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Sex Differences in the Neuromagnetic Cortical Response to Biological Motion

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Body motion is a rich source of information for social interaction, and visual biological motion processing may be considered as a hallmark of social cognition. It is unclear, however, whether the social brain is sex specific. Here we assess sex impact on the magnetoencephalographic (MEG) cortical response to point-light human locomotion. Sex differences in the cortical MEG response to biological motion occur mostly over the right brain hemisphere. At early latencies, females exhibit a greater activation than males over the right parietal, left temporal, and right temporal cortex, a core of the social brain. At later latencies, the boosts of activation are greater in males over the right frontal and occipital cortices. The findings deliver the first evidence for gender-dependent modes in the time course and topography of the neural circuitry underpinning visual processing of biological motion. The outcome represents a framework for studying sex differences in the social brain in psychiatric and neurodevelopmental disorders.
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Sex Differences in the Neuromagnetic Cortical Response to Biological Motion
Marina A. Pavlova1, Alexander N. Sokolov2,3 and Christel Bidet-Ildei4,5
1
Department of Biomedical Magnetic Resonance, Medical School, Eberhard Karls University of Tübingen, Tübingen, Germany,
2
Center for Pediatric Clinical Studies (CPCS), Childrens Hospital, Medical School, Eberhard Karls University of Tübingen,
Tübingen, Germany,
3
Centre for Womens Health, Medical School, Eberhard Karls University of Tübingen, Tübingen, Germany,
4
Center de Recherches sur la Cognition et lApprentissage (CeRCA), CNRS-UMR 7295, University of Poitiers, Poitiers, France and
5
Department of Sport Sciences, University of Poitiers, Poitiers, France
Address correspondence to Prof. Marina Pavlova, Department of Biomedical Magnetic Resonance, Medical School, Eberhard Karls University of
Tübingen, Hoppe-Seyler-Straße 3, 72076 Tübingen, Germany. Email: marina.pavlova@uni-tuebingen.de
Body motion is a rich source of information for social interaction,
and visual biological motion processing may be considered as a hall-
mark of social cognition. It is unclear, however, whether the social
brain is sex specic. Here we assess sex impact on the magnetoen-
cephalographic (MEG) cortical response to point-light human loco-
motion. Sex differences in the cortical MEG response to biological
motion occur mostly over the right brain hemisphere. At early laten-
cies, females exhibit a greater activation than males over the right
parietal, left temporal, and right temporal cortex, a core of the social
brain. At later latencies, the boosts of activation are greater in males
over the right frontal and occipital cortices. The ndings deliver the
rst evidence for gender-dependent modes in the time course and
topography of the neural circuitry underpinning visual processing of
biological motion. The outcome represents a framework for studying
sex differences in the social brain in psychiatric and neurodevelop-
mental disorders.
Keywords: biological motion, dynamic topography, gender, MEG, neural
circuitry, point-light displays, sex differences, social brain, time course
Introduction
Visual sensitivity to human body motion may serve as a hall-
mark of daily-life social cognition, and a basis for nonverbal
communication and social competence (Pavlova 2012). In ex-
perimental research, body motion is often represented by a
point-light technique as a set of dots on the joints of an other-
wise invisible body. This helps to isolate information revealed
by body motion from other cues. Visual sensitivity to point-
light body motion emerges early in life: already 23-day-old
human newborns are tuned to displays depicting point-light
walkers (Bidet-Ildei et al. 2014) and other vertebrates (Simion
et al. 2008). A wealth of brain imaging and neuropsychological
work in typically developing adults and children, lesional pa-
tients, and individuals with neurodevelopmental disorders
suggest that visual processing of point-light biological motion
involves the parieto-temporal junction and fusiform gyrus, por-
tions of the parietal and frontal cortices, primarily in the right
hemisphere, and subcortical structures such as the cerebellum
and amygdala (e.g., Grossman et al. 2000;Vaina et al. 2001;
Pavlova, Marconato, Sokolov, Braun, Birbaumer, Krägeloh-
Mann 2006;Pavlova et al. 2007;Saygin 2007;Sokolov et al.
2010, 2012,2014;Krakowski et al. 2011;Buzzell et al. 2013;
Han et al. 2013;Kröger et al. 2013;White et al. 2014; for
review, see Puce and Perrett 2003;Pavlova 2012). Recent
voxel-based morphometry analysis indicates that gray matter
volumes of the left posterior superior temporal sulcus (pSTS)
and ventral premotor cortex (PMC) may be considered as
predictors of individual differences in detection of camou-
aged point-light biological motion (Gilaie-Dotan et al. 2013).
Transcranial magnetic stimulation over the pSTS and PMC
affects visual sensitivity to biological motion (Grossman et al.
2005;van Kamenade et al. 2012). It appears that processing of
biological motion engages a specialized neural network with a
hub in the right temporal cortex (e.g., Grossman and Blake
2002;Beauchamp et al. 2003;Gobbini et al. 2007;Pavlova
et al. 2004;Kaiser et al. 2010;Herrington et al. 2011), where
this network topographically overlaps and likely communi-
cates with the social brain, namely, with the neural circuits
underlying our ability for perception and understanding of
emotions, intentions, drives, desires, dispositions of others,
and body language reading.
It is unclear, however, whether the social brain is sex-
specic, although growing evidence points to sexual dimorph-
ism of the brain (e.g., Cahill 2006). There is a paucity of
research examining sex differences at a neurobiological level.
