’ detection systems that are more
that the stimulus intensities for the detection task are much separated from each other than the ‘later’ systems’ discrimi-
higher than those for the discrimination task, obviously nating between forms makes a testable prediction. Namely,
allowing discrimination even with deficits of the detection the number of ‘defective’ results should be higher for
mechanism. discrimination than for detection tasks (Fig. 2). This is indeed
Detection thresholds in healthy controls correlate signifi- what we find and while a number of explanations are possible,
cantly on the p < .01 level only between those for luminance it is reassuring that the data are compatible with our sugges-
and motion (Fig. 5A). Detection thresholds for patients are tion (Baizer et al., 1991; Tsotsos et al., 2008). We will discuss
worse and correlate hardly at all between submodalities with this further in the section on imaging data.
p-values (far) less significant than those for controls (in five
out of six cases). This finding points to at least partly separate 4.3. Interpretation of imaging results
neural mechanisms underlying the detection of differences in
luminance, wavelength, motion, and line orientation that can We complemented our perceptual tests with a correlation
be individually ‘disturbed’ thereby decreasing correlations between the deficits and the location of patients’ cortical le-
below the levels found in controls. It is hardly surprising that sions as detected by (MRT) imaging. The underlying hypoth-
deficits in the detection of luminance contrast bear conse- esis was that there would be differences in lesions’ locations
quences for the detection of motion, colour and texture between deficits in different submodalities and between def-
boundaries (p < .05) but these correlations are completely lost icits in detection versus discrimination.
220 c o r t e x 1 3 4 ( 2 0 2 1 ) 2 0 7 e2 2 2

An area located in the posterior third of the elongated single case studies of strokes in V4 (Gallant, Shoup, & Mazer,
fusiform gyrus and extending into the lingual gyrus is pre- 2000; Rizzo, Nawrot, Blake, & Damasio, 1992) support our
dominantly lesioned in patients that score pathologically in view of V4 as an area important for colour vision and pattern
any submodality-specific test as compared to patients scoring processing.
within the normal range (overlay plot Fig. 6 and subtraction The lack of a “significant” area of overlap for impaired
plot Suppl. Fig. 10). Maximally eight of the 26 lesions of pa- motion discrimination may indicate a rather spread out
tients with a pathological score overlap. From there lesions network for form from motion (Gilaie-Dotan et al., 2013).
extend mainly along the course of the gyrus well in line with Since impairments in texture detection and texture
the assumption of neighboring but partly separate networks discrimination both provided maps of significant voxels it was
for different submodalities and discrimination versus possible to use subtraction analysis for these patients (Fig. 8
detection. below). The results show that an impaired detection of orien-
The voxel-based statistical analysis (VLSM) of each sub- tation differences (texture) is associated with lesions located
modality as a single predictor yields significant voxels in this more posteriorly than lesions causing an impaired discrimi-
region of maximal overlap for patients with pathological nation of form from texture. This difference in cortical lesion
perception in texture detection, texture discrimination, and sites is the basis for the fact that some patients suffer from
colour detection. The other correlations between perceptual deficits of texture discrimination only while others from se-
and structural deficits (luminance discrimination, motion lective deficits of texture detection. This implies that in the
detection and discrimination, colour discrimination) fail to patients with impaired discrimination of texture the cortical
reach significance as well as an exploratory analysis using area responsible for the feature selection of texture detection
continuous data. One reason for the lack of significance could was functional and lying nearer to the posterior pole. The le-
be the small number of patients showing a perceptual deficit sions of the four patients affected in both detection and
in a single submodality as there was just one patient scoring discrimination all overlapped at the border between the
pathologically in motion detection. The significant voxel areas lingual and fusiform gyri mentioned above (Fig. 8 above).
of the groups with impaired texture detection and texture
discrimination do not differ much. In contrast to healthy 4.4. Conclusions
controls patients show a significant correlation between def-
icits of texture discrimination and detection (Fig. 5 E). This We would like to stress that almost half of patients suffering
indicates neighboring neuronal networks for texture pro- from strokes of visual cortical areas show highly significant
cessing, in line with the behavioral results. deficits of one or several visual submodalities (Fig. 2), even in
The coordinates in MNI space of the center of the signifi- the absence of visual field defects or other clinical symptoms.
