c o r t e x 5 7 ( 2 0 1 4 ) 2 4 4 e2 5 3

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Research report

Object and space perception e Is it a matter

of hemisphere?
Selene Schintu a,b,*, Fadila Hadj-Bouziane a,b, Olga Dal Monte c,
Kristine M. Knutson d, Matteo Pardini e, Eric M. Wassermann d,
Jordan Grafman f and Frank Krueger g,h,**
a

INSERM, U1028, CNRS, UMR5292, Lyon Neuroscience Research Center, ImpAct Team, Lyon, France
University UCBL Lyon 1, France
c
Department of Neuropsychology, University of Turin, Turin, Italy
d
Behavioral Neurology Unit, National Institute of Neurological Disorders and Stroke, National Institutes of Health,
Bethesda, MD, USA
e
Department of Neuroscience, Rehabilitation, Ophthalmology, Genetics, Maternal and Child Health,
University of Genoa, Genoa, Italy
f
Cognitive Neuroscience Laboratory Rehabilitation Institute of Chicago, Chicago, IL, USA
g
Molecular Neuroscience Department, George Mason University, Fairfax, VA, USA
h
Department of Psychology, George Mason University, Fairfax, VA, USA
b

article info

abstract

Article history:

In the 1980s, following Newcombes observations, Ungerleider and Mishkin put forward the

Received 8 October 2013

functional subdivision of the visual system into a ventral stream dedicated to object

Reviewed 3 December 2013

perception and a dorsal stream dedicated to space perception. Ten years after this dis-

Revised 3 March 2014

covery, the perception-action model re-defined the dorsal stream as responsible for non-

Accepted 23 April 2014

conscious visual guidance, and most recently a tripartition has been suggested to ac-

Action editor Paolo Bartolomeo

count for a variety of visuospatial functions. Here, we investigated the neural un-

Published online 2 May 2014

derpinnings of object and space perception by combining the administration of the Visual
Object Space Perception (VOSP) battery with a voxel-based lesion symptom mapping

Keywords:

(VLSM) approach in a large sample of patients with penetrating traumatic brain injury

Dorsal stream

(pTBI). First, our results provided new support for the complementary role of both hemi-

Ventral stream

spheres in object recognition. The right lateral occipital complex was found to be critical in

Lateralization

early perceptual discrimination, whereas more anterior temporal and frontal regions in the

VLSM

left hemisphere were found to be critical in more complex forms of object discrimination

Insula

and recognition. Second, our findings confirmed that space perception depended on the
integrity of the right inferior parietal lobule (IPL) and revealed that a network linking
the right IPL with the right premotor cortex was critical for the perception of spatial
relationships in both 2D and 3D representations. Taken together, our results supported the

* Corresponding author. CRNL e ImpAct Team, 16, ave Doyen Lepine, 69676 Bron Cedex, France.
** Corresponding author. Molecular Neuroscience Department George Mason University 4400 University Drive, Mails Stop 2A1, Fairfax, VA
22030, USA.
E-mail addresses: [email protected] (S. Schintu), [email protected] (F. Krueger).
http://dx.doi.org/10.1016/j.cortex.2014.04.009
0010-9452/ 2014 Elsevier Ltd. All rights reserved.

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functional subdivision of the visual system and shed new light on the specific processes
involved along both the dorsal and the ventral streams.
2014 Elsevier Ltd. All rights reserved.

1.

