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Experiments using functional magnetic resonance imaging (fMRI) have revealed that the ventral and lateral occipitotemporal cortices (VOTC and LOTC, respectively), areas often associated with high-level visual processing ([Grill-Spector and Malach, 2004][1]), show preferential activation during the
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Journal Club
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Semantic Organization of Body Part Representations in the
Occipitotemporal Cortex
XArran T. Reader
School of Psychology and Clinical Language Sciences, University of Reading, Reading, RG6 6AL, United Kingdom
Review of Bracci et al.
Experiments using functional magnetic
resonance imaging (fMRI) have revealed
that the ventral and lateral occipitot-
emporal cortices (VOTC and LOTC,
respectively), areas often associated with
high-level visual processing (Grill-
Spector and Malach, 2004), show prefer-
ential activation during the observation
of body parts. Early results examining
preferential brain activation during ob-
servation of body parts highlighted the
importance of a region in the LOTC. This
was termed the extrastriate body area
(EBA) by Downing et al. (2001), who
found that this region responded more
strongly to images of body parts than to
various control stimuli. Supporting these
results, Urgesi et al. (2004) applied trans-
cranial magnetic stimulation over EBA,
which resulted in a reduced ability to dis-
criminate between body parts. More re-
cently, Bracci et al. (2010) found an area of
the LOTC that responded preferentially to
the observation of hands, suggesting that
body part representation in the OTC is
likely to be heterogeneous.
While the organization of body part
representations (i.e., somatotopy) in the
somatosensory and motor cortices is well
established, little evidence existed for sim-
ilar organization in the OTC until rela-
tively recently. Orlov et al. (2010) found
that distinct areas of the OTC represented
different visually presented body parts.
They also showed that the organization of
these representations was not accounted
for simply by the shape of the body parts.
Such findings suggested that body part
representations in the LOTC and VOTC
might be organized according to one or
more criteria, for example shape or func-
tion. In a recent issue of The Journal of
Neuroscience,Bracci et al. (2015) further
examined how body-part-related activity
in the OTC is organized. Using fMRI and
a technique called representational simi-
larity analysis (RSA; Kriegeskorte et al.,
2008), they tested five different models of
body part organization in the OTC. Their
results revealed that a model based on se-
mantic similarity best accounted for the
organization of body part representations
in the OTC.
Bracci and colleagues (2015) showed
participants images of whole bodies,
hands, feet, arms, legs, chests, waists, up-
per faces, lower faces, and chairs, while
they performed a one-back repetition
detection task and fMRI data were col-
lected. Regions of interest (ROIs) in the
LOTC and VOTC were defined in each
participant by contrasting the blood-
oxygenation level dependent (BOLD) re-
sponse to whole bodies versus chairs.
ROIs within the OTC were found in both
hemispheres for all participants. Control
regions in the occipital cortex (OC) were
defined by the opposite contrast: chairs
versus whole bodies. Multivoxel pattern
analysis, a tool for comparing patterns of
activation across multiple voxels, was
then used to compare the similarities of
activation among the eight remaining
body part activations in the LOTC and
VOTC. These patterns were correlated
across the different body parts to create an
eight-by-eight neural dissimilarity matrix
(Bracci et al., 2015, their Fig. 3A).
The authors used RSA, which involves
comparing dissimilarity matrices between
a model and measured brain activation
(Fig. 1). Using RSA, different theoretical
models can be compared to discover the
degree to which each can explain the ob-
served brain activity. To use RSA, the au-
thors created dissimilarity matrices for
five possible models of body part organi-
zation: physical shape similarity (com-
puted using the shape context algorithm;
Belongie et al., 2002), perceived shape
similarity (based on six independent par-
ticipants’ arrangement of body parts
based on shape similarity), physical prox-
imity in the body, organization following
the cortical sensory and motor homun-
culi, and semantic similarity (Bracci et al.,
2015, their Fig. 2A). These dissimilarity
matrices were then compared statistically
with the neural dissimilarity matrices of
each of the four ROIs (left and right LOTC
and VOTC).
In the primary analyses, the authors
replicated the body-part-specific activa-
tion of OTC reported previously. More-
over, they found that only the perceived
Received Oct. 14, 2015; revised Nov. 19, 2015; accepted Nov. 23, 2015.
