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Abstract
Different spatial representations are not stored as a single multipurpose map in the brain. Right brain-damaged patients can
show a distortion, a compression of peripersonal and extrapersonal space. Here we report the case of a patient with a right
insulo-thalamic disconnection without spatial neglect. The patient, compared with 10 healthy control subjects, showed a
constant and reliable increase of her peripersonal and extrapersonal egocentric space representations - that we named
spatial hyperschematia - yet left her allocentric space representations intact. This striking dissociation shows that our
interactions with the surrounding world are represented and processed modularly in the human brain, depending on their
frame of reference.
Citation: Saj A, Wilcke JC, Gschwind M, Emond H, Assal F (2013) Spatial Hyperschematia without Spatial Neglect after Insulo-Thalamic Disconnection. PLoS
ONE 8(11): e79938. doi:10.1371/journal.pone.0079938
Editor: Andrea Serino, University of Bologna, Italy
Received January 11, 2013; Accepted October 7, 2013; Published November 26, 2013
Copyright: ß 2013 Saj et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted
use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This work was supported by the Foremane Fund for AS, by the Swiss National Fundation (SNF320030_138163), and the Société Académique de Genève
(Fonds Cognitive Memory, NAC 08-025) to FA. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the
manuscript.
Competing Interests: The authors have declared that no competing interests exist.
* E-mail: arnaud.saj@unige.ch
with left superior quadranopsia. Immediately after being dis- plane at any of 25 possible target positions spaced 1 cm apart. The
charged, she complained about an abnormal feeling of distance maximum attainable distance was initially estimated by asking
from the real environment. Neuropsychological functions were sitting participants to extend their arm as far as possible in front of
examined using a routine battery of standardized clinical tests, them without moving their upper body (on average 60 cm).
including the Mini-Mental State Examination, in order to exclude Targets were randomly presented twice at each position to make
dementia and other major cognitive disorders that would affect up a total of 50 trials.
task performance and collaboration. The results of all neuropsy- Egocentric distance task. Standing subjects had to estimate
chological tests were normal (see Table 1) and her instrumental the horizontal distance between them and the experimenter in
activities of daily living entirely intact. Only the daisy drawing test front of them. The experimenter stood at distances of 20, 50, 90,
(e.g. flower) showed superficial hyperschematia, with 8 petals on 120, 150, 190 or 210 cm in random order.
the left compared to 5 on the right. All evaluations were done as Allocentric distance task. The task required subjects in a
usual (i.e. only in the peripersonal space). sitting position to estimate the horizontal distance between two
Later on, T.R. constantly reported that very unusual feeling of objects (wooden cubes), both of which were placed 90 cm in front
remoteness of her environment and/or would claim to perceive of the participant. The distance varied randomly between 5, 10,
everything around her as far away. The phenomenon had actually 15, 20, 30, 40, 50 and 60 cm, and the task was performed in the
appeared abruptly after the cerebrovascular event, remained frontal and lateral plane.
stable and chronic when standing or sitting, but strikingly Participants performed five trials per condition. Trials were
diminished in the supine position. separated by about 20 seconds, and the tasks by about 2 minutes.
Healthy participants were recruited through advertisements in
the University of Geneva and included 5 female and 5 male Procedure
volunteers (mean age = 79.4 years, SD = 7.7 years, range = 68–93 In the first experiment (egocentric reachable task), participants
years), all right-handed and without any history of previous were installed in front of a line of red points. Then the
neurological or psychiatric disease. They had normal or corrected- experimenter pointed to one of them at the time, and participants
to-normal visual acuity. The study protocol was approved by the were asked to say whether they thought they could reach it. The
local ethics committee (Ethic Central Commission of the actual border (initial point) between reachable and unreachable
University Hospital of Geneva), following the ethical principles points was 60 cm, corresponding to the mean distance of the
expressed in the Declaration of Helsinki. The patient as well as all extended arm. In the second experiment (egocentric distance task),
volunteers were compos mentis and signed written consent forms participants were asked to estimate the distance between their own
before taking part in the experimental testing sessions. The body and the experimenter positioned in front of them beyond
examiners explained the purpose of the research to the patient as arm’s reach. In the last experiment (allocentric distance task),
well as all volunteers and responded to questions and concerns. participants were asked to estimate the distance between two
objects placed in extrapersonal space (in the frontal and the lateral
Behavioral tasks plane). In all tasks, participants gave their distance estimates
Egocentric reachable task. This task served to estimate the verbally.