Introduction

Years after the what and where hypothesis suggesting a functional partition of the visual system into two streams e a
ventral stream subserving object perception and a dorsal stream
subserving space perception (Mishkin, Ungerleider, & Macko,
1983; Newcombe, 1969; Ungerleider & Mishkin, 1982), new
frameworks have emerged refining this subdivision both
anatomically and functionally. Notably, the perception-action
model defines the dorsal stream as responsible for nonconscious visual guidance of action and the ventral stream
for conscious perception (Goodale & Milner, 1992; Milner &
Goodale, 2006). Recently, Kravitz et al. (Kravitz, Saleem,
Baker, & Mishkin, 2011) suggested a tripartition of the dorsal
stream to account for the variety of visuospatial functions.
Three distinct pathways originating in the posterior parietal
cortex (PPC) mediate different visuospatial abilities: (i) a
parieto-premotor pathway for eye movements, several forms
of visually guided action, and grasping; (ii) a parieto-prefrontal
pathway for top-down control of eye movements and spatial
working memory; and (iii) a parieto-medial temporal pathway
for spatial abilities related to navigation. Likewise, the same
group proposed a refinement of the ventral object representation pathway, which is subserved by distinct cortical and
subcortical structures (Kravitz, Saleem, Baker, Ungerleider &
Mishkin, 2013).
Evidence about hemispheric dominance for object
perception and recognition is controversial. Some neuropsychological and neuroimaging studies point toward a right
hemisphere dominance in object perception (Acres, Taylor,
Moss, Stamatakis, & Tyler, 2009; Konen, Behrmann,
Nishimura, & Kastner, 2011), while others suggest a left
hemisphere
dominance
(Price,
Moore,
Humphreys,
Frackowiak, & Friston, 1996; Sergent, Ohta, & MacDonald,
1992; Stewart, Meyer, Frith, & Rothwell, 2001; Zelkowicz,
Herbster, Nebes, Mintun, & Becker, 1998). These conflicting
findings can be reconciled by the fact that object recognition
involves hierarchically organized processes (Ungerleider &
Haxby, 1994) that depend on either the left or the right
hemisphere. According to this view, the right posterior occipital and temporal regions are specialized for the discrimination of basic features, while more anterior left temporal
regions are specialized for assigning a meaning to objects for
categorization and recognition (De Renzi, 1982).
In contrast, general consensus exists on the prominent role
of the right hemisphere in controlling visuospatial attention
(De Renzi, 1982; Kinsbourne, 1987; McCarthy & Warrington,
1990; Mesulam, 1981; Newcombe, 1969). A series of behavioral experiments have demonstrated a relative right hemisphere advantage for processing relationships between spatial
coordinates (i.e., distance evaluation) (Kosslyn et al., 1989). The
right hemispheres dominance in spatial attention, especially

the involvement of the right parietal cortex, is supported by an

abundant literature in neglect patients (e.g., Heilman & Van
Den Abell, 1980; Vallar & Perani, 1986) and by recent evidence
from functional neuroimaging (Thiebaut de Schotten et al.,
2011) and transcranial magnetic stimulation (TMS) (Brighina
et al., 2002; Fierro et al., 2000; Hilgetag, Theoret, & PascualLeone, 2001; Muri et al., 2002; Rounis, Yarrow, & Rothwell,
2007) studies in healthy subjects.
In this study, we investigated the neural underpinnings of
object and space perception by employing the Visual Object
Space Perception (VOSP) battery (Warrington & James, 1991)
and a voxel-based lesion symptom mapping (VLSM) approach
in a large sample of patients with penetrating traumatic brain
injury (pTBI). VLSM studies are of importance in identifying
regions necessary for cognitive processes and corroborating
evidence from single case, clinical, and neuroimaging studies
(Bates et al., 2003). In our study, we addressed the following
two questions: 1) What are the anatomical correlates of both
object and space perception and 2) Do subjects with lesions in
both hemispheres exhibit any hemispheric dominance in
object and space perception? Our results supported the complementary role of both hemispheres in object recognition
and identified key regions associated with different cognitive
processes along the ventral stream that depended on task
demand. Our findings confirmed that space perception
depended on the integrity of the right IPL within the dorsal
stream, and demonstrated that a network linking the right IPL
with the right premotor cortex was critical for the perception
of spatial relationships in both 2D and 3D representations.

2.

Material and methods

2.1.

Subjects

Participants were drawn from Phase III of the W.F. Caveness

Vietnam Head Injury Study (VHIS) registry, which is a prospective, long-term follow-up study (Raymont, Salazar,
Krueger, & Grafman, 2011). Out of the 254 veterans, 247
completed the VOSP battery and were divided into two groups
based on the presence or absence of pTBI: a lesion group
(LG 192) and a control group (CG 55). All veterans gave
their written informed consent before participating in this
study, which was approved by the Institutional Review Board
at the National Naval Medical Center and the National Institute of Neurological Disorders and Stroke, Bethesda, MD.

2.2.
Neuropsychological assessment and behavioral
analysis
All participants underwent a 5e7 day neuropsychological
assessment. As the experimental measure, we employed the