Yet behavioral data are also controversial. According to
popular beliefs about female superiority on visual social cogni-
tion tasks there are some indications for gender inuence on
visual biological motion processing in common marmosets
(Callithrix jacchus): females but not males exhibit curiosity
to point-light biological motion (Brown et al. 2010). Newly
hatched female chicks demonstrate a stronger preference for
point-light biological motion of a walking hen (even over a
walking cat) than their male peers (Miura and Matsushima
2012). Yet, alterations in point-light biological motion process-
ing with age appears to be unaffected by observersgender
(Billino et al. 2009). Gender congruency between perceivers
and actors enhances visual priming of camouaged point-light
human locomotion (Bidet-Ildei et al. 2010). Female and male
observers respond differently when judging whether a point-
light walker shown in a frontal view is facing toward
(approaching) or backward (retreating): for females, the facing
bias for male walkers is weaker (Schouten et al. 2010,2013).
Gender of observers affects body language reading in point-
light biological motion movies depicting knocking at a door,
but effects are modulated by emotional content of actions:
males surpass in recognition accuracy of happy actions,
whereas females tend to excel in recognition of angry knock-
ing (Sokolov et al. 2011). A similar pattern of results was found
for subtle emotions expressed by point-light human locomo-
tion: males surpass females in recognition accuracy and readi-
ness to respond to subtle happy walking portrayed by female
actors, whereas females tend to be better in recognition of
angry locomotion expressed by male actors (Krüger et al.
2013). Females are more accurate in recognition of point-light
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Cerebral Cortex
doi:10.1093/cercor/bhu175
Cerebral Cortex Advance Access published August 14, 2014
at University Tuebingen on August 15, 2014http://cercor.oxfordjournals.org/Downloaded from
activities (such as walking, jumping on the spot, kicking a ball,
and drinking from a bottle), and excel in some aspects of body
language reading: they are faster in discrimination of emotion-
al from neutral body motion (Alaerts et al. 2011). Most import-
ant, in agreement with the assumption that biological motion
processing and social cognition are intimately linked (Pavlova
2012), in typically developing adults and individuals with aut-
istic disorders, the ability to reveal emotions from point-light
body motion is related to more basic capability for discrimin-
ation between canonical and scrambled biological motion
(Alaerts et al. 2011;Nackaerts et al. 2012). In healthy adults,
some aspects of social cognition (such as empathy) and per-
formance on Reading the Mind in the Eyes Test are related to
point-light biological motion processing (Miller and Saygin
2013).
In adult females, increased functional magnetic resonance
imaging (fMRI) activation is found during passive viewing of
point-light biological motion displays (waving, pat-a-cake, and
peek-a-boo) compared with scrambled versions over the
regions known to be involved in social cognition, in particular,
the temporal pole, medial temporal gyrus, cerebellum, and
amygdala (Anderson et al. 2013). Yet sex differences in brain
activation are less pronounced in children and adolescents
aged 416 years (Anderson et al. 2013).
The motivation of the present work was to uncover sex-
specic alterations in the time course and dynamic topography
of the entire cortical network underpinning visual processing
of biological motion. To this end, we focused on analyses of
the whole-head magnetoencephalographic (MEG) response to
biological motion during performance of a one-back repetition
task with canonical and spatially scrambled point-light displays
(Fig. 1).
Materials and Methods
Participants
Fourteen paid right-handed young adults (7 females and 7 males) with
normal or corrected-to-normal vision were enrolled in the study. Age
of females was 25 ± 2.75 years (median ± 95% condence interval) and
age of males was 25 ± 2.43 years. No age-related differences were
found between females and males (MannWhitney test; U= 18, n.s.).
None had a history of neurological or psychiatric disorders, head
injuries, or medication at a period of examination. They were naïve as
to the purpose of the study. Informed written consent was obtained in
accordance with the requirements of the local Ethical Committee at the
University of Tübingen Medical School. Analysis of MEG oscillatory re-
sponse to biological motion in these participants was reported earlier
(Pavlova et al. 2004). Here, we examined sex-related differences in cor-
tical activation to biological motion displays by uncovering alterations
in the evoked root mean square (RMS) activity.
Stimuli, Task, and Experimental Design
The point-light stimuli and task are described in detail elsewhere (e.g.,
Pavlova et al. 2004). In brief, participants were presented with 2 types
of displays: a canonical point-light walker consisting of 11 dots on the
head and main joints of an invisible gure and a spatially scrambled
conguration, for which the spatial positions of dots were randomly
rearranged on the screen (Fig. 1) so that the display lacked an implicit
coherent structure. All other display characteristics remained the same.
The walking gure, facing right, was seen moving as if on a treadmill.
A gait cycle was completed in 40 frames with frame duration of 31 ms
that produced a walking speed of 48 cycles per minute. The cong-
urations were generated by Cuttings algorithm (Cutting 1978), and
subtended a visual angle of 9° in height and 6° in width. Participants
were presented with a randomized set of 200 stimuli of both types. The
stimuli appeared for 650 ms on a blank screen with an inter-stimulus
interval that varied randomly between 2.5 and 3.0 s. Participants
xated a gray cross in the middle of the screen that was seen during
the whole run. They performed a one-back repetition task lifting a fore-
nger placed in a nonmagnetic light-beam response box following the
offset of the second of 2 consecutive identical stimuli of each type.
One-back repetition task obligates attention to all types of stimuli and,
therefore, reduces possible attention effects on recorded MEG traces.
