Neuropsychologia 93 (2016) 301–311

Contents lists available at ScienceDirect

Neuropsychologia
journal homepage: www.elsevier.com/locate/neuropsychologia

Residual perception of biological motion in cortical blindness
a,⁎,1

a,1

a,1

b

a

Nicolas Ruﬃeux, Meike Ramon , Junpeng Lao , Françoise Colombo , Lisa Stacchi ,⁎François-Xavier Borruatc, Ettore Accollab,d, Jean-Marie Annonib,d, Roberto Caldaraa,

crossmarka

Eye and Brain Mapping Laboratory (iBMLab), Department of Psychology, University of Fribourg, Faucigny 2, 1700 Fribourg, Switzerland
Unit of Neuropsychology and Aphasiology, Fribourg Hospital, CP, 1708 Fribourg, Switzerland
Jules-Gonin Eye Hospital, University of Lausanne, Avenue de France 15, 1004 Lausanne, SwitzerlanddLaboratory for Cognitive and Neurological Sciences, Department of Medicine, University of Fribourg, Ch. du Musée 5, 1700 Fribourg, Switzerlandbc

A R T I C L E I N F O

A BS T RAC T

Keywords:
Cortical blindness
Biological motion
Residual visual ability
Striate damage
Task dependency
Eye tracking

From birth, the human visual system shows a remarkable sensitivity for perceiving biological motion. Thisvisual ability relies on a distributed network of brain regions and can be preserved even after damage of highlevel ventral visual areas. However, it remains unknown whether this critical biological skill can withstand theloss of vision following bilateral striate damage. To address this question, we tested the categorization of humanand animal biological motion in BC, a rare case of cortical blindness after anoxia-induced bilateral striate
damage. The severity of his impairment, encompassing various aspects of vision (i.e., color, shape, face, andobject recognition) and causing blind-like behavior, contrasts with a residual ability to process motion. We
presented BC with static or dynamic point-light displays (PLDs) of human or animal walkers. These stimuli were
presented either individually, or in pairs in two alternative forced choice (2AFC) tasks. When confronted withindividual PLDs, the patient was unable to categorize the stimuli, irrespective of whether they were static ordynamic. In the 2AFC task, BC exhibited appropriate eye movements towards diagnostic information, but
performed at chance level with static PLDs, in stark contrast to his ability to eﬃciently categorize dynamic
biological agents. This striking ability to categorize biological motion provided top-down information isimportant for at least two reasons. Firstly, it emphasizes the importance of assessing patients’ (visual) abilities
across a range of task constraints, which can reveal potential residual abilities that may in turn represent a key
feature for patient rehabilitation. Finally, our ﬁndings reinforce the view that the neural network processing
biological motion can eﬃciently operate despite severely impaired low-level vision, positing our natural
predisposition for processing dynamicity in biological agents as a robust feature of human vision.

1. Introduction

have often involved motion conveying stimuli. These studies indicate
that, generally, patients’ awareness ﬂuctuates and depends on nature ofstimuli, paradigms, and tasks used (e.g., Hervais-Adelman et al., 2015;
Weiskrantz et al., 1995; Zeki and Ffytche, 1998). For instance, GY
exhibited diﬀerent levels of awareness for non-identiﬁable visual input(Barbur et al., 1993; Weiskrantz et al., 1995). More precisely, although
his discrimination performance correlated with reported awareness(Zeki and Ffytche, 1998), he was nonetheless “able to discriminate
correctly while being unaware” (p. 32). Finally, neuroimaging studies
involving presentation of motion conveying stimuli to patients withunilateral striate damage have demonstrated extrastriate activation inabsence of striate input (Ajina et al., 2015a, 2015c; Barleben et al.,2015; Goebel et al., 2001; Zeki and Ffytche, 1998).
Detailed reports of patients with cortical blindness due to bilateral
striate damage are far fewer in number compared to unilateral cases.

Cortical blindness is a rare syndrome deﬁned as severe loss of vision
resulting from damage to the primary visual cortex (Aldrich et al.,
1987; Flanagan et al., 2009). Compared to bilateral lesions, consequences of striate damage are reported much more commonly in casesof unilateral lesions. Such studies have reported preserved cognitive
abilities in the absence of awareness, i.e. blindsight, in patients’ blindvisual ﬁelds using diﬀerent types of stimuli (Sanders et al., 1974;
Weiskrantz et al., 1974; for a review see Weiskrantz, 2009). For
instance, the patient JS exhibited normal electrophysiological responses on the P3 component to prespeciﬁed target words presented
in her blind hemiﬁeld (e.g., Shefrin et al., 1988), while GY was able todistinguish facial expression of emotions (de Gelder et al., 1999).
Detailed investigations of residual abilities in patients’ blind ﬁelds⁎

1

Corresponding authors.
E-mail addresses: nicolas.ruﬃeux@unifr.ch (N. Ruﬃeux), roberto.caldara@unifr.ch (R. Caldara).
Indicates equal contribution.

http://dx.doi.org/10.1016/j.neuropsychologia.2016.11.009
Received 28 June 2016; Received in revised form 19 October 2016; Accepted 9 November 2016
Available online 13 November 20160028-3932/ © 2016 Elsevier Ltd. All rights reserved.