perception of action space, operationalized by the farthest target
position perceived as reachable with an extended arm. Visual Statistical analysis
targets were red points 7 mm in diameter, which were presented We used parametric tests ([8]; the Student t test or Bayesian
by the experimenter directly in front of the subject in the frontal hypothesis test [http://www.abdn.ac.uk/̃psy086/dept/psychom.
Figure 1. The patient’s acute ischemic lesion. The figure shown on axial slices of the diffusion weighted image, involves the right ventrolateral
posterior thalamus, the lateral edge of the pulvinar and the adjacent white matter down to the right hippocampus.
doi:10.1371/journal.pone.0079938.g001
Memory Neglect
Span verbal 6 .6 Bell cancellation test
spatial 7 .6 Total omissions 6 ,6
Left-Right omissions 22 ,2
16 words free cued
Recall 1 14 16 pec. 99 Line bisection
Recall 2 16 16 pec. 99 % of deviation 2.5% ,11%
Recall 3 15 16 pec. 99
Delayed Recall 13 16 pec. 99 Bisiach test 0 0
Recognition 16 pec. 99
Language: Boston naming test [45], Fluency test [46]; Apraxia: sub-test CAMCOG [47]; Agnosia: Protocole Montréal-Toulouse d’Evaluation des Gnosies Visuelles [48];
Memory: Span (sub-test CAMCOG), 16 words (Grober and Buschke test, [49]); Executive function: Luria test [50], Stroop [51], Trail Making Test [52]; Neglect [53]. Percentil:
per.
doi:10.1371/journal.pone.0079938.t001
htm]) to compare the continuous dependent variables (estimated fmrib.ox.ac.uk/fsl/fslwiki/FSL) and then performed data recon-
distances in cm) between patient and control subjects. struction and fibre tracking using the Diffusion Toolkit (DTK;
http://trackvis.org/dtk/). We next isolated the acute thalamic
lesion by thresholding the diffusion-weighted image volume and
DTI data acquisition and analysis manually removing unconnected above-threshold voxels. We then
Images of the patient’s brain at the acute stage were acquired used FLIRT (also part of FSL 4.1) to coregister the acute diffusion-
using a 1.5 T whole-body MRI scanner (Achieva, Philips, Best, the weighted image to the chronic diffusion-weighted image ouput by
Netherlands) at the University Hospital Geneva, Switzerland, with DTK and applied the resulting transformation matrix to the lesion
a 6-channel head coil. We obtained diffusion-weighted images image. After thresholding the latter to restore the size of the
with an echo-planar spin-echo pulse sequence (TR = 3263 ms; lesion’s volume after coregistration, we used TrackVis (http://
TE = 68 ms; flip angle = 90u; acquisition matrix = 112688; 24 trackvis.org/) to visualise the fiber tracts passing through the acute
slices with a gap of 1 mm; 0.960.965.0 mm3; 3 averages; PAT right thalamic lesion.
factor 2). After 19 months we acquired diffusion-tensor images of
the patient’s brain using a 3 T whole-body MRI scanner (Trio Results
Tim, Siemens, Erlangen, Germany) with a 12-channel head coil at
the same hospital, this time employing an echo-planar pulse Behavioral results
sequence (TR = 8300 ms; TE = 83 ms; flip angle = 90u; acquisi- In summary, we found a measurable extension of the perception
tion matrix = 1286128; 64 slices; 26262 mm3; PAT factor 2). of certain types of space in a brain-damaged patient compared to
We performed diffusion weighting along 63 independent direc- normal controls. In line with the hypothesized division of spatial
tions (b = 1000 s/mm2) and additionally acquired 10 reference representations, the patient differed from the control group in both
images (b = 0 s/mm2). egocentric tasks but not in the allocentric task (neither in the
All DICOM files were converted to NIfTI format using frontal nor lateral plane).