MEG Recording and Analysis
For recording cortical activity, the whole-head MEG system (CTF
Systems, Inc.; Vancouver, Canada) was used. This system consisted of
151 hardware rst-order magnetic gradiometers distributed with an
average distance of 3 cm between sensors. A participant was seated in
an electromagnetically shielded chamber (Vakuum-Schmelze, Hanau,
Germany). The signals were sampled at a rate of 312.5 Hz. A baseline
was recorded during 300 ms prestimulus. Participants were instructed to
blink only during inter-trial intervals. Vertical eye movements were mon-
itored by electroencephalography/electrooculography recording from
the left eye (impedance was kept below 5 kΩm). Both at the beginning
and at the end of each recording session, the participantsheadposition
was determined with 3 localization coils xed at the nasion and the peri-
auricular sites. Sessions with head movements exceeding 0.5 cm were
discarded. Each MEG recording session (during presentation of a set of
200 stimuli in a run) lasted 1012 min. All epochs of MEG activity were
rst automatically and then manually inspected for artifacts. Epochs con-
taining blinks or eye movements (greater than ±100 μV) were rejected.
The only trials analyzed were those for which a motor response was not
required. If a participant failed to respond to the second identical stimu-
lus, all trials were discarded beginning from the last correct response.
Per participant, a total of 70 correct artifact-free trials were processed
for each type of stimulus. For each participant, we computed difference
in RMS amplitude in response to the canonical against control scrambled
conguration. RMS analysis was performed in equivalent temporal
windows of 50 ms from 0 to 500 ms separately for all sensors over the
occipital, parietal, temporal, and frontal areas of each brain hemisphere.
The sensors over the different cortical areas were dened in accord with
the standard MEG sensor layout.
Results
Behavioral Data
Participants (both females and males) performed the task with
great accuracy reaching ceiling level of performance (Pavlova
et al. 2004). There were just a few errors. For each participant,
Figure 1. Static sample stimuli. Participants were presented with a randomized set of
either (A) a canonical point-light human gure walking as if on a treadmill, or (B) its
spatially scrambled version. Vectors illustrate motion of each dot. The displays are
shown in reverse contrast: they were seen as a set of bright dots against a dark
background. From Pavlova et al. (2004), copyright © 2004 Oxford University Press.
2Sex Differences in the Neuromagnetic Cortical Response to Biological Motion Pavlova et al.
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the miss rate was calculated as a ratio of the number of failures
to respond to the second identical stimulus of each type to the
total number of the required responses. For analysis of false
alarm rate, the number of false alarms for each type of stimulus
was divided by the total number of trials in which this type of
error might occur. Analysis of gender impact on behavioral re-
sponse indicates that in females the miss rate to the canonical
point-light walker was 0.028 ± 0.041 (mean ± standard devi-
ation) and to the scrambled display it was 0.016 ± 0.022. In
males, the miss rate to the canonical walker was 0.008 ± 0.014,
and to the scrambled walker it was 0.005 ± 0.013. No gender
differences in the miss rate were found either in response to
the canonical or to the scrambled walker (MannWhitney test;
U= 19 and U= 17, n.s., respectively). Whereas in females, the
false alarm rate to the canonical point-light walker was very
low 0.004 ± 0.007, male participants did not make any false
alarms. In response to the scrambled display, false alarm rate in
females was 0.004 ± 0.011, and in males it was 0.009 ± 0.017.
No difference between females and males in false alarm rate in
response either to the canonical or scrambled walker was found
(U=17.5andU= 28, n.s., respectively).
Following each run, participants briey indicated any stimu-
lus interpretations they might have had. All female and male
participants spontaneously reported seeing the canonical
walker, and their impression was vivid resulting in high ratings
of the displays vividness on a 5-point unipolar scale. No
gender differences in the ratings were found (U= 25.5, n.s.;
mean, 4.29 ± 0.49 and 4.29 ± 0.76, for females and males, re-
spectively). For the scrambled walker, the ratings were low in
the absence of any gender differences (U= 26, n.s.; 1.43 ± 0.54
and 1.71 ± 1.11, for females and males, respectively).
Sex Differences in MEG Activity
Individual data were submitted to a 4-way (2 × 10 × 4 × 2)
repeated-measures analysis of variance, ANOVA, with a
between-subject factor Gender of observers (female and male)
and within-subject factors Time window, Cortical region
Figure 2. Sex effects in early MEG response to biological motion. The RMS neuromagnetic response to a point-light canonical walker as compared with a scrambled display over
(A) the right parietal, (B) left temporal, and (C) right temporal cortices. At a latency of 200250 ms from the stimulus onset, the RMS response is signicantly greater in females.
(D) The cortical RMS responses are plotted separately for females and males. R_Parietal, L_Temporal, and R_Temporal stand for the right parietal, left temporal, and right temporal
cortex, respectively. Vertical bars represent ±SEM.