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Individual case reports include patients whose lesions occurred at birthor young age (Bova et al., 2008; Giaschi et al., 2003), as well as thoseacquired in adulthood (case TN, reported in Pegna et al., 2005; Burraet al., 2013; de Gelder et al., 2008; Hervais-Adelman et al., 2015; case
SBR, reported in Bridge et al., 2010; see also Riddoch, 1917).
Importantly, while the prior have been reported to show reasonableimprovements of visual functions, this does not appear to be the casefor patients whose lesions occurred in adulthood (see also Zihl, 2000).
Despite the extreme severity of the visual deﬁcits causing blind-likebehavior in patients with bilateral damage, these patients commonly
present with residual, rudimentary visual abilities. Reviewing 25 casesof cortical blindness, Aldrich et al. (1987) reported chronic complete
cortical blindness in less than 10% of the patients (for an even lower
prevalence, see Zihl, 2000), while residual light or motion perception
was commonly found. The presence of residual visual abilities subsequent to bilateral striatal damage in humans coincides with ﬁndings
from animal studies. For instance, Denny-Brown and Chambers (1955)
reported that monkeys who had undergone bilateral V1-ablation wereable to localize moving objects, while others reported residual visuomotor ability in rodents (Carey et al., 1990). Similarly, both TN and
SBR have independently been reported as possessing residual motion
perception abilities. Both patients showed above chance performancefor detection of dynamic stimuli, although SBR's performance varied
across visual ﬁelds (Bridge et al., 2010; Hervais-Adelman et al., 2015).
In both cases, dynamic stimuli elicited activation in cortical regions
associated with motion processing. Together, these results are in linewith the idea that residual abilities observed in cortical blindness, inparticular relating to motion perception, are mediated by alternative
pathways, i.e. those bypassing striate cortex (Bridge et al., 2010;
Hervais-Adelman et al., 2015).
However, to the best of our knowledge, the processing of biologicalmotion (BM) has never been tested in a case of cortical blindness due tobilateral striate damage. This is interesting, as across species, processing of BM is one of the most robust abilities of the visual system (Neriet al., 1998). Individuals who suﬀered complete blindness due to densebilateral congenital cataracts show severe visual impairments years
after surgical correction, including that of global motion processing,but intact BM processing (Bottari et al., 2015; Hadad et al., 2012).
Vallortigara and colleagues (Vallortigara et al., 2005; see also
Vallortigara and Regolin, 2006) reported that newly hatched chicks
reared in complete darkness showed a preference for BM of their own,
as well as other species. In humans, developmental studies havereported BM processing in neonates as early as 10 h post-partum(Bardi et al., 2014; Simion et al., 2008) suggesting that detection andinterpretation of BM is most probably hardwired. However, whether
processing of BM – a critical biological ability essential for survival – isspared in cortical blindness remains an open question.
To this aim, the present study aimed at determining whether BM
can be accurately processed in cortical blindness. We tested BC, apatient who suﬀered from severe hypoxia that caused bilateral lesions
in the striate cortex. Similar to the patient TN (see above), BC presentswith chronic cortical blindness, i.e. he is unable to visually describe or
identify static or moving stimuli by sight. However, mirroring reportsof residual visual processing in cortical blindness, he can show
awareness for moving items, and even catch items thrown at him(see Supplementary Video 1 for a demonstration of BC's ability toprocess motion). BC's main complaint concerns his inability to identify
people based on their visual appearance. In particular, he regrets not
being able to identify his wife, although according to his anecdotal selfreport, he sometimes succeeds to identify her based on her gait.
To clarify BC's ability in processing BM we used human and animal
point-light displays (PLDs) which highlight body joints and trigger the
impression of animate motion (see e.g., Hadad et al., 2015; Johansson,
1973; Troje, 2013). The PLDs of biological agents were presented
under varying conditions (upright, inverted, scrambled, static, dynamic), as well as under diﬀerent task constraints (identiﬁcation of an

Supplementary Video 1. Demonstration of BC’s ability to process motion. The ﬁrst
part of the video was recorded during the initial hospitalization, 6 months after the heart
attack. The second part was recorded at the patient’s home, 6 years after the heart attack.
During this latter recording, BC wore eye tracking glasses to allow demonstration of boththe patient’s view as well as that of the experimenter’s.Supplementary material related tothis article can be found online at http://dx.doi.org/10.1016/j.neuropsychologia.2016.
11.009.

individual PLD vs. selection of a prespeciﬁed PLD among a pair ofstimuli). To anticipate our ﬁndings, BC was unable to identify
individually presented PLDs. However, in notable contrast, whenpresented with two dynamic PLDs simultaneously, he could discriminate with high ﬁdelity between human and animal walkers. Moreover,he displayed normal gaze patterns in this 2AFC task. Our ﬁndings add
novel insights into the limited investigations of cortical blindness.
Importantly they highlight, for the ﬁrst time to our knowledge, theremarkably robust residual capacity in cortical blindness to perceive
motion that is conveyed by living biological agents.
2. Methods
2.1. Patient BC
BC (male, right-handed; born 1954, 62 years of age at the time oftesting) suﬀered from severe anoxic encephalopathy caused by a heart
attack in March 2010. Neuro-ophthalmological assessment was performed 20 months after the heart attack. Visual acuity was limited tothe perception of hand movements only in both eyes. Color vision was
absent as the patient failed to identify the color of large brightly coloredobjects. Kinetic manual perimetry (Goldmann) revealed a marked tosevere concentric loss of sensitivity in both eyes with a partial left
homonymous hemianopsia (Fig. 1). Oculomotility, motion detection,ocular and fundus examinations were normal in both eyes. Visualevoked potentials (Nicolet 1015 visual pattern shift monocular stimulation at a rate of 1.9 Hz) showed a P1 latencies of 106 and 104 ms, N
to P amplitudes were 3.77 and 3.85 µV for the right and left eye,respectively.
Neuroradiological assessment of BC's structural MRI (performed
four months after the heart attack - Fig. 2) revealed moderate corticalsubcortical atrophy and posterior white matter hyper-intensity aﬀecting bilateral striate areas. Due to the delay between anoxia and MRI, nogyriform signal could be obtained with Diﬀusion Weighted Imaging,but occipital white matter hyper intensities found in T2 and Flairsequences strongly suggest delayed-onset white matter anoxic lesions(Sawada et al., 1990).2 Additional MRI could not be performed due to2
Although hypoxia is often associated with hippocampal hypoxia and watershedcerebral cortex alteration (Caine and Watson, 2000), cortical blindness with relative
preservation of visual evoked potentials has also been described in such patients (Tsutsui302