MRIConvert (http://lcni.uoregon.edu/̃jolinda/MRIConvert/). For the egocentric reachable task (figure 2), T.R.’s distance
We first corrected the chronic diffusion-tensor images for eddy estimates (mean = 43.061.8 cm) were significantly shorter than
currents and head motion using FDT (part of FSL 4.1; http://fsl. those of the control group (one-tailed probability = 0.002). The
DTI results
The fiber tracts affected by the patient’s lesion (figure 4a) project
from the ventrolateral posterior nucleus of the right thalamus to
the corpus callosum and frontal areas, and involve, at the
posterolateral edge of the pulvinar, the inferior fronto-occipital
fasciculus (figure 4b), which originates from the lingula and
inferior parietal regions and projects to the external capsule and
the insula.
Discussion
Our data show for the first time an extension of peripersonal
and extrapersonal egocentric space in a patient with vascular
lesions in the right hemisphere, specifically disconnecting the right
posterior thalamus from the insula. Her perception of peripersonal
distances was increased by over 17 cm compared to the
corresponding physical distances, and her perception of extra-
personal distances by more than 20 cm. However, these extensions
Figure 2. Egocentric reachable task. (a) schematic setup and of space were present only when she was estimating a distance
illustration of the mean distance estimates of reachable stimuli; (b)
from her body, but not when estimating the distance between two
estimates of T.R. (diamond) and control group (triangles) of the border
of their peripersonal egocentric space. objects. These results perfectly fit with the patient’s complaint of
doi:10.1371/journal.pone.0079938.g002 remoteness of the environment.
Such a distortion of space has, to our knowledge, never been
estimates of the latter were similar to previously reported data [9], reported in the literature. Other authors [10–11] have carried out
whereas the patient’s perceived reachable point was unequivocally direct tests for perceptual distortions in neglect patients by asking
shifted closer to her body, in line with peripersonal space being them to make matching judgments of pairs of horizontal and
perceived as being further away. vertical rectangles or nonsense shapes. Their results showed
For the egocentric distance task (figure 3), T.R.’s estimates also significant and substantial underestimations of the area of stimuli
showed a significant difference compared to those of the control presented on the left side of egocentric space, but no such
group (one-tailed probability = 0.04). The latter overestimated the misperceptions of stimuli presented along the vertical meridian,
real distance by 5.268.2 cm, whereas the patient did so by and were interpreted in terms of attentional disengagement from
21.468.6 cm. T.R. thus showed an extension of more than 20 cm an image junction and diminished strength of the representation of
of both her peripersonal and extrapersonal space. objects within the neglected side [12]. Nevertheless, these studies
In the allocentric distance task, the patient showed no significant concern the perception of distance between two objects without
difference compared to the control group in the two dimensions. any reference to the perceiver’s body. Studies on spatial perception
In the lateral plane, deviations from the actual distance between with reference to the perceiver’s body found that patients with
two objects were 4.161.0 cm and 5.862.4 cm (one-tailed neglect syndrome showed a shift towards the ipsilesional side [3]
probability = 0.25), respectively. In the frontal plane, they were and a compression of the left contralesional space [13].
Figure 3. Egocentric distance task. (a) schematic setup and illustration of the mean distance estimates between participants and experimenter;
(b) mean estimates of T.R. and control group of a distance in their extrapersonal egocentric space.
doi:10.1371/journal.pone.0079938.g003
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