Many thanks to Dr. Nicholas P. Holmes for his comments on the manu-
script, and for his continued supervision and support.
The author declares no competing financial interests.
Correspondence should be addressed to Arran T. Reader, School of
Psychology and Clinical Language Sciences, University of Reading, Ear-
ley Gate, Whiteknights Road, Reading, RG6 6AL, UK. E-mail:
Copyright © 2016 the authors 0270-6474/16/360265-03$15.00/0
The Journal of Neuroscience, January 13, 2016 36(2):265–267 • 265
shape, physical proximity, and semantic
similarity models were significantly and
positively related to neural similarity in
the LOTC and VOTC. The physical shape
and cortical homunculus models failed to
account for any additional variance in the
neural similarity. When these models
were directly compared, however, the
semantic similarity model was signifi-
cantly more related to neural similarity
than any of the other models, suggesting
that the organization of body part repre-
sentations in the LOTC and VOTC is at
least partly semantic. In examining the
neural dissimilarity matrices, the authors
found three distinctly organized clusters:
effectors (hands, feet, legs, arms), nonef-
fectors (chests, waists), and faces (upper
faces, lower faces). To check if nearby re-
gions showed complementary organiza-
tion, the analysis was performed again on
the left and right OC (control ROIs). Per-
haps unsurprisingly, considering the
importance of the occipital cortex in pro-
cessing lower-level visual stimuli, only the
shape similarity models were significantly
related to patterns of BOLD response in
these areas.
Bracci et al. (2015) provide evidence
that the organization of body part repre-
sentations in the OTC is at least partially
semantic, though such a model alone
could not fully explain the neural similar-
ity. As the authors note, this may have
been due to “imperfections in the models
and/or the existence of additional organi-
zational principles that we did not con-
sider” (p. 12983). The former may be
most likely, considering that the method
by which the semantic similarity model
was defined (frequency of body part word
co-occurrence in written text) may not
adequately reflect the way in which such
semantic similarity is represented in the
OTC. It may be the case that semantic or-
ganization in the OTC is quite different
than that which can be found in the distri-
bution of words in text. For example,
while the combination of body parts in
text may reflect a wide variety of possible
functions (i.e., both feet and hands being
used in climbing, or both hand and
mouth being used in eating), their repre-
sentation in the OTC may be related to
more specific general functions such as
expressing emotion, or moving aversive/
attractive stimuli away from/towards the
body. This may also explain why the phys-
ical proximity model was also positively
associated with neural similarity because,
for example, hands are almost always used
in combination with the arms.
Regardless of how the semantic model
was generated, the clusters of organiza-
tion within the LOTC and VOTC (effec-
tors, noneffectors, faces) did indeed
suggest an organization based on func-
tion. Tools (objects used as effectors) are
represented close to body effectors in the
OTC, and these regions are functionally
connected to the left intraparietal sulcus
(IPS) and left premotor cortex (Bracci et
al., 2012). Interestingly, a whole-brain
analysis run by Bracci et al. (2015) re-
vealed additional clusters of frontal and
parietal activation that were significantly
and positively associated with the seman-
tic similarity model once it was contrasted
with the other four models. These areas
were the left and right superior parietal
lobule, left inferior parietal lobule, left
ventral premotor cortex, and left dorsal
premotor cortex. This may provide
greater insight into the role of these areas
in action perception and execution. Cer-
tainly, it supports the claim that the OTC
is functionally connected to these regions.
This association could be a reflection of
the sensorimotor and functional similar-
ity of body part representations seen in
these areas (Rizzolatti and Craighero,
2004), but it may also highlight overlap-
ping pathways relevant for semantic
meaning and action processing. For ex-
ample, the left IPS has been implicated
both in the processing of words and ob-
jects (Devereux et al., 2013) and in the
representation of observed action goals
(Hamilton and Grafton, 2006).