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VOSP battery (Warrington & James, 1991) with eight visual

perception tasks designed to assess particular aspects of object and space perception (Lezak, 2004). First, we administered
the VOSP shape detection screening task that assessed basic
visual discrimination abilities (i.e., detecting whether or not
the letter X was presented in randomly presented patterns).
Failing the screening task prevented the administration of the
entire subsequent battery.
To assess object perception, we selected two out of four
tasks that specifically targeted object perception and excluded
those using numbers or letters as stimuli to minimize the
involvement of other cognitive skills. The silhouette task tested
the ability to recognize and name animate (i.e., animals) or
inanimate (i.e., objects) from two-dimensional silhouettes.
The object decision task tested the ability to identify and point
at the two-dimensional shape of the real object among three
distractors. To assess space perception, we selected two out of
four tasks that specifically targeted space perception, and
excluded the two tasks involving matching-to-sample procedure or numbers as stimuli. The position discrimination task
tested the ability to estimate and point to the relative position
of an object in a two-dimensional space. The cube analysis task
tested the ability to perceive, extract and count threedimensional shapes from black and white 3D drawings.
As control measures, we administered the following neuropsychological tests/surveys: the Token Test (TT; (McNeil &
Prescott, 1994)) to test basic verbal comprehension; the Boston Naming Test (BN; (Kaplan, Goodglass, & Weintraub, 1976))
to test naming abilities; the Beck Depression Inventory (BDI-II;
(Beck, Steer, & Brown, 1996)) to measure the severity of
depression; and the Armed Forces Qualification Test (AFQT7A; (United States Department of Defense, 1960)) to evaluate
pre- and post-injury general intelligence. The AFQT was
administered to veterans upon entry into the military; it is
extensively standardized within the U.S. military and its
scores correlate highly with the WAIS IQ scores (Wechsler
Adult Intelligence Scale) (Grafman et al., 1988).
Behavioral data analyses were carried out using SPSS
(Statistical Package for the Social Sciences, version 14.0.1,
SPSS Inc., Chicago, USA, http://www.spss.com) with alpha set
to p < .05 (two-tailed). Patients raw scores from each of the
VOSP tasks were converted into z-scores based on the performance of the control participants. Independent samples ttests were performed to compare demographic, experimental,
and control variables between LG and CG.

2.3.

was performed by a physician with clinical experience reading

CT scans, and reviewed by an experienced observer (JG), who
was blind to the results of the clinical evaluation and neuropsychological testing. Each CT scan was spatially normalized
to a template in Montreal Neurological Institute (MNI) space,
using the AIR algorithm (Woods, Mazziotta, & Cherry, 1993)
with a 12-parameters affine fit. To optimize efficacy of the
registration procedure, the brain images were first automatically skull-stripped. Voxels inside the traced lesion were not
included in the spatial normalization procedure. For each
patient, the traced lesion image in MNI space was used for
VLSM analysis. Gyri and Talairach coordinates were obtained
using the AAL atlas (Tzourio-Mazoyer et al., 2002), and Brodmann areas (BAs) were determined using the Volume Occupancy Talairach Labels (VOTL) database (Lancaster et al.,
2000).
To examine the distribution of lesions, a density map was
created by overlaying patients normalized lesion maps. Then,
whole brain VLSM analyses (1-tailed t-test, q(FDR) < .05,
minimum cluster size of 10 voxels) on lesioned participants
were performed to identify brain regions associated with object and/or space perception impairment, using the z-scores
from the four VOSP tasks as the dependent variables and
lesion status of each voxel as the independent variable. To
ensure sufficient statistical power, only voxels in which at
least four participants had lesions were considered for the
VLSM analyses (Glascher et al., 2009).
Moreover, separate conjunction analyses were performed
for the object and space perception tasks to identify the
regions necessary for each of these tasks, while minimizing
the involvement of other cognitive skills related to the specific
tasks demands. The conjunction analyses yielded three statistical maps: one map revealing brain areas common to the
two tasks and two additional maps showing brain areas
unique to each of the tasks.
Finally, to exclude any potential confounds with verbal
comprehension and language difficulties, one-way analyses of
variance (ANOVAs) were performed on verbal comprehension
(TT) and naming abilities (BN) scores and subgroups (control
group and lesion groups based on the identified lesion pattern
for each tasks) as a between-subjects factor.

3.

Results

3.1.

Behavioral results

Computed tomography (CT) and lesion analysis

Axial CT scans were acquired without contrast on a GE

LightSpeed Plus CT scanner. Images were reconstructed with
an in-plane voxel size of .4 mm  .4 mm, an overlapping slice
thickness of 2.5 mm and a 1-mm slice interval. Lesion location
and extent were evaluated on the scans, and the contours
were drawn on each slice using the Analysis of Brain Lesion
software implemented in MEDx v3.44 (Medical Numerics)
(Makale et al., 2002; Solomon, Raymont, Braun, Butman, &
Grafman, 2007) with enhancements to support the Automated Anatomical Labeling (AAL) atlas (Tzourio-Mazoyer
et al., 2002). Lesion volume was calculated by summing the
traced areas and multiplying by slice thickness. The tracing

Groups (LG, CG) did not differ significantly in demographic,

experimental, and control measures, except for post-injury
general intelligence, which was within the normal range for
both groups, and the cube analysis task. Further, naming
abilities (BN) and verbal comprehension (TT) tended to
significantly differ between groups (Table 1).