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deﬁcits when strongly confronted with them; language comprehension
and expression remain largely preserved.
In contrast to his severe visual deﬁcits, BC presents with a striking
ability to perceive motion. For example, the patient was readily able tocatch a ball thrown at him, even though he could not visually identify
the object (see Supplementary Video 1). He is highly cooperative andwilling to participate in experiments, but fatigues quickly, making
extensive psychophysical testing (see e.g., Bridge et al., 2010) impossible. In summary, neuropsychological assessments and the patient's
self-reports indicate that BC i) presents with chronic cortical blindness;ii) has some residual visual abilities, in particular in perceiving motion;iii) is not aided by motion when identiﬁcation of non-biological stimuli
is concerned, although it might improve his ability to process biologicalstimuli.

pacemaker-placement six months after the heart attack.
Neuropsychological assessment (see Table 1) performed fourmonths after the heart attack showed a severe diﬀuse cognitive
impairment. BC's main cognitive symptoms included cortical blindness
with Anton-Babinski syndrome (anosognosia of visual deﬁcit), dysexecutive syndrome, amnesic syndrome (both retro- and anterogradediﬃculties), ideo-motor apraxia, as well as spatial and temporaldisorientation. During the ﬁrst month, BC also presented with visualand auditive hallucinations, confabulations, along with episodes ofagitation and aggressiveness, which rapidly regressed after behavioral
multidisciplinary approach and pharmacological treatment (Trazodone
and Quetiapine). Contrariwise, linguistic abilities were largely intact,with ﬂuent and informative spontaneous speech, and preserved oral
comprehension. Assessment of verbal intelligence (WAIS-III) yielded a
Verbal IQ score of 74. BC's most pronounced deﬁcits were observed in
the visual domain. Unable to identify objects visually, he could readily
do so provided their verbal deﬁnition, or based on haptic exploration.
Visual discrimination or matching of shapes, line drawings of objects,
real objects, letters, faces, or colors was impossible. Copying letters andsimple geometrical shapes was also severely impaired. There were noclinical signs of visual neglect, and the eye movement recordings
described in detail below (see Sections 2.4 and 2.5) demonstrate thatBC spontaneously ﬁxates both the left and right visual ﬁelds, as dohealthy young and age-matched controls (Fig. 4). Overall, BC behaved
as though he were blind, except for the lack of usage of strategies tocompensate for his visual impairments. BC was discharged andreturned home eight months after the heart attack. Regular follow-up
neuropsychological assessments showed mild overall improvements,
particularly in the memory domain. BC showed the typical evolution ofcortical blindness (Bender and Furlow, 1945). Notwithstanding mild
improvements in perceiving light, motion, contrast and colors, his
cortical blindness remains severe: he is unable to navigate independently, and relies entirely on his wife and caregivers for activities ofdaily living. A brief neuropsychological reexamination of BC's visualabilities performed in 2016 showed no signiﬁcant improvementcompared to the assessment in 2010, but mild improvements inexecutive functions were observed (see Table 1). Partial anosognosia
of his visual deﬁcits persists, although he acknowledges his visual

2.2. Control participants
In addition to BC, we recorded behavioral and eye movement datafrom ﬁve healthy (4 young, one age-matched) control participants(mean age: 30 years, range: 22–61, 4 females). All controls had normal
or corrected to normal vision, no history of brain damage, and provided
written informed consent; none received ﬁnancial compensation forparticipation. Approval for the study was obtained through the local
ethics committee.
2.3. Stimuli
Diﬀerent types of unmasked PLDs were used to assess BM
processing and were derived from point-light sequences of a stationary
walking human or cat (see Supplementary Video 2). The stimuli were
the originals, as reported by Troje and colleagues (Troje, 2002; Troje &Chang, 2013; Troje & Westhoﬀ, 2006). These were derived from the
Biomotion Lab website (https://www.biomotionlab.ca/). Humanwalkers were depicted by a set of 11 markers representing the main
joints and the head of a person, while cat walkers were represented by
14 dots. The PLDs were displayed upright, inverted, or scrambled (Fig.
3); static stimuli were created by deriving a still from the respective
video animations. Dynamic PLDs were shown facing either left or right,

Fig. 1. Results of kinetic manual perimetry (Goldmann). Marked to severe loss of sensitivity (isopter obtained with the largest stimulus V4e) and a subtotal left homonymous
hemianopsia (isopter obtained with the smaller stimulus I4e) were present in both eyes. The dotted red line depicts the normal limits of the isopter obtained with the V4e stimulus in anage-matched normal subject. LE = left eye; RE = right eye; V4e =64 mm2 round stimulus of 1000 apostilbs luminance; I4e =1/4 mm2 round stimulus of 1000 apostilbs luminance.