Bracci et al. (2015) posited that seman-
tic organization in the OTC could be a
function of connectivity demands. Body
part information related to action would
feedforward to downstream motor areas,
while areas representing faces would be
strongly connected to regions involved in
social cognition. These claims may be
supported by new findings in studies on
the movement disorder limb apraxia,
which indicate that damage to the OTC
often underlies defective pantomimed
tool use, defective imitation of panto-
mimes, and defective imitation of mean-
ingless gestures (Buxbaum et al., 2014;
Hoeren et al., 2014). In addition, lesions
to the OTC have been implicated in im-
paired (tool-related) action recognition
(Tarhan et al., 2015). Such results confirm
Figure 1. Simplified overview of RSA as used by Bracci et al. (2015). Correlation-based multivoxel pattern analysis can be used
to determine voxelwisedissimilarity between neural activity related to the stimuli a– d.This is used to create a neural dissimilarity
matrix. A dissimilarity matrix is a square, symmetrical matrix that compares the similarity between pairs of elements. Diagonal
pairs (showing the dissimilarity between an element and itself) are defined as zero. The neural dissimilarity matrix can be
comparedtothedissimilaritymatricesposited by a number of models (in this example, model 1 and model 2). InthecaseofBracci
et al. (2015), the authors used a multiple regression (for each individual participant) using the model dissimilarity matrices as
dependent variables and the neural dissimilarity matrices as independent variables. Differences between the computed regres-
sion coefficients were compared using pairwise ttests to reveal which models best explained the neural dissimilarity. This
resulted in bar graphs similar to that seen in this figure, which emphasize the degree to which each model can be related
to the observed brain activity shown in the neural dissimilarity matrix, with beta estimating the explanatory contribution
of each regressor (in this case, the two models).
266 J. Neurosci., January 13, 2016 36(2):265–267 Reader Journal Club
the idea that regions in the OTC could act
as an upstream hub for multiple tasks
reliant on body part recognition. Net-
works that include the OTC could have a
semantic structure built in from the very
beginning. Take action recognition as an
example. Processing of the semantic as-
pects of action recognition is sometimes
considered to rely on top-down cognition
(Wurm et al., 2014;Davey et al., 2015).
The results of Bracci et al. (2015) suggest
that the way in which semantic and visual
information are integrated for the pur-
pose of action recognition may not rely
primarily on top-down processing. If re-
gions with semantic organization in the
OTC and other areas (i.e., IPS, premotor
cortex) are functionally linked, then the
semantic nature of the observed stimu-
lus could be derived from the pathway
through which the stimulus information
travels. Therefore, broad semantic infor-
mation regarding the action context may
in fact be integrated much earlier, follow-
ing the observation of body parts. A recent
study by Wurm and Lingnau (2015) ap-
pears to support this claim, but more
work is needed to confirm the hypothesis.
Bracci et al. (2015) have increased our
understanding of how body parts are rep-
resented in the OTC. They indicate that
semantic information regarding the pos-
sible context in which body parts are ob-
served may be available surprisingly
early, during visual processing, due in
part to the organization of visual pro-
cessing regions. More importantly, their
results have implications for how we
discuss tasks reliant on body part recog-
nition. Further study of the semantic or-
ganization in OTC could shed new light
on processes as varied as action recogni-
tion and imitation, or even social cogni-
tion as a whole.
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Reader Journal Club J. Neurosci., January 13, 2016 36(2):265–267 • 267
... 134). In fact, action recognition could be principally subserved by occipitotemporal regions (Lingnau & Downing, 2015;Peelen & Downing, 2017), as recent evidence suggests that visual representations of body parts and action in this area are organised in terms of semantics, transitivity, and sociality (Bracci, Caramazza, & Peelen, 2015;Wurm, Caramazza, & Lingnau, 2017), and that the structure of these representations could possibly assist in higher-level social cognition in a bottom-up manner (Reader, 2016). Previous VLSM approaches to deficits in gesture recognition, particularly for semantic aspects of action, reflect the importance of these regions (Kal enine, Buxbaum, & Coslett, 2010). ...
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The inferior frontal gyrus and inferior parietal lobe have been characterized as human homologues of the monkey "mirror neuron" system, critical for both action production (AP) and action recognition (AR). However, data from brain lesion patients with selective impairment on only one of these tasks provide evidence of neural and cognitive dissociations. We sought to clarify the relationship between AP and AR, and their critical neural substrates, by directly comparing performance of 131 chronic left-hemisphere stroke patients on both tasks-to our knowledge, the largest lesion-based experimental investigation of action cognition to date. Using voxel-based lesion symptom mapping, we found that lesions to primary motor and somatosensory cortices and inferior parietal lobule were associated with disproportionately impaired performance on AP, whereas lesions to lateral temporo-occipital cortex were associated with a relatively rare pattern of disproportionately impaired performance on AR. In contrast, damage to posterior middle temporal gyrus was associated with impairment on both AP and AR. The distinction between lateral temporo-occipital cortex, critical for recognition, and posterior middle temporal gyrus, important for both tasks, suggests a rough gradient from modality-specific to abstract representations in posterior temporal cortex, the first lesion-based evidence for this phenomenon. Overall, the results of this large patient study help to bring closure to a long-standing debate by showing that tool-related AP and AR critically depend on both common and distinct left hemisphere neural substrates, most of which are external to putative human mirror regions.