Cerebral Cortex 3
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(occipital, parietal, temporal, and frontal), and Hemisphere
(right and left). The outcome reveals a main effect of Cortical
region (F
3,36
= 3.4, P< 0.029), Cortical region by Time window
interaction (F
27,324
= 1.84, P< 0.008), and Time window by
Gender of observers interaction (F
9,108
= 2.67, P< 0.008). Post
hoc analysis of gender-related simple effects shows that irre-
spective of a cortical region and hemisphere, females exhibit
greater RMS amplitude in the early time window of 200250
ms (P< 0.004), whereas males tend to exhibit a greater re-
sponse at later latencies (P< 0.07). At early latencies (200250
ms, Fig. 2), the RMS response is greater in females as compared
with males over the right parietal cortex (mean ± standard
error, 8.02 ± 8.3 fT [femtotesla] in females and 46.5 ± 13.698
fT in males; t
(12)
= 3.4, P< 0.005), left temporal cortex
(10.87 ± 6.58 fT in females and 23.36 ± 11.04 fT in males,
t
(12)
= 2.66, P< 0.02), and over the right temporal cortex
(13.4 ± 6.23 fT in females and 15.64 ± 12.69 fT in males;
t
(12)
=2.44,P< 0.03). At later latencies (Fig. 3), the RMS response
is greater in males as compared with females over the right
frontal lobe at a latency of 250300 ms (4.89 ± 4.77 fT in males
and 12.6 ± 4.6 fT in females; t
(12)
=2.64, P<0.02), and at a
latency of 350400 ms (10.46 ± 5.56 fT in males and 9.36 ± 6.11
fT in females, t
(12)
=2.4,P< 0.03). Over the right occipital cortex,
males exhibit the greater RMS response at a latency of 400450
ms (39.74 ± 5.13 fT in males and 1.99 ± 10.2 fT in females;
t
(12)
=3.65, P< 0.003). Overall, sex differences occur primarily
over the right brain hemisphere.
Discussion
The present work was aimed at uncovering sex-specic altera-
tions in the time course and dynamic topography of the entire
cortical network underpinning visual processing of biological
motion. For this purpose, we analyzed the whole-head MEG
response to biological motion during performance of a one-
back repetition task with unmasked canonical and spatially
scrambled point-light displays. The outcome indicates that in
the absence of behavioral differences, gender of observers
affects the cortical evoked neuromagnetic RMS activation in re-
sponse to human locomotion: (1) Sex differences in the cortical
MEG response to biological motion occur mostly over the right
brain hemisphere; (2) In females, early cortical response to bio-
logical motion is greater over the right parietal, left temporal
and right temporal cortex; and (3) In males, later cortical re-
sponse is greater over the right frontal and occipital cortices.
In the present study, sex differences in the cortical neuro-
magnetic response to biological motion were found over the
regions that are known to be profoundly engaged in visual pro-
cessing of social signals, in particular, in the right brain hemi-
sphere (e.g., Grossman et al. 2004,2005;Gobbini et al. 2007;
Pavlova et al. 2010;Kaiser et al. 2010;Herrington et al. 2011;
Han et al. 2013). Already in 8-month-old infants, the averaged
negative amplitude of the event-related potentials (ERPs) in
the right hemisphere is greater in response to canonical than
to scrambled point-light biological motion (Hirai and Hiraki
2005). While viewing upright as compared with inverted point-
Figure 3. Sex effects in later MEG response to biological motion. The RMS neuromagnetic response to a point-light canonical walker as compared with a scrambled display. In
males, the RMS response is signicantly greater (A) over the right frontal lobe at latencies of 250300 ms and 350400 ms, and (B) over the right occipital cortex at a latency of
400450 ms from the stimulus onset. (C) The cortical RMS responses are plotted separately for females and males. R_Frontal_1, R_Frontal_2, and R_Occipital stand for the rst
and second time window over the right frontal, and for the right occipital cortex, respectively. Vertical bars represent±SEM.
4Sex Differences in the Neuromagnetic Cortical Response to Biological Motion Pavlova et al.
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light biological motion displays of the whole body, infants of
this age exhibit larger positive ERP amplitude over the right
parietal cortex at a latency of 200300 ms (Reid et al. 2006). In
healthy adults, electroencephalographic ndings on biological
motion processing identify early and late ERP components
with peaks varying in different studies from 120 to 300 ms for
the rst and from 190 to 500 ms for the second component
(Hirai et al. 2003,2005;Hirai and Hiraki 2005;Krakowski
et al. 2011;Jokisch et al. 2005;White et al. 2014). It appears
that, in particular, early stages in visual processing of biologic-
al motion are associated with the right hemisphere (Hirai et al.
2003;Krakowski et al. 2011;Kröger et al. 2013). Some studies
also report a late (beyond 300 ms) medial posterior positivity/
ventral lateral negativity (MPP/VAN) ERP component (Hirai
and Hiraki 2005;Krakowski et al. 2011;White et al. 2014),
which likely reects involvement of higher-order top-down
and task-relevant cognitive processes.
Our MEG ndings show that earlier stages in visual process-
ing of biological motion are associated with greater cortical ac-
tivation in females. Keeping in mind that from the evolutionary
and socio-cultural points of view, female roles are often asso-
ciated with offspring care providing and detecting a potential
danger, it appears that the female brain may be more visually
tuned to human locomotion. In accordance with this, recent
behavioral data suggest that in contrast to men, body motion
stimuli automatically capture womens attention even if these
displays are irrelevant for the task and serve as distractors
(Bidet-Ildei and Bouquet 2014). In males, late boosts of cor-
tical activation over the right frontal and occipital cortices may
point to a stronger higher-order cognitive involvement in bio-
logical motion processing. The greater activation over the right
frontal cortex likely reects engagement of decision processes,
whereas late boosts over the right occipital cortex may be
driven by feedback from the cortical regions involved in
higher-order cognitive processing. However, this assumption
requires further experimental proof.