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Fig. 2. BC's structural MRI acquired four months after anoxic encephalopathy. The patient's FLAIR MRI (left) is compared to an acquisition from a healthy, age-matched subject (right).
For illustration purposes, volumes have been bias-corrected, skull stripped, and underwent arithmetic squaring. The patient's occipital white matter lesions are rather diﬀuse and include
projections to early visual areas including V1, V2, and possibly V3; the medial temporal sulcus and neighboring areas are relatively spared.

provided a verbal response that was recorded by the experimenter; no
feedback was provided. Control participants completed the experiments described below in a single session; BC completed the experiments in six separate sessions, each performed on a diﬀerent day.
A Pre-test was performed to assess BC's ability to detect thepresence/absence of the PLDs. To this end he completed 100 trials,
comprising 20 trials where nothing was presented, as well as 80 trials
involving presentation of either human or animal PLDS (40 each; 20
static, 20 dynamic). On each trial, he was instructed to indicate
whether a) a stimulus was present (“Is there something on the screen?
”), and in the case of the presence of a stimulus, b) determine its
dynamic or static nature (“Is it moving? ”).
Task 1 involved recognition of individually, centrally presented
PLDs. Provided an incorrect or no response, three alternative choices
were provided (i.e. “Is it a cat, a human, or something else?”; chancelevel: 33.3%). First, 10 trials of static PLDs were completed, followedby 10 trials with dynamic PLDs.
Task 2 involved two alternative forced-choice (2AFC) decisions
between simultaneously presented pairs of the stimuli used in the ﬁrst
task. For trials involving a human paired with a cat PLD, subjects were
instructed to detect the human; for trials involving diﬀerent human
PLDs, they had to indicate which displayed an upright human walker.
This task involved 15 blocks of 60 trials each, for each of the two
conditions (static, dynamic). The location of the target was randomly
selected and counterbalanced (50% left; 50% right visual ﬁeld). Control
participants only completed 10 trials per block, as their performance
was at ceiling.

and walking in place, as if on a treadmill. The stimuli appeared as white
dots on a black background. Gait frequencies were 0.93 Hz for thehuman and 1.7 Hz for the cat, reﬂecting realistic frequencies. At a
60 cm viewing distance the human and cat PLDs subtended ~3×6°(width×height) and ~7×3° visual angle, respectively. PLDs presented inpairs were displayed side by side in the center of the screen (13°distance between their centroids). To create scrambled PLDs, dots
sampled from a normal coherent walker were relocated to a randomly
selected location within the same area that was covered by the coherent
PLD.
2.4. Procedure
Processing of BM was tested using two diﬀerent tasks, which
diﬀered with regards to the number of stimuli displayed, and subsequently task performed. Stimuli were displayed on a portable PC
computer (1280×1024 pixels spatial resolution, 85 Hz refresh rate),and on a VIEWPixx/3D monitor (1920×1080 pixels spatial resolution,
120 Hz refresh rate) during eye tracking. Each trial was initiated by theexperimenter. The direction of gait depicted by a stimulus (left or
right), as well as correct response location (i.e., left/right in the 2AFC
task), were randomly selected with a constrained probability of 50% foreach condition. The static or dynamic PLDs were presented forunlimited duration and could be freely explored until participants(footnote continued)
et al., 1984). The MRI changes due to cortical striate abnormalities in such diseases are
generally post-acute (in the ﬁrst month) and sometimes diﬃcult to visualize while
delayed leukoencephalopathy and atrophy has been repeatedly described (Chen-Plotkin
et al., 2008; Margolin et al., 2007).

2.4.1. Eye movement recordings
For each task, we recorded participant's eye movements on a subset
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Table 1 (continued)

Table 1Results of BC's neuropsychological assessment four months after brain damage.

Test
Test

Performance

Performance

Qualitativedescriptor

5

Lim

Preserved
Immediate recalls (Trials1–3): 1/2/2
Delayed recall: 0/10
Recognition: 2/10 (8false alarms)

N
D

5/8
4/10
3/10
SS=3

D
D
D
D

SS=7

N

7/8
39/40
Impossible

NN
D

10/15c50

D
D

No grasping/palm-chinreflex

N

74
79

Lim
Lim

Qualitativedescriptor
MemoryOrientation
TemporalSpatialLanguage
Oral expression
Spontaneous

Vocabulary subtests (WAISIII)
Verbal Fluency (1’)
Litteral (M)Semantic (animals)
Naming objects on verbal
deﬁnitions
Sentence completion
Repetition (complexes
sentences, logatomes)
Oral Comprehension
Situational
Onomatopoeia recognition
Apragmatic/passive
sentences
Syllables discrimination
Verbal Associative Color test
Comprehension subtest(WAIS-III)
Verbal Comprehension Index
Written expression
Simple words
Sentences
Spelling
Reading
Oral calculation
Simple arithmetic facts
Simple Calculation
Arithmetic subtest (WAISIII)
Number semantic
Quantity estimation
Number oral comparisonsPraxiaIdeomotor
Ideational
Constructional
Buccofacial
Visual processing
Visual discrimination andmatching of real objects,
colors, faces
VOSP Shape Detection
screening subtest
Color matching
Associative Color test
Familiar and Famous Faces
recognition
Mental imagery production
Identiﬁcation of body parts
Auditory processing
Familiar noises recognition
Pitch and tone recognition
Intensity diﬀerences
perception