3.2.

VLSM results

3.2.1.

Lesion results associated with each VOSP tasks

The lesion density map showed sufficient coverage in most

areas of the temporal, parietal and frontal lobes; allowing the
assessment of the impact of these lesions on the object and

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Table 1 e Descriptive (mean standard deviations) and inferential statistics for demographic, experimental, and control
measures comparing the lesion group (LG [ 192) with the control group (CG [ 55).
Group

LG

Age (years)
Education (years)
Handedness (R : A : L)

58.27  2.96
14.80  2.49
147 : 6 : 21

VOSP Screening task

VOSP Silhouette task
VOSP Object decision task
VOSP Position discrimination task
VOSP Cube analysis task

19.80  0.61
20.10  4.01
17.70  2.08
19.01  1.83
9.37  1.11

Pre-Injury IQ (AFQT, percentile)

Post-Injury IQ (AFQT, percentile)
Token Test (Total correct)
BDI-II (Total score)
Boston Naming Test (Total score)

60.99  25.07
52.72  24.92
97.49  5.86
9.38  9.15
53.44  7.53

CG
Demographic Measures
59.00  3.40
15.19  2.47
43 : 4 : 8
Experimental Measures
19.71  1.45
20.13  3.86
17.80  2.73
19.35  1.80
9.69  0.63
Control Measures
65.40  22.91
68.50  21.63
98.83  1.55
11.56  9.66
55.44  4.73

Statistics
t 1.56, p .121
t 1.00, p .316
c2 7.46, p .113
t
t
t
t
t

0.66,
0.04,
0.28,
1.22,
2.01,

p
p
p
p
p

.509
.970
.777
.224
.046

t
t
t
t
t

0.96,
4.22,
1.67,
1.52,
1.86,

p
p
p
p
p

.336
.001
.097
.129
.064

Age: years at the time of VOSP administration; Education: years at the time of VOSP administration; Handedness: R, right-handed; A, ambidextrous; L, left-handed; Pre-injury Intelligence and Post-injury Intelligence (percentile scores) AFQT: Armed Forces Qualification Test for
general intelligence; Token Test: for basic verbal comprehension; BDI-II: Beck Depression Inventory-II for depression severity; Boston Naming
Test: for object naming; VOSP: Visual Object and Space Perception for object and space perception.

space perception tasks in both hemispheres (Fig. 1) (Note that

brain areas such as the occipital cortex were spared, a prerequisite to allow the participants to complete the tasks.)
The whole brain VLSM analyses revealed brain areas
necessary for each of the four VOSP tasks (Fig. 2) and for the
screening task (Supplementary Fig. S1). For the screening task
the lateral occipital complex (LOC) was associated with task
impairment (Supplementary Fig. S1). For the silhouette task,
behavioral impairment was associated with the left middle
temporal gyrus (MTG), and to a less extent parts of the superior temporal gyrus (STG), inferior temporal gyrus (ITG) and
superior temporal pole (STpole), extending to the boundaries
of the precentral and postcentral gyri (Fig. 2a). For the object
decision task, behavioral impairment was associated with
lesions in the MTG, STG, ITG, along with the frontal operculum
and insula in the left hemisphere (Fig. 2b). For the position
discrimination task, behavioral impairment was associated
with lesions in the inferior frontal gyrus (IFG), middle temporal pole (MidTPole), STpole, ITG, along with the insula,
fusiform gyrus, hippocampus and inferior parietal lobule (IPL)

in the left hemisphere, including the STG and MTG bilaterally.

In the right hemisphere, lesions were found in the superior
frontal gyrus (SFG), premotor area including the supplementary motor area (SMA) and extended to the supramarginal
gyrus (SMG), angular gyrus (AG), IPL, the middle occipital
gyrus (MOG) and superior occipital gyrus (SOG) (Fig 2c). For the
cube analysis task, behavioral impairment was associated
with lesions in the SFG, middle frontal gyrus (MFG), frontal
operculum, insula, and precentral gyrus bilaterally. In the
right hemisphere, lesions were found in the premotor area
including SMA and extended to the STG, MTG, SMG, postcentral gyrus, superior parietal lobule and (SPL), IPL, extending
to the MOG (Fig. 2d). Percentage of lesions (>1%) within each
brain structures that were critical for the each of the four
VOSP tasks in the lesion group are reported in Supplementary
Table 1.