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Brain regions that mediate action understanding must contain representations that are action specific and at the same time tolerate a wide range of perceptual variance. Whereas progress has been made in understanding such generalization mechanisms in the object domain, the neural mechanisms to conceptualize actions remain unknown. In particular, there is ongoing dissent between motor-centric and cognitive accounts whether premotor cortex or brain regions in closer relation to perceptual systems, i.e., lateral occipitotemporal cortex, contain neural populations with such mapping properties. To date, it is unclear to which degree action-specific representations in these brain regions generalize from concrete action instantiations to abstract action concepts. However, such information would be crucial to differentiate between motor and cognitive theories. Using ROI-based and searchlight-based fMRI multivoxel pattern decoding, we sought brain regions in human cortex that manage the balancing act between specificity and generality. We investigated a concrete level that distinguishes actions based on perceptual features (e.g., opening vs closing a specific bottle), an intermediate level that generalizes across movement kinematics and specific objects involved in the action (e.g., opening different bottles with cork or screw cap), and an abstract level that additionally generalizes across object category (e.g., opening bottles or boxes). We demonstrate that the inferior parietal and occipitotemporal cortex code actions at abstract levels whereas the premotor cortex codes actions at the concrete level only. Hence, occipitotemporal, but not premotor, regions fulfill the necessary criteria for action understanding. This result is compatible with cognitive theories but strongly undermines motor theories of action understanding. Copyright © 2015 the authors 0270-6474/15/357727-09$15.00/0.
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Apraxia is a cognitive disorder of skilled movements that characteristically affects the ability to imitate meaningless gestures, or to pantomime the use of tools. Despite substantial research, the neural underpinnings of imitation and pantomime have remained debated. An influential model states that higher motor functions are supported by different processing streams. A dorso-dorsal stream may mediate movements based on physical object properties, like reaching or grasping, whereas skilled tool use or pantomime rely on action representations stored within a ventro-dorsal stream. However, given variable results of past studies, the role of the two streams for imitation of meaningless gestures has remained uncertain, and the importance of the ventro-dorsal stream for pantomime of tool use has been questioned. To clarify the involvement of ventral and dorsal streams in imitation and pantomime, we performed voxel-based lesion-symptom mapping in a sample of 96 consecutive left-hemisphere stroke patients (mean age ± SD, 63.4 ± 14.8 years, 56 male). Patients were examined in the acute phase after ischaemic stroke (after a mean of 5.3, maximum 10 days) to avoid interference of brain reorganization with a reliable lesion-symptom mapping as best as possible. Patients were asked to imitate 20 meaningless hand and finger postures, and to pantomime the use of 14 common tools depicted as line drawings. Following the distinction between movement engrams and action semantics, pantomime errors were characterized as either movement or content errors, respectively. Whereas movement errors referred to incorrect spatio-temporal features of overall recognizable movements, content errors reflected an inability to associate tools with their prototypical actions. Both imitation and pantomime deficits were associated with lesions within the lateral occipitotemporal cortex, posterior inferior parietal lobule, posterior intraparietal sulcus and superior parietal lobule. However, the areas specifically related to the dorso-dorsal stream, i.e. posterior intraparietal sulcus and superior parietal lobule, were more strongly associated with imitation. Conversely, in contrast to imitation, pantomime deficits were associated with ventro-dorsal regions such as the supramarginal gyrus, as well as brain structures counted to the ventral stream, such as the extreme capsule. Ventral stream involvement was especially clear for content errors which were related to anterior temporal damage. However, movement errors were not consistently associated with a specific lesion location. In summary, our results indicate that imitation mainly relies on the dorso-dorsal stream for visuo-motor conversion and on-line movement control. Conversely, pantomime additionally requires ventro-dorsal and ventral streams for access to stored action engrams and retrieval of tool-action relationships. © The Author (2014). Published by Oxford University Press on behalf of the Guarantors of Brain. All rights reserved. For Permissions, please email: [email protected] /* */
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Executive-semantic control and action understanding appear to recruit overlapping brain regions but existing evidence from neuroimaging meta-analyses and neuropsychology lacks spatial precision; we therefore manipulated difficulty and feature type (visual vs. action) in a single fMRI study. Harder judgements recruited an executive-semantic network encompassing medial and inferior frontal regions (including LIFG) and posterior temporal cortex (including pMTG). These regions partially overlapped with brain areas involved in action but not visual judgements. In LIFG, the peak responses to action and difficulty were spatially identical across participants, while these responses were overlapping yet spatially distinct in posterior temporal cortex. We propose that the co-activation of LIFG and pMTG allows the flexible retrieval of semantic information, appropriate to the current context; this might be necessary both for semantic control and understanding actions. Feature selection in difficult trials also recruited ventral occipital-temporal areas, not implicated in action understanding.
