Cerebral Cortex February 2010;20:486--491
doi:10.1093/cercor/bhp117
Advance Access publication June 22, 2009
Cerebellar Engagement in an Action
Observation Network
Arseny A. Sokolov1, Alireza Gharabaghi1,2, Marcos S. Tatagiba1
and Marina Pavlova3,4
Department of Neurosurgery, 2Neuroprosthetics Research
Group, Werner Reichardt Centre for Integrative Neuroscience,
3
Department of Pediatric Neurology and Child Development,
Children’s Hospital and 4Institute of Medical Psychology and
Behavioral Neurobiology, MEG Center, University of Tübingen
Medical School, D72076 Tübingen, Germany
1
The cerebellum has traditionally been viewed as a brain structure
subserving skilled motor behaviors. However, the cerebellum might
be involved not only in movement coordination, but also in action
observation and understanding of others’ actions. Veridical visual
perception of human body motion is of immense importance for a
variety of daily-life situations and for successful social interactions.
Here, by combining visual psychophysics with a lesion analysis, we
assessed visual sensitivity to human walking in patients with
lesions to the left cerebellum. Patients with left lateral cerebellar
lesions exhibit deficits in visual sensitivity to body motion, whereas
medial lesions do not substantially affect visual perception of
human locomotion. The findings point to left lateral cerebellar
involvement in an action observation network. We discuss possible
mechanisms of cerebellar engagement in visual social perception
revealed by body motion.
Keywords: biological motion, cerebellum, lesions, visual psychophysics
Introduction
The cerebellum has traditionally been viewed as a brain
structure subserving skilled motor behaviors, and cerebellar
damage is commonly associated with difficulties in motor
control and posture balance. Recent work suggests a much
broader functional value of the cerebellum with contributions
to a number of higher cognitive functions ranging from
working memory and visual attention to language functions
and speech comprehension (Ravizza et al. 2006; Hayter et al.
2007; Ackermann et al. 2007; Stoodley and Schmahmann 2009).
However, the findings are controversial (Glickstein 2006;
Haarmeier and Thier 2007). Brain imaging in humans as well
as nonprimate lesion data suggest that the cerebellum might be
involved not only in movement coordination, but also in visual
action observation (Leggio et al. 2000; Gallagher and Frith
2004; Calvo-Merino et al. 2006; Frey and Gerry 2006; Gazzola
and Keysers 2009).
Veridical visual perception of others’ actions is of immense
value for a variety of daily life situations, such as safe car driving
and self-locomotion, as well as for successful social communication (Puce and Perrett 2003; De Gelder 2006; Blake and
Shiffrar 2007). Body movements help to improve our social
interaction by means of nonverbal information about social
properties such as intentions, emotions and dispositions of
others. Visual sensitivity to body motion emerges early in
perceptual development (Fox and McDaniel 1982), and is well
preserved in the elderly (Norman et al. 2004). Moreover,
preference for biological motion is believed to be predisposed
in the brain of vertebrates (Vallortigara et al. 2005). Brain
imaging in humans, single cell recording in the macaque
Ó The Author 2009. Published by Oxford University Press. All rights reserved.
For permissions, please e-mail: [email protected]
monkey, and neuropsychological lesion studies suggest that
body motion processing engages a specialized neural network
that differs from processing of other moving stimuli (Grossman
et al. 2000; Vaina et al. 2001; Grossman and Blake 2002;
Pelphrey et al. 2003; Jellema et al. 2004; Pavlova et al. 2004;
Peelen et al. 2006; Saygin 2007). Proper functioning of this
network depends on intact communication between several
areas throughout the brain. Early periventricular lesions that
impair brain connectivity lead to reduced visual sensitivity and
affect cortical neuromagnetic response to body movements
(Pavlova et al. 2003, 2005, 2007, 2009). Brain imaging reveals
that the posterior temporal cortex, in particular, the superior
temporal sulcus (STS) and parietal regions in the right cerebral
hemisphere are an essential part of the brain network engaged
in visual processing of body motion (Bonda et al. 1996;
Grossman et al. 2000; Beauchamp et al. 2003; Pelphrey et al.
2003, 2005; Zacks et al. 2006).