cant three maps mentioned above, namely texture detection, These deficits involve the part of the visual field expected on
texture discrimination and colour detection, conform to the the basis of the lesions’ topography (Fig. 4) and may well
location of human visual cortex area V4 (hV4)1 (Arcaro, impair everyday visual performance in subtle ways and that
McMains, Singer, & Kastner, 2009; Brewer, Liu, Wade, & the patients are not fully aware of. Although we chose the
Wandell, 2005). This area lies medially to face selective areas behavioural results of the expected contralesional quadrant
and posteriorly to place selective areas. Area hV4 borders for the voxel-based lesion-symptom mapping (VLSM)
anteriorly to the ventral occipital area (VO1) which is part of approach it is obvious from our data that often patient’s re-
the ventral temporal cortex (VTC). However the anatomical sults were affected even in the “intact” hemifield when
borders, and the retinotopical and functional organization of compared to the controls. Two factors might contribute. First,
hV4 are still under debate (Winawer & Witthoft, 2015). Ac- a general deficit of visual processing; however, the fact that
cording to the model of Brewer et al. (2005) it represents the most of our patients were capable to solve even more complex
entire contralateral visual hemifield. tasks such as discriminating between male and female faces
While earlier functional MRI studies on humans consid- (results not shown) argues against this possibility. The second
ered V4 primarily to be a colour area (Zeki et al., 1991) newer possible explanation is that on the level of hV4 a certain
studies indicate that hV4 is involved in the encoding of amount of bilateral processing takes place. Hence, a stroke
texture, form and surfaces (Dumoulin & Hess, 2007; Konen & involving one side may also affect processing of the ipsile-
Kastner, 2008). The role of visual area V4 in object percep- sional visual field for pattern recognition while not for lumi-
tion is not fully understood. Based mainly on monkey studies nance detection (since the latter is achieved in the strictly
it is considered as a mid-tier area of vision facilitating figure- contralaterally connected V1). It is interesting in this context,
ground segmentation (see Roe et al. (2012), for a review). that indeed results for the mirror-symmetrical quadrant (Q III)
Studies on human V4 systematically comparing responses to are clearly worse than those for the other quadrant on the
multiple feature spaces are still lacking. The finding that the intact side (Q IV) see page 21.
functional organization for the attributes of colour, size, and Patient’s detection thresholds correlate very weakly be-
orientation is not highly segregated in macaque V4 (Ghose & tween submodalities. Thresholds for (most) discriminations,
Ts’o, 2017) may explain our results of largely congruent sig- on the other hand, are significantly correlated indicating
nificant areas of the VLSM analysis for texture detection, partly shared mechanisms for even simple form discrimina-
texture discrimination, and colour detection. In addition a few tion. Moreover, we do find a double dissociation between defi-
cits in detection versus discrimination in the same
1
Coordinates given in Tailarach space were transformed into submodality in several patients indicating separate neural
MNI space based on the formula of Lancaster et al. (2007). mechanisms for detection versus discrimination.
 c o r t e x 1 3 4 ( 2 0 2 1 ) 2 0 7 e2 2 2 221

The imaging results are compatible with this view, Baldo, J. V., Kacinik, N., Ludy, C., Paulraj, S., Moncrief, A., Piai, V.,
showing different areas of overlap between the deficits of et al. (2018). Voxel-based lesion analysis of brain regions
patients suffering from problems with texture detection underlying reading and writing. Neuropsychologia, 115, 51e59.
Bartolomeo, P., Bachoud-Levi, A. C., & Thiebaut de Schotten, M.
versus texture discrimination.
(2014). The anatomy of cerebral achromatopsia: A
We interpret these findings as indicating that visual reappraisal and comparison of two case reports. Cortex; a
perception relies on a multi-layered neuronal network with Journal Devoted to the Study of the Nervous System and Behavior,
strong feedback connections (Herzog & Fahle, 1998). Hence, 56, 138e144.
terms such as ‘disturbance of colour vision’ are too vague. Bates, E., Wilson, S. M., Saygin, A. P., Dick, F., Sereno, M. I.,
Given that processing of submodalities such as colour in- Knight, R. T., et al. (2003). Voxel-based lesion-symptom
corporates several separate levels, realized in different mapping. Nature Neuroscience, 6(5), 448e450.
Beume, L. A., Martin, M., Kaller, C. P., Kloppel, S., Schmidt, C. S.,
cortical networks, a more precise clarification would be
Urbach, H., et al. (2017). Visual neglect after left-hemispheric
desirable regarding the level on which processing in the lesions: A voxel-based lesion-symptom mapping study in 121
network is disturbed. acute stroke patients. Experimental Brain Research, 235(1),
The high variation between patient’s results may in part rely 83e95.
on the effects of compensatory effects in the neuronal net- Brewer, A. A., Liu, J., Wade, A. R., & Wandell, B. A. (2005). Visual
works “disturbed” by the cortical lesion. These compensatory field maps and stimulus selectivity in human ventral occipital
cortex. Nature Neuroscience, 8(8), 1102e1109.
mechanisms may involve both other regions of the ipsilesional
Britten, K. H., Shadlen, M. N., Newsome, W. T., & Movshon, J. A.
network and (mirror-symmetrical) regions of the contralesional
(1993). Responses of neurons in macaque MT to stochastic
network. Especially the contralesional contributions may be of motion signals. Visual Neuroscience, 10(6), 1157e1169.
importance, given the fact, mentioned above, that we do find Dumoulin, S. O., & Hess, R. F. (2007). Cortical specialization for
clear signs in our data that even a strictly unilateral cortical concentric shape processing. Vision Research, 47(12),
lesion of hV4 often reduces performance for the ipsilesional 1608e1613.
visual field, indicating a partial bilateral processing of both vi- Fahle, M. (2003). Failures of visual analysis. In M. Fahle, &
M. Greenlee (Eds.), The neuropsychology of vision (p. 197). New
sual half fields on the level of hV4.
