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A Lateralized Brain Network for Visuospatial Attention
Michel Thiebaut de Schotten, Flavio Dell’Acqua, Stephanie Forkel, Andrew
Simmons, Francesco Vergani, Declan G.M. Murphy, Marco Catani
To cite this version:
Michel Thiebaut de Schotten, Flavio Dell’Acqua, Stephanie Forkel, Andrew Simmons, Francesco Ver-
gani, et al.. A Lateralized Brain Network for Visuospatial Attention. Nature Neuroscience, Nature
Publishing Group, 2011, �10.1038/nn.2905�. �hal-00680170�
1
A Lateralized Brain Network for Visuospatial Attention
Michel Thiebaut de Schotten *
1,2,3†
, Flavio Dell’Acqua
1,3,4†
, Stephanie Forkel
1
,
Andrew Simmons
3,4,5
, Francesco Vergani
6
, Declan G.M. Murphy
1
and Marco Catani
1,3
1
Natbrainlab, Department of Forensic and Neurodevelopmental Sciences, Institute of
Psychiatry, King’s College London, London, UK
2
INSERM–UPMC UMR S 975, G.H. Pitié–Salpêtrière, Paris, France
3
Department of Neuroimaging, Institute of Psychiatry, King’s College London,
London, UK
4
NIHR Biomedical Research Centre for Mental Health at South London and
Maudsley NHS Foundation Trust and King’s College London Institute of Psychiatry,
UK
5
MRC Centre for Neurodegeneration Research, King’s College London, UK
6
Department of Neurosurgery, Royal Victoria Infirmary, Newcastle upon Tyne, UK
†
Contributed Equally to this work
*Corresponding Author: Michel Thiebaut de Schotten, Natbrainlab, Department of
Forensic and Neurodevelopmental Sciences, King's College, Institute of Psychiatry,
16 De Crespigny Park, SE5 8AF London UK. Email: michel.thiebaut@gmail.com
2
ABSTRACT
Right hemisphere dominance for visuospatial attention is characteristic for most
humans, but its anatomical basis remains unknown. We report the first evidence in
humans for a larger parieto–frontal network in the right than left hemisphere; and a
significant correlation between the degree of anatomical lateralization and asymmetry
of performance on visuospatial tasks. Our results suggest that hemispheric
specialization is associated with an unbalanced speed of visuospatial processing.
3
Clinical studies in patients with brain lesions, and decades of neuropsychological
testing in split–brain patients, have led to the assumption that visuospatial attention is
a function of the right hemisphere
1, 2
. Nevertheless, right visuospatial neglect is not an
infrequent finding in patients with left hemisphere damage
3
suggesting that
visuospatial attention is probably a bilateral function; with right hemisphere
dominance in most, but not all, humans
4
. However, the anatomical basis of the
hemispheric dominance for visuospatial attention is largely unknown.
In the monkey brain the activity of neurons dedicated to visuospatial attention has
been recorded simultaneously using multiple electrodes implanted in the parietal and
frontal cortex
5
. Axonal tracing studies have shown that these neurons are directly
linked through a system of connections running longitudinally in the dorsolateral
regions of the brain
6
. Recent structural
7
and functional
8
imaging studies provide
indirect evidence of a similar system in the human brain. However, the hemispheric
lateralization of the parieto–frontal connections in the human brain and its correlation
with visuospatial performances has never been demonstrated.
In this study, we performed virtual in vivo dissections of the parieto–frontal
connections in 20 right–handed subjects (11 males, 9 females) using diffusion
imaging tractography based on spherical deconvolution
9
.
A comparison between our human tractography dissections and the corresponding
reconstructions from a monkey atlas
6
that we modified are illustrated in Fig. 1.
Overall, parieto–frontal connections of the human and the monkey brain are similarly
organized in three longitudinal parieto–frontal tracts separated into a dorsal superior
4
longitudinal fasciculus (SLF) I, middle SLF II and ventral SLF III (see supplementary
material)
10
.
By measuring the volumes of the tracts in both hemispheres we were able to show a
dorsal to ventral gradient of lateralization of the SLF (Fig. 2a). The SLF I is
symmetrically distributed between left and right hemispheres (t
(19)
< 1); the SLF II
shows a trend of right lateralization (t
(19)
= 1.141; p = 0.268) and the SLF III is right
lateralized (t
(19)
= 6.083; p < 0.001).
To test whether this lateralization was related to the attentional bias for one visual
hemi–field, we asked the participants to perform a line bisection test
11
. In the general
population a small left deviation in the line bisection test is observed and referred to
as the ‘pseudoneglect effect’
11
. Consistent with previous studies
12
, our participants
deviated towards the left at a group level (– 1.53 ± 2.02mm ; t
(19)
= 3.148 ; p = 0.005).
In the majority of participants the correlation analysis indicates that larger SLF II
volumes on the right hemisphere corresponded to a greater deviation to the left in the
line bisection (r = – 0.734; p < 0.001)(Fig. 2b). Importantly the three subjects
deviating to the right showed an opposite pattern of lateralization (i.e. larger volume
of the left SLF II). Correlations with the SLF I (r = 0.258; p = 0.286) and the SLF III
(r = – 0.295; p = 0.220) were not statistically significant.
It is unknown how differences between the two hemispheres in SLF II volume can
lead to asymmetrical processing of visual scenes. Larger tract in the right hemisphere
could depend on a number of factors, including greater fiber myelination, higher
number of axons and larger axonal diameter that are correlated with the conduction
speed
13, 14
. In light of these previous works, we suggest that the left deviation in the