According to neuroanatomical findings in monkey and
humans, the cerebellum might have contralateral interconnections primarily via the thalamus and also the basis pontis with
multiple cortical areas in both cerebral hemispheres (Middleton
and Strick 1994; Hoschi et al. 2005), including the posterior
areas of the parieto-temporal cortex (Dum and Strick 2003;
Clower et al. 2005) and the STS (Schmahmann and Pandya 1991;
Booth et al. 2007). Multiple loops operate both in feedforward
(cerebral cortex to the cerebellum) and feedback directions
(Middleton and Strick 1994). Whereas the vermis of the
cerebellum (in particular, its lower lobes) represents the
cerebellar limbic system involved in modulation of emotions
and social behavior, more lateral regions are believed to engage
in modulation of higher cognitive functions (Schmahmann et al.
2007). The intracerebellar functional differentiation appears to
emerge already in childhood. Children with right cerebellar
damage exhibit impairments of language processing, whereas
left hemispheric lesions result in visual spatial deficits (Riva and
Giorgi 2000; Scott et al. 2001). Because of contralateral
connections, the left cerebellum may interact with the right
temporal cortex that is heavily involved in visual processing of
body motion (Bonda et al. 1996; Grossman et al. 2000;
Beauchamp et al. 2003; Pelphrey et al. 2003, 2005; Zacks et al.
2006). For this reason, we assume that the left cerebellar
hemisphere might be important for visual processing of human
locomotion.
Although in healthy adults functional magnetic resonance
imaging (fMRI) and positron emission tomography (PET) reveal
cerebellar activation during visual perception of human
walking (Grossman et al. 2000; Vaina et al. 2001; Ptito et al.
2003), there is a lack of consensus as to cerebellar substructures that matter. It is unclear whether, and, if so, how
cerebellar lesions of different topography affect visual processing of human locomotion. Convergent evidence from neuroimaging and lesion studies is of importance for establishing
structure--function relationships. Methodological difficulties,
however, can lead to a failure in attempts to reveal deficits in
visual processing of body motion in patients with heterogeneous lesion topography (Jokisch et al. 2005). Here we address
the issue of whether and, if so, how damage to the cerebellum
affects visual perception of body motion in patients with
medial and lateral left cerebellar lesions selected for similar
lesion extent and topography. Taking advantage of point-light
methodology that isolates information about body motion from
featural cues, and, therefore, minimizes the availability of
structural information, we had patients with cerebellar lesions
and matched healthy controls detect a point-light walking
figure consisting of a number of dots placed on the main joints
of an otherwise invisible human body (Fig. 1A).
Methods
Participants
Eleven patients (aged 26--51 years) with tumors to the left cerebellum
participated in the psychophysical part of the study. One patient had
a lesion of large extent affecting both medial and lateral cerebellum,
and 2 patients declined to properly complete psychophysical testing.
After lesion analysis (see below), 2 groups of patients with similar lesion
topography entered subsequent data processing: 4 patients with left
medial (1 female, 3 male, mean age 41.1 ± 3.5 years), and 4 patients with
left lateral (3 female, 1 male, 37.5 ± 10.8 years) cerebellar tumors
revealed on a structural MRI scan. Medial cerebellar lesions were
located closely to cerebellar midline, whereas lateral cerebellar lesions
were confined to the left lateral cerebellar hemisphere (Fig. 2). No
other signs of brain abnormality were detectable on an MRI scan.
Neither radiological nor neurological signs of increased intracranial
pressure were observed. There were no age differences between the
patient groups (Mann--Whitney test, U = 11, n.s.). Healthy participants
person-to-person matched for age, gender, socioeconomic, and
educational status to each cerebellar patient were recruited from the
local community. None of the controls had a history of neurological or
psychiatric disorders. All participants were right-handed and had
normal or corrected-to-normal vision. They had normal verbal IQ
(Wechsler-Intelligenztest für Erwachsene, a battery based on the
Wechsler Adult Intelligence Scale (WAIS-III) by David Wechsler
adapted to the German population, Von Aster et al. 2006). Tumors
varied in their etiology, including hemangioblastoma, low grade glioma,
medulloblastoma, and glioblastoma, with equal representation of
benign and malign entity in both groups. Psychophysical examination
was conducted before neurosurgery. Patients did not have radio- or
chemotherapy prior to and at time of testing. Neurological and
ophthalmological examination did not reveal any oculomotor deficits.
Patients with left lateral cerebellar lesions were free from fine motor,
posture or balance deficits. One patient with medial cerebellar lesion
exhibited an uncertain gait pattern, another patient had discrete left
hypacusis and fine motor deficits (dysdiadochokinesia) in the left hand.
In one medial cerebellar patient, a dysmetria of the left hand was
observed. No other neurological deficits were found.