York: Oxford University Press.
Freiwald, W. A., & Tsao, D. Y. (2010). Functional
compartmentalization and viewpoint generalization within
Open practices the macaque face-processing system. Science (New York, N.Y.),
330(6005), 845e851.
The study in this article earned an Open Materials badge for Gallant, J. L., Shoup, R. E., & Mazer, J. A. (2000). A human
transparent practices. Materials for the study are available at extrastriate area functionally homologous to macaque V4.
Neuron, 27(2), 227e235.
https://doi.org/10.5281/zenodo.3479558.
Ghose, G. M., & Ts’o, D. Y. (2017). Integration of color, orientation,
and size functional domains in the ventral pathway.
Neurophotonics, 4(3), Article 031216.
Acknowledgements Gilaie-Dotan, S., Saygin, A. P., Lorenzi, L. J., Egan, R., Rees, G., &
Behrmann, M. (2013). The role of human ventral visual cortex
in motion perception. Brain : A Journal of Neurology, 136(Pt 9),
This work was supported by the German Research Foundation
2784e2798.
(BR 1691/5-1 and FA 119/17-1). The authors would like to thank Gruesser, O., & Landis, T. (1991). In O. Gruesser, & T. Landis (Eds.),
€ thner, M. Hanke and Y. Schaar for assistance
M. Sengutta, I. Ka Visual agnosias and other disturbances of visual perception and
in collecting the data, D. Trenner for supplying the computer cognition. Boca Raton: CRC Press.
program for assessing the data, and Lynn Schmittwilken for Herzog, M. H., & Fahle, M. (1998). Modeling perceptual learning:
help in data analysis and graphics. Difficulties and how they can be overcome. Biological
Cybernetics, 78(2), 107e117.
Horton, J. C., & Hoyt, W. F. (1991). Quadrantic visual field defects.
A hallmark of lesions in extrastriate (V2/V3) cortex. Brain : A
Supplementary data Journal of Neurology, 114(Pt 4), 1703e1718. Pt 4.
Inouye, T. (1909). Die Sehst€ orungen bei Schußverletzungen der
Supplementary data to this article can be found online at kortikalen Sehspha €re nach Beobachtungen an Verletzten der letzten
https://doi.org/10.1016/j.cortex.2020.06.006. japanischen Kriege. Leipzig: Engelmann.
Kandel, E. R., & Wurtz, R. H. (2000). Constructing the visual image.
In E. R. Kandel, J. H. Schwartz, & T. M. Jessel (Eds.), Principles of
references
neural science (4th ed., p. 492). New York: McGraw Hill
Professional.
Karnath, H. O., Rennig, J., Johannsen, L., & Rorden, C. (2011). The
Arcaro, M. J., McMains, S. A., Singer, B. D., & Kastner, S. (2009). anatomy underlying acute versus chronic spatial neglect: A
Retinotopic organization of human ventral visual cortex. The longitudinal study. Brain : A Journal of Neurology, 134(Pt 3),
Journal of Neuroscience : The Official Journal of the Society for 903e912.
Neuroscience, 29(34), 10638e10652. Konen, C. S., & Kastner, S. (2008). Two hierarchically organized
Baizer, J. S., Ungerleider, L. G., & Desimone, R. (1991). Organization neural systems for object information in human visual cortex.
of visual inputs to the inferior temporal and posterior parietal Nature Neuroscience, 11(2), 224e231.
cortex in macaques. The Journal of Neuroscience : The Official Kraft, A., Grimsen, C., Kehrer, S., Bahnemann, M., Spang, K.,
Journal of the Society for Neuroscience, 11(1), 168e190. Prass, M., et al. (2014). Neurological and neuropsychological
222 c o r t e x 1 3 4 ( 2 0 2 1 ) 2 0 7 e2 2 2

characteristics of occipital, occipito-temporal and occipito- distribution of the posterior cerebral artery. Neuro-
parietal infarction. Cortex; a Journal Devoted to the Study of the Ophthtalmology, 11(1), 33e38.