3.2.2.

Lesion results for object perception

Subgroups derived from the VSLM analysis were then tested

to investigate any potential confounds between object

Fig. 1 e Lesion Density Overlap Map for pTBI patients. Axial slices (z-coordinates from L38 to D63 in MNI space) illustrating
the number of overlapping lesions at each voxel across the whole population. All analyses were restricted to a minimum
overlap of 4 patients at a given voxel and the color range indicates this overlap, from blue (4 patients) to red (31 patients).
The maximum overlap of 31 patients occurred in frontal areas. The right hemisphere is on the readers left.

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Fig. 2 e Voxel-Based Lesion Symptom Mapping (VLSM) results for A, Silhouette Task; B, Object Decision Task; C, Position
Discrimination Task; D, Cube Analysis Task. For A, B, C, D, all colored regions are critical for the corresponding task
performance (q(FDR) [ .05, minimum cluster size of 10 voxels). Color range displays z-scores, from red (minimum z-score
displayed on the right side) to yellow (maximum z-score). Axial slices display z-coordinates from L38 to D63 in MNI space.
The right hemisphere is on the readers left.

perception tasks and verbal comprehension and naming

abilities: a silhouette group (n 19) with brain lesions associated with both tasks (i.e., silhouette & object decision task); an
object decision group (n 136) with brain lesions associated
with the object decision task, and a normal control group
(n 55) serving as a baseline group for normal verbal
comprehension and language processing (Supplementary
Table 2). The one-way ANOVAs on language test scores
showed a main Group effect (BN: F(2,107) 13.60, p < .01; TT:
F(2,106) 10.77, p < .01). Follow-up post-hoc comparisons
demonstrated that only the performance of the silhouette
group differed significantly from the performances of the
other two groups (Ps < .01, after Bonferroni correction).
Given the potential confound of verbal comprehension and
naming abilities in the silhouette group, a subtraction analysis
(object decision task > silhouette task) was performed to
remove the explicit verbal component involved in the
silhouette task and to isolate only those brain areas involved
in object perception as measured by the object decision task.
The subtraction analysis revealed a left hemispheric network:

STG (Brodmann area, BA 22), ITG (BA 20), frontal operculum,

and insula (BA 13) (Fig. 3a).

3.2.3.

Lesion results for space perception

As for the object group, subgroups derived from the VSLM

analysis were tested to investigate any potential confounds
between space perception tasks and verbal comprehension and
naming abilities: a position discrimination group (n 10) with
patients whose brain lesions were associated only with the
position discrimination task, a cube analysis group (n 40) with
patients whose brain lesions were associated only with the cube
analysis task, a combined group (n 120) with patients whose
brain lesions were associated with both tasks, and a normal
control group (n 55) serving as a baseline group for normal
verbal comprehension and language processing. Note that all
patients having lesions for object-related tasks were included in
the group of patients having lesion for the space tasks.
The one-way ANOVAs on language test scores (BN and TT)
revealed no significant main effect of Group [BN:
F(3,217) 1.83, p .09; F(3, 214) 1.66, p .09] (Supplementary

c o r t e x 5 7 ( 2 0 1 4 ) 2 4 4 e2 5 3

249

Fig. 3 e Conjunction Maps for A, Object perception, and B, Space perception. Lesions resulting from conjunction analyses are
areas of damage associated with space perception and object perception tasks. A, Unique brain regions for the object
decision task. B, Overlapping brain regions for the two space perception tasks (position discrimination and cube analysis).
Axial slices display z-coordinates from L38 to D63 in MNI space. The right hemisphere is on the readers left.

Table 2). Given the null main effect, a conjunction analysis

(position discrimination task X cube analysis task) was performed to identify brain regions commonly involved in the
two space perception tasks. The analysis found brain regions
critical for the perception of spatial relationships in 2D and 3D
representations and excluded brain regions that may be linked
to more specific task-related cognitive demands (e.g., counting, responding verbally, evaluating distance, and pointing).
The conjunction analysis revealed a network lateralized to
the right hemisphere (Fig. 3b): posterior part of the superior
and medial frontal gyri extending to the precentral gyrus,
premotor area including SMA (BA 6), postcentral gyrus (BA 2
and 3), insula (BA 13), and MOG (BA 19), extending to the
boundaries of the MTG (BA 19), SMG (BA 40), and IPL (BA 40). In
addition, a discrete region in the IFG (BA 47) of the left hemisphere was found. Among these regions, the largest cluster
affecting space perception performance was found within the
right IPL.