Lesion Analysis
Cerebellar lesions were identified by structural whole-brain MRI
recording performed on a 1.5-T scanner (Siemens Medical Solutions,
Erlangen, Germany). MRI scans included T1, T2, FLAIR, and diffusion
weighted sequences. By using MRIcro software (http://www.sph.sc.edu/
comd/rorden/mricro.html), the lesions were manually traced on each
slice of T1-weighted sequences (32 axial slices, TR [repetition time] 500
ms, TE [echo time] 12 ms, 4-mm slice thickness). Image alignment to
stereotaxic space allowed one to compare lesion topography and extent
between the patients, and to relate lesion topography to activation in
functional imaging studies showing cerebellar involvement in visual
processing of body motion (Grèzes et al. 2004, 2007). Before spatial
normalization of the T1 images by Statistical Parametric Mapping 2
(SPM2, Wellcome Institute of Cognitive Neuroscience, London, UK,
http://www.fil.ion.ucl.ac.uk/spm/software/spm2), the lesions were
masked in order to avoid disruption of automated SPM2 normalization
functions and undue distortion of the images (Brett et al. 2001). Prior to
normalization, the source images were manually reoriented so that their
origin and rotation matched those of the SPM2 T1-template. To ensure
that only voxels located within the brain were included in the
normalization process, the SPM2 threshold template brain mask was
used. The images were then automatically aligned to the T1-template by
using linear transformations. Finally, nonlinear cosine transformations
were performed for matching of image details. Lesion volumetry was
conducted by MRIcro on normalized images. For patients with medial
cerebellar lesions, the resulting lesion volume was 16.78 ± 8.43 mL. For
patients with lateral lesions, it was 20.1 ± 11.48 mL. There was no
difference in volumetric lesion extent between the groups (Mann-Whitney test, U = 7.5, n.s.). According to the 3D-MRI atlas of the human
cerebellum in proportional stereotaxic space (Schmahmann et al. 1999),
the lobules I, II, III, IV, and V were affected in patients with medial
lesions. In patients with lateral lesions, lesions were located in the
lobules VIIb, VIIIa, Crus I, and Crus II. For lateral and medial cerebellar
lesions, separate density plots were created by using the MRIcro
intersection method. These plots represent regions of mutual involvement of either lateral or medial cerebellar lesions. Figure 2 shows
the resulting axial, coronal, and sagittal density plots displayed on a T1weighted MRI image in stereotaxic space provided with the MRIcro
package. This T1-weighted image is an average of 27 scans of the same
subject (http://www.bic.mni.mcgill.ca/cgi/icbm_view).
Figure 1. Upright (A) and inverted 180°, mirror-image, (B) point-light walking figures simultaneously camouflaged by a 44-dot moving mask. For illustrative purposes, an outline
of the walking figure is presented. Participants saw only a set of 55 bright dots either in walker-present or in walker-absent (mask only) displays. The motion of each dot of the
mask was identical to the motion of one of the dots defining the point-light figure. The type, size, luminance, and phase relations of the dots also remained unchanged.
Cerebral Cortex February 2010, V 20 N 2 487
masking dots were randomly distributed in space within a region of
about 5° in height by 7° in width. Head movements were restricted by
the head-and-chin rest. The stimulus duration was 1 s, that is, less than
one gait cycle consisting of 2 steps was shown on each trial. The stimuli
were presented either in an upright orientation or inverted 180°
(mirror-image, see Fig. 1B). In 3 separate runs, participants were shown
a set of 96 upright, computer-generated body motion stimuli (32
different displays in each run, in randomized order) with an equal
number of walker-present and walker-absent displays. In 3 other runs,
96 inverted displays were presented. The order of runs was
randomized. Each run was preceded by a 10-s exposure to the
noncamouflaged walking figure presented with respective orientation.
Participants used a confidence rating procedure to verbally judge the
presence of a walker (1, confident in the presence of walker from 100
to 80%; 2, from 80 to 60%; 3, from 60 to 40%; 4, from 40 to 20%; and 5,
from 20 to 0%). To avoid time pressure during performance of the task,
participants were asked to start each trial by pressing a button on
a keyboard. No immediate feedback was given regarding performance.
Results
Figure 2. Regions of mutual lesion involvement for all patients with medial (A) or
lateral (B) cerebellar lesions are represented as density plots at a T1-weighted MRI
template in MNI space: first row—the transversal slices corresponding to the
maximal axial extent of the density plots (z 5 25 for medial lesions, z 5 55 for
lateral lesions); second row—the maximal coronal extent (y 5 55 for medial
lesions, y 5 70 for lateral lesions), third row—the maximal sagittal extent (x 5
10 for medial lesions, x 5 40 for lateral lesions). These areas (marked by cyan or
red) are affected in all patients with tumors either to the left medial or lateral
cerebellum, respectively.