0/5
0/3

D
D

Immediate
Auditivo-verbal span

Lim

Anterograde verbal
Assessor's name recall
10 words list (Rey)

Fluent and informative,
mild word finding
difficulties
SS=8

N

9
7
9/10

D
D
N

12/13
Preserved

N
N

Preserved
Preserved
Mild difficulties

N
N
D

34/40
8/10
SS=9

Lim
Lim
N

79
Handwriting severely
impaired2/2
Impossible
2/5
Impossible

Lim
D

Retrograde
Objects structural properties
AutobiographicalEpisodic collective
Information subtest (WAISIII)
Similitudes subtest (WAISIII)
Encyclopedic knowledge
Celebrities knowledge
Drawing on demand
Executive functions
Frontal Assessment Battery
Working memory subtest(WAIS-III)
Archaic reﬂexes

Global Scale
Verbal IQ (WAIS-III)
Verbal Comprehension index(WAIS-III)

N
D
D
D

FailedFailed
SS=2

D
D
D

3/9
Preserved
Preserved

D
N
N

FailedFailedFailedPreserved

D
D
D
N

Failed*

D

9/20a

D

0/10*
0/10*
0/10*

D
D
D

Failed*
4/10b

D
D

6/10
Preserved
8/10

Lim
N
Lim

D
D

N = within normal limits; Lim = inferior limit; D = deficit; SS=standard score. VOSP =Visual Object and Space Perception Battery; WAIS = Wechsler Adult Intelligence Scale.
Partial reassessment performed in 2016 revealed no improvement (*) or mild
improvements:a
12/20.
b
5/10.
c13/15.

of trials. The reason this was not done for the entire number of trials wasof practical nature. The patient BC, who fatigues extremely quickly,
showed normal gaze patterns on the initially acquired trials (see Section
3). Therefore, we discontinued eye tracking, which is technically moretime consuming due to the frequent calibration required, as compared topurely behavioral testing. On these trials for which gaze data wererecorded, the stimuli were presented using the Psychophysics & Video
Toolboxes (PTB-3; Brainard, 1997; Pelli, 1997) in a Matlab environment(R2010a, The MathWorks, Natick, MA, USA), on a 1920×1080 pixels
VIEWPixx/3D monitor (refresh rate: 120 Hz) at a 70 cm viewing distance.
Eye movements were recorded via Eyelink Toolbox extensions(Cornelissen et al., 2002), using an SR Research Desktop-Mount
EyeLink 2 K eye-tracker, which has an average gaze position error of~.25°, and a spatial resolution of 0.01°. Gaze location on the screen wasrecorded from the dominant eye with a sampling rate of 1000 Hz. A chin/forehead rest ensured stable head positioning. A nine-point calibration
was conducted before each block; additional calibration was performed
when necessary to ensure an optimal recording quality.
2.5. Analyses
Data analyses were performed in Python using PyMC3 (Salvatieret al., 2016) and visualized using Seaborn (Waskom et al., 2014). Eye
movement raw data were preprocessed using custom scripts that
employed the same ﬁlter parameters for saccade and ﬁxation detection(continued)

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Supplementary Video 2. Individual dynamic PLD stimuli used to assess biological motion perception.Supplementary material related to this article can be found online at http://dx.
doi.org/10.1016/j.neuropsychologia.2016.11.009.

Y~

as the Eyelink software (saccade velocity threshold =30°/s; saccade
acceleration threshold =4000°/s). We mirrored the horizontal ﬁxation
location of trials on which the target stimulus was presented on theright side, and overlaid BC's ﬁxation locations onto the ﬁxation
distribution of the controls (separately for young adults and agematched controls). The spatial ﬁxation distribution was estimated via
Gaussian Kernel smoothing (full width at half maximum (FWHM) at 1°
visual angle), resulting in a smoothed ﬁxation map for each condition
per participant. Fig. 4a and b shows controls’ eye ﬁxation patterns
during the 2AFC task, with BC's raw ﬁxation data are superimposed inred. Moreover, to determine the ﬁxation pattern similarity between
controls and BC, we performed Pearson correlations on the ﬁxation
maps between all possible pairs of participants, independently for eachcondition; Fig. 4c shows the mean derived from these similarity
matrices. Fig. 4d indicates the average pattern similarity amongst
young controls (left), as well as between the age-matched control andyoung controls (middle), and the patient and young controls (right).
We modeled the behavioral data from both paradigms (i.e.,
accuracy rate) using a beta-binomial model with Bayesian parameter
estimation. As an alternative to the conventional Null hypothesis
signiﬁcance testing (NHST), a Bayesian approach yields more consistent results under extreme cases, for instance single case studies withsmall number of trials (i.e., 60 trials with a binary decision) (Crawford
and Garthwaite, 2007; Jaynes, 2003). Moreover, parameter estimation
using Bayesian statistics returns probability distributions over the fullrange of possible parameter values, instead of point estimates of themost likely values (e.g., Maximum likelihood estimation). This isimportant as in the current experiment we aimed to estimate thepatient's general recognition ability of static and dynamic stimuli. This
was achieved by using a hierarchical Bayesian approach, which allowed
us to estimate and compare the patient-level hyperparameters (i.e.,
recognition ability for static and dynamic stimuli), with the conditionlevel parameters simultaneously estimated in an optimal way (for the
2AFC task). Additionally, where applicable, hypotheses were tested bycomputing Bayes factor using the Savage-Dickey method(Wagenmakers et al., 2010).
In the beta-binomial model, the total number of accurate responses
after N trials follows a binomial distribution with a probability ofcorrect response p, and the distribution of p follows a beta distribution
with parameters α and β:p~Beta (α ,Binomial(p ,n)Statistical inference of the ﬁrst task (recognition of individual
PLDs) is drawn directly from the posterior distribution of p for eachcondition with a uniform prior p ~ Beta (α=1, β=1). Importantly, toinfer the probability of correct response p across the diﬀerent conditions in the second task (2AFC between PLD pairs), we re-parameterized the beta distribution by the mode ω and the concentration κ(Kruschke, 2015, cf. Eq. 9.4, pp. 223):