4.

Discussion

The aim of the study was to investigate the neural underpinnings of object and space perception using VLSM
analysis in a large pTBI cohort. Our findings identified distinct
and lateralized brain regions critical for object and space
perception within the left ventral stream and the right dorsal
stream, respectively. These results support the functional
subdivision of the visual system and shed new light on the
specific processes involved along both the dorsal and ventral
streams.

4.1.

Object perception and ventral stream

Object recognition has been described as a hierarchical

process (Ungerleider & Haxby, 1994), where posterior regions
of the ventral stream process low-level features of an object

(Grill-Spector et al., 1999), and more anterior regions integrate

those basic features into a more abstract representation
necessary for the object to acquire a meaning (semantic processing) (Ungerleider & Mishkin, 1982). The right and
left hemispheres are thought to be differentially involved
in these stages e right brain-damaged patients were found to
be impaired on perceptual processing (apperceptive agnosia),
whereas left brain-damaged patients were found to be
impaired in semantic processing (associative agnosia) (De
Renzi, 2000; De Renzi, Scotti, & Spinnler, 1969; Warrington &
Taylor, 1978). Regions of left posterior temporal cortex,
including the fusiform gyrus, the ITG and the MTG, were
found to be activated during conceptual processing of both
pictures and words in several neuroimaging studies
(Bookheimer, 2002; Thompson-Schill, 2003; Vandenberghe,
Price, Wise, Josephs, & Frackowiak, 1996; Xu, Gannon,
Emmorey, Smith, & Braun, 2009). Focal damage in this area
can lead to a loss of conceptual knowledge, including difficulties in object naming even in the absence of diagnosed
aphasia (Newcombe, Oldfield, Ratcliff, & Wingfield, 1971).
Despite this literature supporting a left hemispheric
dominance in object processing at the level of meaning, the
majority of case studies documenting visual form agnosia
describe patients with diffuse bilateral brain damage (James,
Culham, Humphrey, Milner, & Goodale, 2003; Karnath, Ruter,
Mandler, & Himmelbach, 2009). Recently, Konen et al. (2011)
reported a comprehensive case study of patient SM who suffered from object agnosia and prosopagnosia following a circumscribed lesion in the right posterior lateral fusiform gyrus.
Using fMRI, the authors found impaired object-related activation at sites both proximal and distal to the lesion (in both
the temporal and parietal cortex) compared to controls.
Interestingly, the unilateral lesion also altered object-related
activation in the intact left hemisphere, leading the authors
to argue that the proximal and distal induced impairments
following a unilateral lesion essentially mimicked a bilateral
lesion.

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How do our results fit with this framework? First, we did

not include patients suffering from visual agnosia, and
instead investigated performance in various object recognition tasks in a large sample of patients with lesions that
covered critical brain regions in both hemispheres. Second,
we included only patients whose basic visual discrimination
abilities were intact, as only those who passed the detection
screening task were included. With the silhouette and object
decision tasks, we assessed the subjects ability to recognize
more complex objects. Indeed, for the initial stage of object
perception we found the right LOC as a critical brain region,
while brain structures necessary for object recognition were
identified more anteriorly and were restricted to the left
hemisphere. For the silhouette task, our VSLM analysis uncovered the left MTG as a necessary region for naming the
presented objects. For the object decision task, we identified a
more widespread network e including the MTG that extended
to the STG, along with the frontal operculum and the insula e
necessary for selecting the meaningful object among distractors. Since only patients with lesions associated with the
silhouette task differed from patients with lesion associated
with the object decision task and healthy controls in verbal
comprehension and naming abilities (as measured by the
Boston Naming and Token Tests), it is possible that the
involvement of the left MTG is related to naming difficulties
(Baldo, Arevalo, Patterson, & Dronkers, 2013).
Yet, altogether, using a large sample of patients and a
whole brain approach, our data are in line with the abundant
literature supporting a hierarchical organization in the ventral
stream, and they also bring new support for the complementary role of both hemispheres in object recognition. We
found that the ability to discriminate simple shapes depended
on the integrity of the right LOC, while the ability to recognize
more complex objects (in the silhouette and the object decision tasks) depended on the integrity of more anterior temporal and frontal regions in the left hemisphere. In addition,
our results suggest that, in object recognition, different regions may be recruited depending on the task demand. It is
possible that the more widespread network identified in the
object decision task compared to the silhouette task was
associated with an increase in task demand. Along this line, it
has been shown that activity in the temporal lobes increases
and spreads more anteriorly (Bar et al., 2001) as more information about the objects identity is gained. Similarly, a shift
of activations from STG to the MTG appears when conscious
object recognition takes place (Martens, Wahl, Hassler, Friese,
& Gruber, 2012). In addition, recent neuroimaging results have
shown that bilateral activation of the frontal operculum and
the insula regions were associated with perceptual recognition when stimuli were gradually revealed to the subjects
(Ploran et al., 2007), and degree of activation for those brain
regions may be associated with stimulus complexity and
saliency (Sterzer & Kleinschmidt, 2010). While neuroimaging
findings only determine the involvement of brain regions, our
VLSM results identified the left frontal operculum and the
insula as necessary regions for object recognition in a context
where a perceptual decision was influenced by the presence of
distractors.
Object recognition is subserved by distributed and interconnected brain regions in the ventral stream (Kravitz et al.,