Psychophysical Examination: Visual Body Motion Perception
Task
A point-light walker was comprised of 11 dots placed on the joints
(ankles, shoulder, etc.) of an otherwise invisible human body. It was
seen moving and facing right, in a sagittal view, with no net translation.
A gait cycle was accomplished in 40 frames with frame duration of 36
ms. One type of stimulus represented a point-light walker embedded in
an array of 44 distracters competing with motions of the walker’s dots
(Fig. 1A). Each of 4 sets of distracters consisted of 11 spatially
scrambled dots on the joints of a point-light walker. The motion of each
dot of the set was identical to the motion of one of the dots defining the
canonical point-light figure. The other type of stimulus was a 55-dot
mask: additional 11 dots were added to the walker-absent displays so
that their density matched that of the walker-present displays. The
type, size, luminance, and phase relations of the dots were the same in
walker-present and walker-absent displays. At a viewing distance of 57
cm, the walking figure subtended a visual angle of 4.0° in height and
2.8° in width at the most extended point of a gait cycle. In a display,
488 Cerebellum and Visual Perception of Body Movement
d
Sokolov et al.
For psychophysical data processing, the jackknife procedure
was employed to calculate statistically unbiased parameters of
receiver operating characteristic (ROC) curves from pooled
rating-method data (Dorfman and Berbaum 1986). Data analysis
was performed on the jackknife estimates of the area under the
ROC curve (Az), a standard measure of sensitivity in signal
detection theory (Macmillan and Creelman 2005). ROC analysis
indicates higher susceptibility of the patients’ visual system to
the camouflage of a point-light walker (Fig. 3A). As assessed by
v2 statistic that involved both the sensitivity index and the
slope of the binormal ROC curve (Metz and Kronman 1980),
patients with lateral lesions had significantly lower sensitivity to
body motion than healthy person-to-person matched controls
without signs of cerebellar abnormality on an MRI scan
(v2 = 11.44, P < 0.01). Visual sensitivity in left lateral cerebellar patients was lower than in medial patients (v2 = 6.87,
P < 0.05). Patients with medial cerebellar lesions, however, did
not significantly differ from matched controls (v2 = 1.95, n.s.).
Both control groups exhibited an equally high level of visual
sensitivity (v2 = 1.36, n.s.). No differences were found in the
cognitive decision criteria (ln b) between patients with medial
and lateral cerebellar lesions as well as between the patients
and controls. This indicates that it is a reduction in visual
sensitivity that is responsible for poorer performance of
patients with lateral cerebellar lesions.
As a control condition for visual sensitivity to body motion,
we used upside-down presentation of the same point-light
displays inverted 180° (mirror-image). Although an inverted
display retains the same relational structure and amount of
motion as an upright one, it is shown by earlier work that
inversion severely impedes integration of the moving local dots
into a point-light walking figure (Pavlova and Sokolov 2000;
Tadin et al. 2002; Pavlova, Sokolov et al. 2006). The upsidedown presentation has a number of advantages as a control for
the visual body motion detection task. The most important of
them is that manipulation with display orientation allows one
to keep the same amount of sensory information available. The
only difference between upright and inverted displays is that in
upright displays, the trajectories of moving dots on the main
limbs of the point-light walker correspond to body motion
during human walking under natural conditions, and in
inverted displays these trajectories contradict gravity forces.
The human visual system is extraordinarily sensitive to the
Figure 3. ROC curves for patients with left lateral (red), medial (cyan) cerebellar lesions, and controls for lateral and medial cerebellar patients (orange and blue, respectively)
obtained for upright (A) and for inverted (B) display orientations. The diagonal represents chance level. The Az, a standard measure of sensitivity in signal detection theory,
characterizes visual sensitivity to point-light body motion.
gravity laws (Pavlova and Sokolov 2000; Shipley 2003) and even
newborn chicks appear to have a predisposition for gravity
forces in point-light body motion displays (Vallortigara and
Regolin 2006). As expected, display inversion resulted in an
overall substantial reduction of sensitivity so that it no longer
differed between patients with lateral lesions and matched
controls (v2 = 5.13, n.s.; see Fig. 3B). No difference in sensitivity
to upside-down body motion displays occurred between
medial cerebellar patients and matched controls (v2 = 0.04,
n.s.), as well as between the control groups (v2 = 4.09, n.s.).
These findings indicate that impaired performance of the
patients with lateral cerebellar lesions on the detection task
under upright stimulus presentation was caused by difficulties
in the visual processing of body motion.