α=ω (κ −2)+1

andβ =(1 − ω)(κ −2)+1

withκ >2

We placed a uniform distribution on the mode ω ~ Uniform (0, 1)
as a prior, and a uniform distribution on the concentration parameter κ~ Uniform (2, N). The parameterization using the mode instead of themean is more intuitive for skewed distributions, since the mode is abetter description of central tendency (Kruschke, 2015). Moreover, bymodeling the mode ω as a hyper-parameter, we can directly infer any
advantage for dynamic over static condition across a wide range ofdiﬀerent stimuli pairs (i.e., ωdynamic - ωstatic).
Model parameters were estimated using PyMC3 (Salvatier et al.,2016). Monte Carlo sampling methods were used to accurately
approximate the posterior distributions of the estimated parameters(p or ω) by summarizing their estimation and uncertainty. 30,000
samples were drawn from the posterior to obtain smooth parameter
estimates.

2.6. Initial observations: eye movement recordings
The eye movement recordings showed that, across both tasks, BCorientated his eye gaze correctly to the stimuli presented. BC's patternof eye movements overlaps with those of the young adult controls, aswell as his age-matched control. Fig. 4a and b shows the eye gaze
patterns of BC and controls in one of the conditions (dynamic
presentation of human upright versus animal upright) of the 2AFC
discrimination task. The ﬁxation pattern similarity is quantiﬁed using
Pearson correlation coeﬃcients reported as a similarity matrix in
Fig. 4c, which demonstrate that all participants displayed similar eye
movement patterns. Moreover, a pair-wise permutation t-test revealed
no signiﬁcant diﬀerences amongst the three average correlationcoeﬃcients displayed in Fig. 4d.

β)306

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Fig. 3. Individual PLD stimuli used to assess biological motion perception. For illustration of dynamic stimuli, see Supplemental Video 2.

Fig. 4. Participants’ eye movement patterns during the 2AFC discrimination of dynamic, upright human and animal PLDs. On the trials displayed, subjects had to indicate the locationof the human walker. BC's ﬁxation locations (red dots) superimposed on the ﬁxation heat map derived from (a.) young adult controls, and (b.) the age-matched control. Black squares
show the locations of the presented stimuli (examples of upright human and animal walkers are superimposed in the left and right squares for illustration purposes). We recorded BC'seye movements in order to rule out the possibility of his impairment arising from an inability to ﬁxate the diagnostic information. As his eye movements strongly resembled those ofcontrols, we terminated acquisition of eye recordings while continuing extensive behavioral testing (see Procedure). (c.) Average similarity matrix derived from Pearson correlationcoeﬃcients between participants’ ﬁxation patterns per condition. (d.) Average pattern similarity among young controls (left), between the age-matched and young controls (center), andbetween BC and young controls (right); error bar display 95% conﬁdence intervals.

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3.95 and 3.79 respectively, providing substantial evidence that performance in both conditions did not diﬀer from chance.

3. Results
3.1. Pre-test: stimulus detection and static vs. dynamic
discrimination

3.3. Task 2: two-alternative forced choice task (2AFC) discrimination
between PLD pairs

BC showed neither diﬃculty in determining the presence/absenceof PLDs (97%), nor in determining whether they were static (95%) or
dynamic (95%); all scores signiﬁcantly above chance level (one-tailed
binomial tests).

Table 2 and Fig. 6 summarize BC's performance for 2AFC decisions
performed on simultaneously presented static and dynamic PLD pairs.
For static PLD pairs, BC's overall performance did not diﬀer fromchance level (432 correct responses out of a total 900 trials across allconditions; posterior estimation of the mode of accuracy p=46.8% with
the 95% HDI [31.7, 62.7]; see red line in Fig. 6a). Contrariwise, fordynamic PLD pairs BC showed above chance level performance (777correct responses out of a total 900 trials across all conditions;posterior estimation of the mode of accuracy p=93.3% with the 95%
HDI [87.7, 99.9], see green line in Fig. 6a). Moreover, the posterior
distribution of accuracy rates in all but one condition showed a higher
estimation for the dynamic compared to static condition (see Fig. 6b).
Indeed, by computing the diﬀerences between the modes (i.e.,ωdynamic - ωstatic) we estimated the performance improvement of
the dynamic condition compared to the static condition at Δp=46.5%[29.5, 63.5].
To further determine whether the recognition improvement following the display of dynamic stimuli is species-speciﬁc, we performed two
similar Bayesian hierarchical models on data from trials involving
presentation of pairs of (a) human stimuli (i.e., upright vs. inverted,
upright vs. scrambled, and inverted vs. scrambled), and (b) animal
stimuli (same pairs as for human PLD pairs; see above). The dynamic
over static recognition improvement (displayed in Fig. 6c) for humanstimuli is 25.4% [11.4, 39.7], and 28.9% [15.5, 42.2] for animal stimuli.
The Bayes factor (5.66) indicates that the performance improvement
related to dynamic displays was comparable for human and animal
stimuli.