2013), and while our study helped identify critical nodes

along this stream, the precise neural mechanisms occurring
within and between these different regions still remain to be
understood. Surprisingly, critical substrates subserving object
recognition uncovered by our VLSM study did not include the
IFG as typically reported by neuroimaging studies (Haxby
et al., 1991; Konen & Kastner, 2008), despite the presence of
a lesion in this part of the brain in a significant number of
patients. It is therefore possible that compared to regions in
the temporal lobes, the role of the IFG may be more related to
other aspects of object recognition not measured by our tasks,
such as tasks involving top-down attentional control (Bar
et al., 2001). For instance, compared to the temporal regions,
Bar et al. (2001) showed that IFG activity is associated with
recognition ratings in conditions where the stimuli were
masked.

4.2.

Space perception and dorsal stream

The dorsal stream, dedicated to space perception, was originally described as an occipito-parietal circuit projecting from
the early visual cortical areas to the posterior regions of the
parietal cortex (Goodale & Milner, 1992; Ungerleider &
Mishkin, 1982). A new framework has recently been formulated, and describes three different pathways originating from
the PPC that mediate spatial perception and visually guided
actions (Kravitz et al., 2011). Within the dorsal pathway, the
right parietal cortex acts as a fundamental nexus and the large
body of evidence from neglect patients has brought unequivocal support for its role in space perception and visuospatial
attention (Bartolomeo, Thiebaut de Schotten, & Chica, 2012;
De Renzi, 1982; Kinsbourne, 1987; McCarthy & Warrington,
1990; Mesulam, 1981). Contrary to the ongoing debate about
the lateralization of the ventral stream, the right hemispheric
dominance for space perception is well established, and the
study of the neglect patients has largely contributed to this
knowledge (Taylor & Warrington, 1973). Evidence for the
dorsal stream lateralization has also been repeatedly reported
in healthy subjects. For instance, TMS on the right PPC induces neglect-like behavior (Brighina et al., 2002; Fierro et al.,
2000) and enhances ipsilateral detection compared to that
elicited by left hemisphere stimulation (Hilgetag et al., 2001).
In addition, the volume of the longitudinal parieto-frontal
tract identified as the superior longitudinal fasciculus II was
found to be larger in the right hemisphere compared to the left
hemisphere, and this asymmetry correlates with a deviation
toward the left in a line bisection task (Thiebaut de Schotten
et al., 2011).
In line with these findings, we identified a set of brain regions in the right hemisphere necessary for space perception
using two different space recognition tasks, including regions
from the PPC to the precentral gyrus, premotor area (BA 6) to the
postcentral gyrus (BA 2 and 3), and the insula (BA 13). One
critical lesion site associated with space perception impairment
was the right IPL. This region, known to receive vestibular inputs from the cerebellum (Clower, Dum, & Strick, 2005; Clower,
West, Lynch, & Strick, 2001), is strongly connected with somatosensory areas (Lewis & Van Essen, 2000), and maintains
visual somatotopic maps (Ishida, Nakajima, Inase, & Murata,
2009). Maintaining a continuously aligned representation of