Discussion
Most recent neuroanatomical, neuroimaging and neuropsychological lesion studies suggest that the cerebellum is involved
in diverse networks subserving higher cognitive functions.
However, cerebellar substructures underlying these functions
have not yet been identified. The right temporal cerebral
cortex, and, in particular, the STS, is repeatedly reported to
substantially contribute to the visual processing of body motion
(e.g., Grossman et al. 2000; Beauchamp et al. 2003; Pelphrey
et al. 2003, 2005; Zacks et al. 2006). Human magnetoencephalography reveals a specific pattern of oscillatory
response to a point-light walker that rapidly unfolds in time
over the left occipital (100 ms) and bilateral parietal (130 ms)
regions, and finally peaks over the right temporal (170 ms)
cortex (Pavlova et al. 2004, 2006). By contrast, a peak of
activation over the right temporal regions is absent in response
to an inverted point-light walker that turns to become
unrecognizable. We expected that because of contralateral
connections to the cerebellar regions, the right temporal
cortex may interact with the left cerebellum.
The present data point to left lateral cerebellar involvement
into the action observation network. These findings substantially extend brain imaging data in healthy adults revealing
cerebellar activation during visual processing of point-light
body motion (Grossman et al. 2000; Vaina et al. 2001; Ptito
et al. 2003). Previous fMRI and PET data, however, do not
reach consensus as to cerebellar substructures that are
engaged in visual processing of body motion. The main
outcome of the present work indicates that damage to the left
lateral cerebellum causes a pronounced deficit in the visual
sensitivity to human locomotion, whereas medial lesions do
not substantially affect visual perception of human walking.
These data were obtained with rigorous psychophysical
methodology in patients that were selected for similar lesion
extent and (within a group) for similar lesion topography. The
finding dovetails with previous fMRI data inasmuch as the
lateral cerebellum appears to be selectively activated during
visual processing of point-light biological motion (Vaina et al.
2001).
Although the right temporal cortex is reported to be activated more strongly and frequently during visual processing of
body motion (Grossman et al. 2000; Beauchamp et al. 2003;
Pelphrey et al. 2003; Grossman et al. 2004; Pavlova et al. 2004,
2007; Pelphrey et al. 2005; Zacks et al. 2006), brain imaging and
lesion data suggest that the left parieto-temporal cortex might
also be involved (Bonda et al. 1996; Grossman et al. 2000;
Grossman and Blake 2002; Saygin et al. 2004; Saygin 2007).
Therefore, engagement of the right cerebellum in visual processing of human actions and locomotion remains to be
clarified in future research.
Keeping in mind that the cerebellum is heavily involved in
movement production, one can assume that it might also be
interconnected with the mirror neuron system, which has been
considered as a core for understanding the actions and
intentions of others (Iacoboni and Dapretto 2006). This system
is thought to bridge the gap between the physical self and
social perception through motor-simulation mechanisms. The
action representation system contributes to the perception and
understanding of actions and intentions of others; that is when
we observe others, we mentally simulate the actions we see
(Rizzolatti and Fabbri-Destro 2008).
Compromised visual processing of body motion in left lateral
cerebellar patients suggests that this part of the cerebellum
may be of particular importance for social perception through
body motion and understanding of others’ actions. In accord
with this view, recent brain imaging data reveal cerebellar
involvement in visual social cognition through body motion.
PET indicates that the left lateral cerebellum is activated during
Cerebral Cortex February 2010, V 20 N 2 489
recognition of dynamic, but not static, emotional facial
expressions (Kilts et al. 2003). Recent fMRI data show that
left lateral cerebellar activation is observed during perception
of dynamic, as compared to static, emotional expressions of the
whole body (Grèzes et al. 2007). This observation also agrees
with reports that autistic individuals known for their impairments in social cognition have substantial alterations in the
neuroanatomy and connectivity of the cerebellum, such as
reduced white matter volume (McAlonan et al. 2005).
Healthy perceivers are able to reliably infer emotions,
desires, intentions, and dispositions represented only through
body motion dynamics (Heberlein et al. 2004; Chouchourelou
et al. 2006). Furthermore, observers can discriminate between
deceptive and true intentions conveyed by body dynamics, and
true information is precisely detected despite misleading
endeavors (Runeson and Frykholm 1983). When observers
reveal false intentions in others’ actions, elevated fMRI
activation is found among other regions in the right STS and
the left lateral cerebellum (Grèzes et al. 2004). Obviously,
a proper functioning of the brain network involved in social
perception through body motion depends on intact communication between several areas throughout the brain. Future
research will shed light on the role of the cerebellum for social
cognition through body motion.