3.2. Task 1: recognition of individually presented PLDs
Fig. 5 summarizes BC's performance for recognition of individuallypresented static and dynamic PLDs. For static stimuli, contrary tohealthy controls, BC was unable to identify any of the stimuli.
Prompted to choose amongst the three alternative responses, his
performance did not diﬀer from chance (7 correct responses out of
20 trials; posterior estimation of accuracy p=36.3% with the 95%
highest density interval (HDI) [17.7, 56.6]; see red line in Fig. 5). For
dynamic stimuli, BC was again unable to identify any of the presented
PLDs, in contrast to controls who performed at ceiling. Again his
performance provided the three response alternatives did not diﬀer
from chance (6 correct responses out of 20 trials; posterior estimationof accuracy p=31.8% with the 95% HDI [13.7, 50.8]; see green line in
Fig. 5). The Bayes factor computed using the Savage-Dickey method is

4. Discussion
To the best of our knowledge, this is the ﬁrst report of residual BM
perception in a rare case of cortical blindness due to bilateral striate
damage. The patient BC is unable to visually identify objects, but caninterestingly perceive motion and even sometimes identify his wife
based on her gait. We therefore assessed BM in BC by using PLDs ofstatic and dynamic human and animal walkers, including their inverted
and scrambled versions, under diﬀerent task demands. Contrary tocontrols, who generally performed at ceiling, BC was unable to identify
individually presented PLDs regardless of whether they were static orconveyed motion. Strikingly, however, in the context of a 2AFC
discrimination task, his performance was at chance for discriminationof static images,3 but signiﬁcantly above chance level when dynamic
PLD pairs were presented (86%).

Fig. 5. Posterior distribution of BC's performance for individually presented PLDs.
Static and dynamic conditions are represented by red and green lines, respectively; thedashed vertical line indicates chance level. Note that the shape of the distribution
represents the posterior estimation and its associated uncertainty: the more certain of theestimation, the higher the peak of the distribution.

Table 2
BC's performance for the 2AFC task. For each possible stimulus pair (i.e., cell) BC's
percentages of correct responses are provided for static (normal font) and dynamic(italics) conditions, respectively. Asterisks indicate conditions for which performance issignificantly above chance (one-tailed binomial tests performed separately for static anddynamic conditions). Note that for trials involving a human paired with an animal PLD,
subjects were instructed to detect the human; for trials involving different human (oranimal) PLDs, they had to indicate which displayed an upright human (or animal)
walker.
PLD pairs

HumanuprightHumaninverted
Humanscrambled
Animalupright
Animalinverted
Animalscrambled

55|87*

Human
inverted

Humanscrambled

Animalupright

37|88*

53|38

50|95*

43|93*

75*|93*25|88*

8|90*

83*|93*48|82*

55|97*

50|95*

32|97*

58|80*

4.1. Independence of processing form and BM
Previous neuroimaging and patient studies have demonstrated thatprocessing of BM involves various cerebral regions (Grosbras et al.,2012), encompassing those associated with form and motion perception (Kourtzi et al., 2008). These include the ventral premotor cortex,
as well as the posterior superior temporal sulcus (pSTS; Grossman

Animalinverted3
As demonstrated in Fig. 6b, BC displayed above chance level discrimination
performance in two static conditions: human scrambled vs. animal upright, and human
scrambled vs. animal inverted. Conceptually speaking, we believe it is diﬃcult to provide
a solid theoretical explanation for this pattern of results. These two signiﬁcant diﬀerences
should not be considered in isolation, as we did not observe a general advantage for thehuman scrambled condition. We instead would like to suggest that the likelihood of
observing by chance signiﬁcant diﬀerences will increase with the number of tested
combinations.