Regions in human lateral and ventral occipitotemporal cortices (OTC) respond selectively to pictures of the human body and its parts. What are the organizational principles underlying body part responses in these regions? Here we used representational similarity analysis (RSA) of fMRI data to test multiple possible organizational principles: shape similarity, physical proximity, cortical homunculus proximity, and semantic similarity. Participants viewed pictures of whole persons, chairs, and eight body parts (hands, arms, legs, feet, chests, waists, upper faces, and lower faces). The similarity of multivoxel activity patterns for all body part pairs was established in whole person-selective OTC regions. The resulting neural similarity matrices were then compared with similarity matrices capturing the hypothesized organizational principles. Results showed that the semantic similarity model best captured the neural similarity of body parts in lateral and ventral OTC, which followed an organization in three clusters: (1) body parts used as action effectors (hands, feet, arms, and legs), (2) noneffector body parts (chests and waists), and (3) face parts (upper and lower faces). Whole-brain RSA revealed, in addition to OTC, regions in parietal and frontal cortex in which neural similarity was related to semantic similarity. In contrast, neural similarity in occipital cortex was best predicted by shape similarity models. We suggest that the semantic organization of body parts in high-level visual cortex relates to the different functions associated with the three body part clusters, reflecting the unique processing and connectivity demands associated with the different types of information (e.g., action, social) different body parts (e.g., limbs, faces) convey.
When a child reaches toward a cookie, the watching parent knows immediately what the child wants. The neural basis of this ability to interpret other people's actions in terms of their goals has been the subject of much speculation. Research with infants has shown that 6 month olds respond when they see an adult reach to a novel goal but habituate when an adult reaches to the same goal repeatedly. We used a similar approach in an event-related functional magnetic resonance imaging experiment. Adult participants observed a series of movies depicting goal-directed actions, with the sequence controlled so that some goals were novel and others repeated relative to the previous movie. Repeated presentation of the same goal caused a suppression of the blood oxygen level-dependent response in two regions of the left intraparietal sulcus. These regions were not sensitive to the trajectory taken by the actor's hand. This result demonstrates that the anterior intraparietal sulcus represents the goal of an observed action.
The perception of object-directed actions performed by either hands or tools recruits regions in left fronto-parietal cortex. Here, using functional MRI (fMRI), we tested whether the common role of hands and tools in object manipulation is also reflected in the distribution of response patterns to these categories in visual cortex. In two experiments we found that static pictures of hands and tools activated closely overlapping regions in left lateral occipitotemporal cortex (LOTC). Left LOTC responses to tools selectively overlapped with responses to hands but not with responses to whole bodies, nonhand body parts, other objects, or visual motion. Multivoxel pattern analysis in left LOTC indicated a high degree of similarity between response patterns to hands and tools but not between hands or tools and other body parts. Finally, functional connectivity analysis showed that the left LOTC hand/tool region was selectively connected, relative to neighboring body-, motion-, and object-responsive regions, with regions in left intraparietal sulcus and left premotor cortex that have previously been implicated in hand/tool action-related processing. Taken together, these results suggest that action-related object properties shared by hands and tools are reflected in the organization of high-order visual cortex. We propose that the functional organization of high-order visual cortex partly reflects the organization of downstream functional networks, such as the fronto-parietal action network, due to differences within visual cortex in the connectivity to these networks.