A further step toward uncovering localization of cerebellar
regions and their connections to other brain structures
engaged in the network underlying visual processing of body
motion would be a combination of psychophysical methods
with an analysis of functional brain activity and diffusion tensor
imaging. Overall, the present findings offer new insights into
the functional role of the cerebellum in normalcy and
pathology beyond the purely motor domain.
Funding
University of Tübingen Medical School (fortüne-Program
Grants 1576-0-0 and 1757-0-0) to M.P.; Else-Kröner-Fresenius
Foundation (Grant P63/2008) to M.P.; and Integrated Graduate
School of the Collaborative Research Center 550 of the German
Research Foundation (DFG) at the University of Tübingen
supported A.A.S.
Notes
We thank the participants for their kind cooperation, Wolfgang Grodd
and Michael Erb for valuable advice on MRI analysis, and Alexander N.
Sokolov for helpful comments on the psychophysical part of the study.
Conflict of Interest : None declared.
Address correspondence to Arseny Sokolov, Department of Neurosurgery, University of Tübingen Medical School, Hoppe-SeylerStrasse 3, D72076 Tübingen, Germany. Email: arseny.sokolov@med.
uni-tuebingen.de.
References
Ackermann H, Mathiak K, Riecker A. 2007. The contribution of the
cerebellum to speech production and speech perception: clinical
and functional imaging data. Cerebellum. 6:202--213.
Beauchamp MS, Lee KE, Haxby JV, Martin A. 2003. fMRI response to
video and point-light displays of moving humans and manipulable
objects. J Cogn Neurosci. 15:991--1001.
Blake R, Shiffrar M. 2007. Perception of human motion. Ann Rev
Psychol. 58:47--73.
Booth JR, Wood L, Lu D, Houk JC, Bitan T. 2007. The role of the basal
ganglia and cerebellum in language processing. Brain Res.
1133:136--144.
490 Cerebellum and Visual Perception of Body Movement
d
Sokolov et al.
Bonda E, Petrides M, Ostry D, Evans A. 1996. Specific involvement of
human parietal systems and the amygdala in the perception of
biological motion. J Neurosci. 16:3737--3744.
Brett M, Leff AP, Rorden C, Ashburner J. 2001. Spatial normalization of
brain images with focal lesions using cost function masking.
Neuroimage. 14:486--500.
Calvo-Merino B, Grèzes J, Glaser DE, Passingham RE, Hoggard P. 2006.
Seeing or doing? Influence of visual and motor familiarity in action
observation. Curr Biol. 16:1905--1910.
Chouchourelou A, Toshihiko M, Harber K, Shiffrar M. 2006. The visual
analysis of emotional actions. Soc Neurosci. 1:63--74.
Clower DM, Dum RP, Strick PL. 2005. Basal ganglia and cerebellar
inputs to ‘AIP’. Cereb Cortex. 15:913--920.
De Gelder B. 2006. Towards the neurobiology of emotional body
language. Nat Rev Neurosci. 7:242--249.
Dorfman DD, Berbaum KS. 1986. RSCORE-J: Pooled rating method data:
a computer program for analyzing pooled ROC curves. Behav Res
Methods Instr Comput. 18:452--462.
Dum RP, Strick LP. 2003. An unfolded map of the cerebellar dentate
nucleus and its projections to the cerebral cortex. J Neurophysiol.
89:634--639.
Fox R, McDaniel C. 1982. The perception of biological motion by
human infants. Science. 218:486--487.
Frey SH, Gerry VE. 2006. Modulation of neural activity during
observational learning of actions and their sequential orders. J
Neurosci. 26:13194--13201.
Gallagher HL, Frith C. 2004. Dissociable neural pathways for the
perception and recognition of expressive and instrumental gestures.
Neuropsychologia. 42:1725--1736.
Gazzola V, Keysers C. 2009. The observation and execution of actions
share motor and somatosensory voxels in all tested subjects: singlesubject analyses of unsmoothed fMRI data. Cereb Cortex.
19:1239--1255.
Glickstein M. 2006. Thinking about the cerebellum. Brain. 129:288--292.
Grèzes J, Frith CD, Passingham RE. 2004. Inferring false beliefs from the
actions of oneself and others: an fMRI study. Neuroimage.
21:744--750.
Grèzes J, Pichon S, de Gelder B. 2007. Perceiving fear in dynamic body
expressions. Neuroimage. 35:959--967.