47|78*

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Gilaie-Dotan et al., 2013; Lu, 2010; Peelen et al., 2006; Vaina et al.,2001). Until recently, it was unclear whether perception of BM
critically relies on processing of object form (Beauchamp et al., 2002;
Grossman and Blake, 2002; Jastorﬀ and Orban, 2009; Lu, 2010; Vaina
et al., 2001). However, Gilaie-Dotan et al. (2015) reported intact
perception of BM in visual agnosic patients presenting with varied
ventral lesions, thus providing compelling evidence for independent
processing of BM and visual form. Our results thus add to a body ofevidence suggesting that processing of BM as well as general motion
are mediated by mechanisms that are distinct from those involved inprocessing object form.
4.2. Task-dependency of residual abilities in cortical blindness
Our ﬁndings corroborate previous results reporting that patients’
residual abilities depend on the speciﬁc testing conditions and stimuli
employed (Hervais-Adelman et al., 2015; Richoz et al., 2015;
Weiskrantz et al., 1995; Zeki and Ffytche, 1998). Mirroring previous
neuropsychological reports, they demonstrate that reliable discrimination can be observed under circumstances of reduced uncertainty byproviding task-relevant information (Barton et al., 2002; Joubert et al.,
2003; Ramon and Rossion, 2010; Ramon et al., under review). We
speculate that in the 2AFC task, simultaneously increasing the available
visual information and constraining the number of choice alternatives
enhances residual cortical signal relative to noise.4 Thus, the present
results highlight the role of top-down modulation on patients’ residual
visual processing abilities, which can lead to a substantial improvement
in behavioral performance. This has important implications for thedevelopment of intervention and compensation strategies in visually
impaired (and most probably other) patients. These should speciﬁcallyincorporate knowledge concerning the conditions under which taskdependent improvements and residual abilities can be observed.
Whether such top-down facilitation generalizes to other aspects ofvision such as color and object perception remains to be clariﬁed infuture studies.
4.3. Residual processing of motion conveyed by living agents
As described above, our 2AFC tasks involved diﬀerent types ofstimulus pairs. Trials could involve pairs of a) distinct categories of
biological agents (animal vs. human), or b) exemplars of the same
category (e.g., human upright vs. inverted). In the ﬁrst case, discrimination could be based on low level information alone, i.e. the diﬀerencein the visually stimulated surface, the orientation of which diﬀered
between PLDs displaying a bi- or quadruped (i.e., vertical vs. horizontal). Importantly, BC also showed a BM processing advantage on
trials involving within-category pairings, which did not incorporatesuch low-level diﬀerences. Finally, BC showed high and moreover
comparable performance levels for trials involving either pairs ofhuman or animal PLDs (see Fig. 6c). Overall these observations
indicate that the advantage for BM is not species-speciﬁc (Bardi
et al., 2014; Simion et al., 2008; Vallortigara et al., 2005;
Vallortigara and Regolin, 2006) or straightforwardly related to a
strategy based on low-level stimulus properties. The processing of
motion conveyed by living agents is therefore a genuine residual
capacity observable in cortical blindness.

Fig. 6. BC's performance for discrimination between pairs of PLDs. (a.) Posterior
distributions of BC's overall performance. Note that the shape of the distribution
represents the posterior estimation and its associated uncertainty: the more certain of
the estimation, the higher the peak of the distribution. (b.) Results of the Bayesianhierarchical modeling performed on the data shown in Table 2. Line plots show posterior
distributions of BC's recognition accuracy for each PLD pairing. (c.) Posterior distribution of BC's recognition improvement (dynamic - static) in the 2AFC task for trials
involving pairs of human (dashed line), or animal (solid line) PLDs. Red and green lines
in a. and b. represent the static and dynamic condition, respectively; dashed vertical lines
represent chance level. (For interpretation of the references to color in this ﬁgure legend,
the reader is referred to the web version of this article.)

5. Conclusions

et al., 2000; Puce and Perrett, 2003; Vangeneugden et al., 2014).
Disruption to either (e.g., via transcranial magnetic stimulation, or
brain damage) can impair perception of BM (Grossman et al., 2005;
Saygin, 2007; Vaina and Gross, 2004; van Kemenade et al., 2012).
Additional regions implied in processing of BM include MT+/V5 andregions of the visual form pathway, i.e. the extrastriate body area andlateral temporal cortex (Beauchamp et al., 2002; Brooks et al., 2008;

It has been previously suggested that residual motion processing
4This notion is supported by other neuropsychological reports as well. For instanceBattelli et al., (2003) reported that neglect patients with parietal lesions could be, albeit
slowed down, capable of determining the presence of rightward BM provided presentation of one or two PLDs, but were dramatically impaired when more than two stimuli
were shown (Experiment 2a).

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abilities in cortical blindness are mediated by alternative pathways thatbypass striate cortex (Bridge et al., 2010; Hervais-Adelman et al.,2015). Such geniculo-extrastriate pathways have been suggested tounderlie MT/V5 activation in the absence of striate input (Ajina et al.,2015a, 2015b, 2015c; Barleben et al., 2015; Goebel et al., 2001;
Morland et al., 2004; Schoenfeld et al., 2002; Sincich et al., 2004;
Zeki, 2015). We speculate that BC's residual abilities may reﬂect
processing within other regions critically involved in BM which areprobably spared, such as STS and V5.
It is worth noting that the aforementioned previous studies havefocused on processing of general motion. As such the present study
represents the ﬁrst investigation into BM processing in a rare case ofbilateral cortical blindness, presenting with severely impaired visual
categorization (i.e., color, shapes, faces and objects). Since additional
MRI was not possible in BC, our future eﬀorts are directed towards
developing non-invasive neuroimaging techniques (e.g. NIRS, EEG) for
further investigation of this unique patient. This will serve to specify
the extent of his (extra)striate damage and determine whether and if
which regions are spared. Moreover, we aim to investigate theneurofunctional correlates of BM in greater detail in this rare case todisentangle the respective roles of e.g. STS in BM processing, andaddress how task demands shape neural responses in structurally
intact cortices given absent or restricted striate input.
Conﬂict of interest statement
The authors declare that the research was conducted in the absenceof any commercial or ﬁnancial relationships that could be construed asa potential conﬂict of interest.
Acknowledgments
We thank BC and his wife for their continued cooperation, Vincent
Junod for assistance during data acquisition, as well as Neil Docherty
and two anonymous reviewers for helpful comments on a previous
version of the manuscript. This study was supported by the Swiss
National Science Foundation (Grant no. 316030_144998) awarded toRoberto Caldara and Jean-Marie Annoni.
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