Most remarkable outcome of this work is that females exhibit
greater activity over the right temporal cortex, a hub of the
social brain, where the network specialized for biological
motion processing topographically overlaps and communicates
with the neural circuitry underpinning visual social cognition
(perception and understanding of social properties of others
such as intentions, emotions, and expectations). Brain activation
during visual processing of point-light biological motion over-
laps topographically, especially, in the right temporal cortex,
with the network engaged in visual perception of agency and
social attribution in Heider-and-Simmel-like movies represent-
ing motion of geometric shapes (e.g., Gobbini et al. 2007;
Pavlova et al. 2010). Yet sex differences are not evident in the
neural circuitry underpinning visual processing of social inter-
action in Heider-and-Simmel-like animations. Instead, sex differ-
ences are observed only in the regions engaged in perceptual
decision making: in males, the MEG oscillatory induced gamma
response boosts later over the left prefrontal cortex (Pavlova
et al. 2010). It appears that females anticipate social interaction
predicting othersactions ahead of their occurrence, whereas
males require accumulation of more sensory evidence for
proper decisions.
More generally, gender-related brain differences do not always
parallelbehavior. Instead,severaltypesofinterrelations between
behavior and brain mechanisms in respect to sex differences
potentially occur: (1) gender-related differences both in overt
behavioral and brain responses to visual social stimuli; (2)
gender-related differences detectable either at the behavioral
level or (3) solely in brain activation; and (4) a lack of gender-
related differences both at the overt behavioral level and brain
activation. The present ndings deliver the rst evidence for
gender-dependent modes in the time course and topography
of the neural circuitry underpinning visual processing of
biological motion. In light of the absence of differences in be-
havioral responses, it is conceivable that gender-related di-
morphism in the cortical response may prevent behavioral
differences if they are maladaptive, and in such a way promote
adaptive behavioral response.
Further investigation of sex differences in visual processing
of biological motion and body language reading would en-
courage clarication of the nature of neurodevelopmental and
psychiatric disorders characterized by impairments in social
cognition. Many of these disorders are gender specic: females
and males are differently affected in terms of clinical picture,
prevalence, and severity. Females are more often affected by
anxiety disorders with a ratio of 2:1 or even 3:1, and gender
differences increase with age (Craske 2003;Beesdo-Baum and
Knappe 2012). Depression is approximately twice as common
in females as in males (Diorio and Jones 2010). By contrast,
males have a higher risk for developing autistic spectrum dis-
orders than females, with a sex ratio of 4:1 (Newschaffer et al.
2007) or even higher, but females are more severily affected.
Neuroanatomy of autism differs between females and males
(Lai et al. 2013). Schizophrenia occurs 1.4 times more frequent-
ly in males than females, and the onset of disease is earlier in
men (Picchioni and Murray 2007). Males are at a 1420%
higher risk for premature birth and of its complications in the
brain development and cognition (Pavlova and Krägeloh-Mann
2013). Males are more often affected by attention decit hyper-
activity disorder, ADHD (Bloom et al. 2012). Some aspects of
biological motion processing are reported to be impaired in
these and other gender-specic diseases: in schizophrenia
(Kim et al. 2005,2011,2013;Hastings et al. 2013;Spencer
et al. 2013), in autism (e.g., Klin et al. 2009;Kröger et al. 2013;
Nackaerts et al. 2012), in obsessive compulsive disorders
(OCD; Kim et al. 2008), in ADHD (Kröger et al. 2014), and in
individuals who were born preterm (e.g., Pavlova, Marconato,
Sokolov, Braun, Birbaumer, Krägeloh-Mann 2006;Pavlova,
Sokolov, Birbaumer, Krägeloh-Mann 2006;Taylor et al. 2009;
see Pavlova 2012). Yet gender impact on impairments in bio-
logical motion processing and body language reading is
poorly understood. Clarication of sex impact on neural cir-
cuits underpinning biological motion processing would
provide novel insights into understanding of gender vulner-
ability to psychiatric and neurodevelopmental decits in social
cognition (Pavlova 2012).
Conclusions
By analysis of cortical neuromagnetic activity, the present
work delivers the rst evidence for gender dependent modes
in time course and topography of the neural circuitry under-
pinning visual processing of biological motion. The ndings
show that in the absence of behavioral differences, gender of
observers affects the cortical evoked RMS response to human
locomotion: (a) sex differences in the cortical MEG response to
biological motion occur mostly over the right brain hemi-
sphere; and (b) females exhibit greater early cortical response
Cerebral Cortex 5
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over the right parietal and bilateral temporal cortex, whereas
males exhibit greater later cortical response to biological
motion over the right frontal and occipital cortex. Gender-
related differences in the time course and topography of cor-
tical neuromagnetic response found in this study may prevent
behavioral differences if they are maladaptive. The outcome re-
presents a framework for studying sex differences in the social
brain in psychiatric and neurodevelopmental disorders.
Funding
This work was supported by the Else Kröner Fresenius Foun-
dation (grant 2013_A127), the Reinhold Beitlich Foundation,
and the Heidehof Foundation (grant 59073.01.1/3.13) to M.A.P.
C.B.-I. was supported by the grant of the National Center for
Scientic Research (CNRS), France.
Notes
We greatly appreciate Krunoslav Stingl and Christoph Braun at the
MEG-Center of the University of Tübingen Medical School for assist-
ance with MEG data analysis, and Jürgen Dax and Gabriele Walker-
Dietrich for technical assistance with MEG recording.