Grossman E, Blake R. 2002. Brain areas active during visual perception
of biological motion. Neuron. 35:1167--1175.
Grossman E, Donnelly M, Price R, Morgan V, Pickens D, Neighbor G,
Blake R. 2000. Brain areas involved in perception of biological
motion. J Cogn Neurosci. 12:711--720.
Grossman ED, Blake R, Kim C-Y. 2004. Learning to see biological
motion: brain activity parallels behavior. J Cogn Neurosci.
16:1669--1679.
Haarmeier T, Thier P. 2007. The attentive cerebellum—myth or reality?
Cerebellum. 6:177--183.
Heberlein AS, Adolphs R, Tranel D, Damasio H. 2004. Cortical regions
for judgments of emotions and personality from point-light walkers.
J Cogn Neurosci. 16:1143--1158.
Hayter AL, Langdon DW, Ramnani N. 2007. Cerebellar contributions to
working memory. Neuroimage. 36:943--954.
Hoschi E, Tremblay L, Feger J, Carras PL, Strick PL. 2005. The cerebellum
communicates with the basal ganglia. Nat Neurosci. 11:1491--1493.
Iacoboni M, Dapretto M. 2006. The mirror neuron system and the
consequences of its dysfunction. Nat Rev Neurosci. 7:942--951.
Jellema T, Maassen G, Perrett DI. 2004. Single cell integration of
animate form, motion and location in the superior temporal cortex
of the macaque monkey. Cereb Cortex. 14:781--790.
Jokisch D, Troje NF, Koch B, Schwarz M, Daum I. 2005. Differential
involvement of the cerebellum in biological and coherent motion
perception. Eur J Neurosci. 21:3439--3446.
Leggio MG, Molinari M, Neri P, Graziano A, Mandolesi L, Petrosini L.
2000. Representation of actions in rats: the role of cerebellum in
learning spatial performances by observation. Proc Natl Acad Sci
USA. 97:2320--2325.
Kilts CD, Egan G, Gideon DA, Ely TD, Hoffman JM. 2003. Dissociable
neural pathways are involved in the recognition of emotion in static
and dynamic facial expressions. Neuroimage. 18:156--168.
Macmillan NA, Creelman CD. 2005. Detection theory: a user’s guide.
Mahwah (NJ): Lawrence Erlbaum Associates.
McAlonan GM, Cheung V, Cheung C, Suckling J, Lam GY, Tai KS, Yip L,
Murphy DGM, Chua SE. 2005. Mapping the brain in autism. A voxelbased MRI study of volumetric differences and intercorrelations in
autism. Brain. 128:268--276.
Metz CE, Kronman HB. 1980. Statistical significance tests for binormal
ROC curves. J Math Psychol. 22:218--243.
Middleton FA, Strick PL. 1994. Anatomical evidence for cerebellar and
basal ganglia involvement in higher cognitive function. Science.
266:458--461.
Norman JF, Pasyton SM, Long JR, Hawkes LM. 2004. Aging and the
perception of biological motion. Psychol Aging. 19:219--225.
Pavlova M, Bidet-Ildei C, Sokolov AN, Braun C, Krägeloh-Mann I. 2009.
Neuromagnetic response to body motion and brain connectivity. J
Cogn Neurosci. 21:837--846.
Pavlova M, Birbaumer N, Sokolov A. 2006. Attentional modulation of
cortical neuromagnetic gamma response to biological movement.
Cereb Cortex. 16:321--327.
Pavlova M, Lutzenberger W, Sokolov A, Birbaumer N. 2004. Dissociable
cortical processing of recognizable and non-recognizable biological
movement: analyzing gamma MEG activity. Cereb Cortex.
14:181--188.
Pavlova M, Lutzenberger W, Sokolov AN, Birbaumer N, Krägeloh-Mann I.
2007. Oscillatory MEG response to human locomotion is modulated
by periventricular lesions. Neuroimage. 35:1256--1263.
Pavlova M, Sokolov A. 2000. Orientation specificity in biological motion
perception. Percept Psychoph. 62:889--899.
Pavlova M, Sokolov A, Birbaumer N, Krägeloh-Mann I. 2006. Biological
motion processing in adolescents with early periventricular brain
damage. Neuropsychologia. 44:586--593.
Pavlova M, Sokolov A, Staudt M, Marconato F, Birbaumer N, KrägelohMann I. 2005. Recruitment of periventricular parietal regions in
processing cluttered point-light biological motion. Cereb Cortex.
15:594--601.
Pavlova M, Staudt M, Sokolov A, Birbaumer N, Krägeloh-Mann I. 2003.