c o r t e x 5 7 ( 2 0 1 4 ) 2 4 4 e2 5 3

visual coordinates relative to the location of body parts is

essential not only for visually guided action in peripersonal
space (Milner & Goodale, 2008), but also for accurate space
perception (Sirigu, Grafman, Bressler, & Sunderland, 1991). Our
results are also in agreement with a previous VLSM study
showing that the right PPC is necessary for visuospatial processing as measured by the block design task, a subtest of the
WAIS battery (Glascher et al., 2009) (see Behrmann, Geng, &
Shomstein, 2004 for a review).
In addition to the IPL, another critical region for space
perception was the premotor area (BA 6). The involvement of
this region has been reported in previous functional neuroimaging studies employing a task similar to our VOSP position
discrimination task (Ungerleider & Haxby, 1994) and a task
involving visuospatial attention (Corbetta, Miezin, Shulman,
& Petersen, 1993). According to a recent model, the dorsal
stream is subdivided into three separate pathways: parietoprefrontal, parieto-premotor and parieto-medial temporal
pathways (Kravitz et al., 2011). Our conjunction analysis
revealed that lesions associated with space perception overlap
with the parieto-premotor pathway (Kravitz et al., 2011). This
parieto-premotor pathway mediates not only reaching and
grasping (Fattori et al., 2009, 2010; Galletti et al., 2001), but also
eye movements (Nachev, Kennard, & Husain, 2008) and other
forms of visually guided action, along with the ability to
maintain coordinated maps of space and body position
(Kravitz et al., 2011). Our findings pointed to the critical role of
the parieto-premotor pathway in the perception of spatial
relationships in both 2D and 3D representations as it was a
common region for both space perception tasks in the absence
of visually guided action, reaching or grasping; therefore, its
general role may be of maintaining coordinated maps of space
and body position (Kravitz et al., 2011).

4.3.

Conclusion

Our findings added novel support for the necessary involvement of a left temporo-frontal network for object perception
and a right parieto-premotor network for space perception.
Even though our results showed a different hemispheric
dominance for both the ventral and dorsal stream, this does
not preclude any possible interaction between the two streams
(Konen & Kastner, 2008; Kravitz et al., 2013; Ungerleider &
Haxby, 1994; Zachariou, Klatzky, & Behrmann, 2013). It is
possible that both our analysis strategy and the specifics of our
sample did not allow us to uncover the structure(s) common to
both visual streams. Given the nature of the lesions in our pTBI
population, brain injuries were not randomly distributed (i.e.,
some brain areas were over- and others under-represented)
and covariation of damage across brain regions cannot be
excluded. As age has been shown to have an influence on most
of the VOSP tasks (Bonello, Rapport, & Millis, 1997), the fact
that our sample included only elderly adults is a limitation, as
well as the chronicity of their brain lesions. In fact, all patients
were studied more than 35 years after the brain injury, and it is
therefore possible that some functional recovering may have
affected our findings. Finally, our lesion data were entirely
based on CT scans which has lower resolution and less capacity to discriminate between grey and white matter
compared to MRI. Despite these limitations, the results from

251

our study constituted compelling evidence supporting the

functional subdivision of the visual system in humans. They
also added novel support to the hemispheric dominance of
these visual streams. In conclusion, our results derived from a
large cohort of pTBI patients by implementing a whole brain
lesion-based symptom mapping approach to identify brain
regions necessary for object and space perception (Rorden &
Karnath, 2004) added new knowledge to the literature and
allowed the inference of more direct causal relationships between brain and behavior. Importantly, our results corroborated evidence from both neuropsychological studies, which
are often single case studies, and functional neuroimaging
studies, which are an excellent tool for studying brain areas
involved in a particular process/task; however, its power is
limited when it comes to making inferences about brain areas
that are necessary for the task.

Acknowledgments
The work was supported by the U.S. National Institute of
Neurological Disorders and Stroke intramural research program, and a project grant from the United States Army Medical Research and Material Command administrated by the
Henry M. Jackson Foundation (Vietnam Head Injury Study
Phase III: a 30-year post-injury follow-up study, Grant
DAMD17-01-1-0675). Selene Schintu was supported with
funding from the Henry M. Jackson Foundation, and Fadila
Hadj-Bouziane by the NEURODIS Foundation. The authors are
grateful to all the Vietnam veterans who participated in this
study and the National Naval Medical Center for their support
and provision of facilities, as well as V. Raymont, S. Bonifant,
B. Cheon, C. Ngo, A. Greathouse, K. Reding, and G. Tasick for
their invaluable help with the testing of participants and organization of this study. Note that the views expressed in this
article are those of the authors and do not necessarily reflect
the official policy or position of the Department of the Navy,
the Department of Defense, nor the U.S. Government. For
further information about the Vietnam Head Injury Study,
contact J. G. at [email protected]. The authors
declare that the research was conducted in the absence of any
commercial or financial relationships that could be construed
as a potential conflict of interest.

Supplementary data
Supplementary data related to this article can be found at
http://dx.doi.org/10.1016/j.cortex.2014.04.009.

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