References
Alaerts K, Nackaerts E, Meyns P, Swinnen SP, Wenderoth N. 2011.
Action and emotion recognition from point light displays: an inves-
tigation of gender differences. PLoS ONE. 6:e20989.
Anderson LC, Bolling DZ, Schelinski S, Coffman MC, Pelphrey KA,
Kaiser MD. 2013. Sex differences in the development of brain
mechanisms for processing biological motion. Neuroimage.
83:751760.
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. 15:9911001.
Beesdo-Baum K, Knappe S. 2012. Developmental epidemiology of
anxiety disorders. Child Adolesc Psychiatr Clin N Am. 21:457478.
Bidet-Ildei C, Bouquet C. 2014. Motor knowledge modulates attention-
al processing during action judgment. Athens: ATINERS Confer-
ence Paper Series, no: PSY20140945.
Bidet-Ildei C, Chauvin A, Coello Y. 2010. Observing or producing
a motor action improves later perception of biological motion:
evidence for a gender effect. Acta Psychol (Amst). 134:215224.
Bidet-Ildei C, Kitromilides-Salerio E, Orliaguet J-P, Pavlova MA, Gentaz
E. 2014. Preference for point-light human biological motion in
newborns: contribution of translational displacement. Dev Psychol.
50:113120.
Billino J, Braun DI, Böhm KD, Bremmer F, Gegenfurtner KR. 2009.
Cortical networks for motion processing: effects of focal brain
lesions on perception of different motion types. Neuropsychologia.
47:21332144.
Bloom B, Cohen RA, Freeman G. 2012. Summary health statistics for U.
S. children: National Health Interview Survey, 2011. National
Center for Health Statistics. Vital Health Stat. Series 10(254).
Brown J, Kaplan G, Rogers LJ, Vallortigara G. 2010. Perception of
biological motion in common marmosets (Callithrix jacchus): by
females only. Anim Cogn. 13:555564.
Buzzell G, Chubb L, Safford AS, Thompson JC, McDonald CG. 2013.
Speed of human biological form and motion processing. PLoS
ONE. 8:e69396.
Cahill L. 2006. Why sex matters for neuroscience. Nat Rev Neurosci.
7:477484.
Craske MG. 2003. Origins of phobias and anxiety disorders: why more
women than men? Amsterdam, The Netherlands: Elsevier.
Cutting JE. 1978. A program to generate synthetic walkers as dynamic
point-light displays. Behav Res Meth Instrum. 10:9194.
Diorio A, Jones I. 2010. Is sex important? Gender differences in
bipolar disorder. Int Rev Psych. 22:437452.
Gilaie-Dotan S, Kanai R, Bahrami B, Rees G, Saygin AP. 2013. Neuro-
anatomical correlates of biological motion detection. Neuropsycho-
logia. 51:457463.
Gobbini MI, Koralek AC, Bryan RE, Montgomery KJ, Haxby JV. 2007.
Two takes on the social brain: a comparison of theory of mind
tasks. J Cogn Neurosci. 19:18031814.
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. 12:711720.
Grossman ED, Battelli L, Pascual-Leone A. 2005. Repetitive TMS over
posterior STS disrupts perception of biological motion. Vis Res.
45:28472853.
Grossman ED, Blake R. 2002. Brain areas active during visual percep-
tion of biological motion. Neuron. 35:11671175.
Grossman ED, Blake R, Kim CY. 2004. Learning to see biological
motion: brain activity parallels behavior. J Cogn Neurosci.
16:16691679.
Han Z, Bi Y, Chen J, Chen Q, He Y, Caramazza A. 2013. Distinct
regions of right temporal cortex are associated with biological and
human-agent motion: functional magnetic resonance imaging and
neuropsychological evidence. J Neurosci. 3:1544215453.
Hastings CN, Brittain PJ, Ffytche DH. 2013. An asymmetry of transla-
tional biological motion perception in schizophrenia. Front
Psychol. 4:436.
Herrington JD, Nymberg C, Schultz RT. 2011. Biological motion task
performance predicts superior temporal sulcus activity. Brain
Cogn. 77:372381.
Hirai M, Fukushima H, Hiraki K. 2003. An event-related potentials study
of biological motion perception in humans. Neurosci Lett. 344:4144.
Hirai M, Hiraki K. 2005. An event-related potentials study of biological
motion perception in human infants. Brain Res Cogn Brain Res.
22:301304.
Hirai M, Senju A, Fukushima H, Hiraki K. 2005. Active processing of
biological motion perception: an ERP study. Brain Res Cogn Brain
Res. 23:387396.
Jokisch D, Daum I, Suchan B, Troje NF. 2005. Structural encoding and
recognition of biological motion: evidence from event-related po-
tentials and source analysis. Behav Brain Res. 157:195204.
Kaiser MD, Hudac CM, Shultz S, Lee SM, Cheung C, Berken AM, Deen
B, Pitskel NB, Sugrue DR, Voos AC et al. 2010. Neural signatures of
autism. Proc Natl Acad Sci USA. 107:2122321228.
Kim J, Blake R, Park S, Shin YW, Kang DH, Kwon JS. 2008. Selective
impairment in visual perception of biological motion in obsessive-
compulsive disorder. Depress Anxiety. 25:E15E25.
Kim J, Doop ML, Blake R, Park S. 2005. Impaired visual recognition of
biological motion in schizophrenia. Schizophr Res. 77:299307.