Nervous System and Behavior, 56, 38e50. Troscianko, T., Davidoff, J., Humphreys, G., Landis, T., Fahle, M.,
Kraft, A., Grimsen, C., Trenner, D., Kehrer, S., Lipfert, A., Greenlee, M., et al. (1996). Human colour discrimination based on
Kohnlein, M., et al. (2010). Specificity of fast perceptual a non-parvocellular pathway. Current Biology : CB, 6(2), 200e210.
learning in shape localisation tasks based on detection versus Tsotsos, J. K., Rodrı́guez-Sa nchez, A. J., Rothenstein, A. L., &
form discrimination. Vision Research, 50(4), 473e478. Simine, E. (2008). The different stages of visual recognition
Lancaster, J. L., Tordesillas-Gutierrez, D., Martinez, M., Salinas, F., need different attentional binding strategies. Brain Research,
Evans, A., Zilles, K., et al. (2007). Bias between MNI and 1225, 119e132.
talairach coordinates analyzed using the ICBM-152 brain Tzourio-Mazoyer, N., Landeau, B., Papathanassiou, D., Crivello, F.,
template. Human Brain Mapping, 28(11), 1194e1205. Etard, O., Delcroix, N., et al. (2002). Automated anatomical
Merigan, W. H., & Maunsell, J. H. (1993). How parallel are the primate labeling of activations in SPM using a macroscopic anatomical
visual pathways? Annual Review of Neuroscience, 16, 369e402. parcellation of the MNI MRI single-subject brain. Neuroimage,
Meyer, S., Kessner, S. S., Cheng, B., Bonstrup, M., Schulz, R., 15(1), 273e289.
Hummel, F. C., et al. (2015). Voxel-based lesion-symptom Vaina, L. M., Lemay, M., Bienfang, D. C., Choi, A. Y., &
mapping of stroke lesions underlying somatosensory deficits. Nakayama, K. (1990). Intact “biological motion” and
NeuroImage.Clinical, 10, 257e266. “structure from motion” perception in a patient with
Moeller, S., Freiwald, W. A., & Tsao, D. Y. (2008). Patches with impaired motion mechanisms: A case study. Visual
links: A unified system for processing faces in the macaque Neuroscience, 5(4), 353e369.
temporal lobe. Science (New York, N.Y.), 320(5881), 1355e1359. Van Essen, D. C., Anderson, C. H., & Felleman, D. J. (1992).
Rizzo, M., Nawrot, M., Blake, R., & Damasio, A. (1992). A human Information processing in the primate visual system: An
visual disorder resembling area V4 dysfunction in the integrated systems perspective. Science (New York, N.Y.),
monkey. Neurology, 42(6), 1175e1180. 255(5043), 419e423.
Roe, A. W., Chelazzi, L., Connor, C. E., Conway, B. R., Fujita, I., Van Essen, D. C., & Gallant, J. L. (1994). Neural mechanisms of
Gallant, J. L., et al. (2012). Toward a unified theory of visual form and motion processing in the primate visual system.
area V4. Neuron, 74(1), 12e29. Neuron, 13(1), 1e10.
Rorden, C., Karnath, H. O., & Bonilha, L. (2007). Improving lesion- Winawer, J., & Witthoft, N. (2015). Human V4 and ventral occipital
symptom mapping. Journal of Cognitive Neuroscience, 19(7), retinotopic maps. Visual Neuroscience, 32, E020.
1081e1088. Zeki, S. M. (1978). Functional specialisation in the visual cortex of
Rorden, C., Bonilha, L., Fridriksson, J., Bender, B., & Karnath, H. O. the rhesus monkey. Nature, 274(5670), 423e428.
(2012). Age-specific CT and MRI templates for spatial Zeki, S., Watson, J. D., Lueck, C. J., Friston, K. J., Kennard, C., &
normalization. Neuroimage, 61(4), 957e965. Frackowiak, R. S. (1991). A direct demonstration of functional
Rumelhart, D. E., McClelland, J. L., & the PDPResearchGroup. specialization in human visual cortex. The Journal of
(1986). Parallel distributed processing: Explorations in the Neuroscience : The Official Journal of the Society for Neuroscience,
microstructure of cognition. Cambridge, Mass: MIT Press. 11(3), 641e649.
Ruttiger, L., Braun, D. I., Gegenfurtner, K. R., Petersen, D., Zihl, J., von Cramon, D., & Mai, N. (1983). Selective disturbance of
Schonle, P., & Sharpe, L. T. (1999). Selective color constancy movement vision after bilateral brain damage. Brain, 106(2),
deficits after circumscribed unilateral brain lesions. The Journal 313e340.
of Neuroscience, 19(8), 3094e3106. Watson, A. B., & Pelli, D. G. (1983). QUEST: A bayesian adaptive
Thiel, K., & Kolmel, H. W. (1991). Pattern of recovery from psychometric method. Perception & Psychophysics, 33(2),
homonymous hemianopia subsequent to infarction in the 113e120.