Perception and production of biological movement in patients with
early periventricular brain lesions. Brain. 126:692--701.
Peelen MV, Wiggett AJ, Dowing PE. 2006. Patterns of fMRI activity
dissociate overlapping functional brain areas that respond to
biological motion. Neuron. 49:815--822.
Pelphrey KA, Mitchell TV, McKeown MJ, Goldstein J, Allison T,
McCarthy G. 2003. Brain activity evoked by the perception of
human walking: controlling for meaningful coherent motion. J
Neurosci. 23:6819--6825.
Pelphrey KA, Morris JP, Michelich CR, Allison T, McCarthy G. 2005.
Functional anatomy of biological motion perception in posterior
temporal cortex: an fMRI study of eye, mouth and hand movement.
Cereb Cortex. 15:1866--1876.
Ptito M, Faubert J, Gjedde A, Kupers R. 2003. Separate neural pathways
for contour and biological-motion cues in motion-defined animal
shapes. Neuroimage. 19:246--252.
Puce A, Perrett D. 2003. Electrophysiology and brain imaging of
biological motion. Phil Trans R Soc Lond B. 358:435--445.
Ravizza SM, McCormick CA, Schlerf JE, Justus T, Ivry RB, Fiez JA. 2006.
Cerebellar damage produces selective deficits in verbal working
memory. Brain. 129:306--320.
Riva D, Giorgi C. 2000. The cerebellum contributes to higher functions
during development. Evidence from a series of children surgically
treated for posterior fossa tumor. Brain. 123:1051--1061.
Rizzolatti G, Fabbri-Destro M. 2008. The mirror system and its role in
social cognition. Curr Opin Neurobiol. 8:179--184.
Runeson S, Frykholm G. 1983. Kinematic specification of dynamics as
information basis for the person-and-action perception: expectation, gender recognition, and deceptive intention. J Exp Psychol
General. 112:585--615.
Saygin AP. 2007. Superior temporal and premotor brain areas necessary
for biological motion perception. Brain. 130:2452--2461.
Saygin AP, Wilson SM, Hagler DJ, Jr, Bates E, Sereno MI. 2004. Point-light
biological motion perception activates human premotor cortex. J
Neurosci. 24:6181--6188.
Schmahmann JD, Doyon J, McDonald D, Holmes C, Lavoie K,
Hurwitz AS, Kabani N, Toga A, Evans A, Petrides M. 1999. Threedimensional MRI atlas of the human cerebellum in proportional
stereotaxic space. Neuroimage. 10:233--260.
Schmahmann JD, Pandya DN. 1991. Projections to the basis pontis fron
the superior temporal sulcus and superior temporal region in the
rhesus monkey. J Comp Neurol. 308:224--248.
Schmahmann JD, Weilburg JB, Sherman JC. 2007. The neuropsychiatry
of the cerebellum—insights from the clinic. Cerebellum. 6:254--267.
Scott RB, Stoodley CJ, Anslow P, Paul C, Stein JF, Sugden EM,
Mitchell CD. 2001. Lateralized cognitive deficits in children
following cerebellar lesions. Dev Med Child Neurol. 43:685--691.
Shipley TF. 2003. The effect of object and event orientation on
perception of biological motion. Psychol Sci. 14:377--380.
Stoodley CJ, Schmahmann JD. 2009. Functional topography in the
human cerebellum: a meta-analysis of neuroimaging studies. Neuroimage. 44:489--501.
Tadin D, Lappin JS, Blake R, Grossman ED. 2002. What constitutes an
efficient reference frame for vision? Nat Neurosci. 5:1010--1015.
Vaina LM, Solomon J, Chowdhury S, Sinha P, Belliveau JW. 2001.
Functional neuroanatomy of biological motion perception in
humans. Proc Natl Acad Sci USA. 98:11656--11661.
Vallortigara G, Regolin L. 2006. Gravity bias in the interpretation of
biological motion by inexperienced chicks. Curr Biol. 16:R279--280.
Vallortigara G, Regolin L, Marconato F. 2005. Visually inexperienced
chicks exhibit spontaneous preference for biological motion
patterns. PLoS Biol. 3:1312--1316.
Von Aster M, Neubauer A, Horn R. 2006. Wechsler-Intelligenztest für
Erwachsene WIE Manual. Übersetzung und Adaptation der WAIS-III
von David Wechsler. USA: The Psychological Corporation.
Zacks JM, Swallow KM, Vettel JM, McAvoy MP. 2006. Visual motion
and the neural correlates of event perception. Brain Res. 1076:
150--162.
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