Kim J, Norton D, McBain R, Ongur D, Chen Y. 2013. Decient biologic-
al motion perception in schizophrenia: results from a motion noise
paradigm. Front Psychol. 4:391.
Kim J, Park S, Blake R. 2011. Perception of biological motion in schizo-
phrenia and healthy individuals: a behavioral and FMRI study.
PLoS ONE. 6:e19971.
Klin A, Lin DJ, Gorrindo P, Ramsay G, Jones W. 2009. Two-year-olds
with autism orient to non-social contingencies rather than biologic-
al motion. Nature. 459:257261.
Krakowski AI, Ross LA, Snyder AC, Sehatpour P, Kelly SP, Foxe JJ.
2011. The neurophysiology of human biological motion processing:
a high-density electrical mapping study. Neuroimage. 56:373383.
Kröger A, Bletsch A, Krick C, Siniatchkin M, Jarczok TA, Freitag CM,
Bender S. 2013. Visual event-related potentials to biological motion
stimuli in autism spectrum disorders. Soc Cogn Affect Neurosci. ad-
vanced online access. doi:10.1093/scan7nst103.
Kröger A, Hof K, Krick C, Siniatchkin M, Jarczok T, Freitag CM, Bender
S. 2014. Visual processing of biological motion in children and ado-
lescents with attention-decit/hyperactivity disorder: an event
related potential-study. PLoS ONE. 9:e88585.
Krüger S, Sokolov AN, Enck P, Krägeloh-Mann I, Pavlova MA. 2013.
Emotion through locomotion: gender impact. PLoS ONE. 11:
e81716.
6Sex Differences in the Neuromagnetic Cortical Response to Biological Motion Pavlova et al.
at University Tuebingen on August 15, 2014http://cercor.oxfordjournals.org/Downloaded from
Lai MC, Lombardo MV, Suckling J, Ruigrok AN, Chakrabarti B, Ecker C,
Deoni SC, Craig MC, Murphy DG, Bullmore ETet al. 2013. Biologic-
al sex affects the neurobiology of autism. Brain. 136:27992815.
Miller LE, Saygin AP. 2013. Individual differences in the perception of
biological motion: links to social cognition and motor imagery.
Cognition. 128:140148.
Miura M, Matsushima T. 2012. Preference for biological motion in do-
mestic chicks: sex-dependent effect of early visual experience.
Anim Cogn. 15:871879.
Nackaerts E, Wagemans J, Helsen W, Swinnen SP, Wenderoth N,
Alaerts K. 2012. Recognizing biological motion and emotions from
point-light displays in autism spectrum disorders. PLoS ONE. 7:
e44473.
Newschaffer CJ, Croen LA, Daniels J, Giarelli E, Grether JK, Levy SE,
Mandell DS, Miller LA, Pinto-Martin J, Reaven J et al. 2007. The epi-
demiology of autism spectrum disorders. Ann Rev Publ Health.
28:235258.
Pavlova M, Guerreschi M, Lutzenberger W, Sokolov AN, Krägeloh-
Mann I. 2010. Cortical response to social interaction is affected by
gender. Neuroimage. 50:13271332.
Pavlova M, Lutzenberger W, Sokolov A, Birbaumer N. 2004. Dissoci-
able cortical processing of recognizable and non-recognizable bio-
logical movement: analyzing gamma MEG activity. Cereb Cortex.
14:181188.
Pavlova M, Lutzenberger W, Sokolov AN, Birbaumer N, Krägeloh-
Mann I. 2007. Oscillatory MEG response to human locomotion is
modulated by periventricular lesions. NeuroImage. 35:12561263.
Pavlova M, Marconato F, Sokolov A, Braun C, Birbaumer N, Krägeloh-
Mann I. 2006. Periventricular leukomalacia specically affects
cortical MEG response to biological motion. Ann Neurol. 59:
415419.
Pavlova M, Sokolov A, Birbaumer N, Krägeloh-Mann I. 2006. Biologic-
al motion processing in adolescents with early periventricular brain
damage. Neuropsychologia. 44:586593.
Pavlova MA. 2012. Biological motion processing as a hallmark of social
cognition. Cereb Cortex. 22:981995.
Pavlova MA, Krägeloh-Mann I. 2013. Limitations on the developing
preterm brain: Impact of periventricular white matter lesions on
brain connectivity and cognition. Brain. 136:9981011.
Picchioni MM, Murray RM. 2007. Schizophrenia. BMJ. 335:9195.
Puce A, Perrett D. 2003. Electrophysiology and brain imaging of bio-
logical motion. Philos Trans R Soc Lond B Biol Sci. 358:435445.
Reid VM, Hoehl S, Striano T. 2006. The perception of biological motion
by infants: an event-related potential study. Neurosci Lett.
395:211214.
Saygin AP. 2007. Superior temporal and premotor brain areas neces-
sary for biological motion perception. Brain. 130:24522461.
Schouten B, Davila A, Verfaillie K. 2013. Further explorations of the
facing bias in biological motion perception: perspective cues, ob-
server sex, and response times. PLoS ONE. 8:e56978.
Schouten B, Troje NF, Brooks A, van der Zwan R, Verfaillie K.
2010. The facing bias in biological motion perception: effects of
stimulus gender and observer sex. Atten Percept Psychophys.
72:12561260.
Simion F, Regolin L, Bulf H. 2008. A predisposition for biological
motion in the newborn baby. Proc Natl Acad Sci USA. 105:809813.
Sokolov AA, Erb M, Gharabaghi A, Grodd W, Tatagiba MS, Pavlova MA.
2012. Biological motion processing: the left cerebellum communi-
cates with the right superior temporal sulcus. Neuroimage.
59:28242830.
Sokolov AA, Erb M, Grodd W, Pavlova MA. 2014. Structural loop
between the cerebellum and the superior temporal sulcus: evidence
from diffusion tensor imaging. Cereb Cortex. 24:626632.
Sokolov AA, Gharabaghi A, Tatagiba M, Pavlova M. 2010. Cerebellar
engagement in an action observation network. Cereb Cortex.
20:486491.
Sokolov AA, Krüger S, Enck P, Krägeloh-Mann I, Pavlova MA. 2011.
Gender affects body language reading. Front Psychol. 2:16.
Spencer JM, Sekuler AB, Bennett PJ, Christensen BK. 2013. Contribu-
tion of coherent motion to the perception of biological motion
among persons with schizophrenia. Front Psychol. 4:507.
Taylor NM, Jakobson LS, Maurer D, Lewis TL. 2009. Differential vulner-
ability of global motion, global form, and biological motion pro-
cessing in full-term and preterm children. Neuropsychologia.
47:27662778.
Vaina LM, Solomon J, Chowdhury S, Sinha P, Belliveau JW. 2001. Func-
tional neuroanatomy of biological motion perception in humans.
Proc Natl Acad Sci USA. 98:1165611661.
van Kemenade BM, Muggleton N, Walsh V, Saygin AP. 2012. Effects of
TMS over premotor and superior temporal cortices on biological
motion perception. J Cogn Neurosci. 24:896904.
White NC, Fawcett JM, Newman AJ. 2014. Electrophysiological
markers of biological motion and human form recognition. Neuro-
image. 84:854867.
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at University Tuebingen on August 15, 2014http://cercor.oxfordjournals.org/Downloaded from
... • Hemispheric lateralization for face processing (Bourne, 2005;Proverbio et al., 2006aProverbio et al., , b, 2010aProverbio et al., , b, c, 2011aProverbio et al., , b, c, 2012 • Facial expression decoding (e.g., Orozco & Ehlers, 1988) • Emotional response to negative affective information ( (Pavlova et al., 2014(Pavlova et al., , 2015 • Parental response (Seifritz et al., 2003;Sander et al., 2007) ...
... This piece of evidence fits with the Baron-Cohen model of sexual dimorphism in empathy and facial expression coding ability (Baron-Cohen et al., 2001;Baron-Cohen and Wheelwright, 2004). In the light of this framework, it can be proposed that the higher female ratings of valence and arousal found in the present study might reflect a greater attentional allocation to (or interest for) human faces as sensory signals (Pavlova et al., 2014(Pavlova et al., , 2015. ...
Chapter
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Machine learning (ML) is a subarea of artificial intelligence which uses the induction approach to learn based on previous experiences and make conclusions about new inputs (Mitchell, Machine learning. McGraw Hill, 1997). In the last decades, the use of ML approaches to analyze neuroimaging data has attracted widening attention (Pereira et al., Neuroimage 45(1):S199–S209, 2009; Lemm et al., Neuroimage 56(2):387–399, 2011). Particularly interesting recent applications to affective and social neuroscience include affective state decoding, exploring potential biomarkers of neurological and psychiatric disorders, predicting treatment response, and developing real-time neurofeedback and brain-computer interface protocols. In this chapter, we review the bases of the most common neuroimaging techniques, the basic concepts of ML, and how it can be applied to neuroimaging data. We also describe some recent examples of applications of ML-based analysis of neuroimaging data to social and affective neuroscience issues. Finally, we discuss the main ethical aspects and future perspectives for these emerging approaches.
... • Hemispheric lateralization for face processing (Bourne, 2005;Proverbio et al., 2006aProverbio et al., , b, 2010aProverbio et al., , b, c, 2011aProverbio et al., , b, c, 2012 • Facial expression decoding (e.g., Orozco & Ehlers, 1988) • Emotional response to negative affective information ( (Pavlova et al., 2014(Pavlova et al., , 2015 • Parental response (Seifritz et al., 2003;Sander et al., 2007) ...
... This piece of evidence fits with the Baron-Cohen model of sexual dimorphism in empathy and facial expression coding ability (Baron-Cohen et al., 2001;Baron-Cohen and Wheelwright, 2004). In the light of this framework, it can be proposed that the higher female ratings of valence and arousal found in the present study might reflect a greater attentional allocation to (or interest for) human faces as sensory signals (Pavlova et al., 2014(Pavlova et al., , 2015. ...
Chapter
Full-text available
Several studies have demonstrated sex differences in empathy and social abilities. This chapter reviews studies on sex differences in the brain, with particular reference to how women and men process faces and facial expressions, social interactions, pain of others, infant faces, faces in things ( pareidolia ), living vs. non-living information, purposeful actions, biological motion, erotic vs. emotional information. Sex differences in oxytocin-based attachment response and emotional memory are also discussed. Overall, the female and male brains show some neuro-functional differences in several aspects of social cognition, with particular regard to emotional coding, face processing and response to baby schema that might be interpreted in the light of evolutionary psychobiology.
... • Hemispheric lateralization for face processing (Bourne, 2005;Proverbio et al., 2006aProverbio et al., , b, 2010aProverbio et al., , b, c, 2011aProverbio et al., , b, c, 2012 • Facial expression decoding (e.g., Orozco & Ehlers, 1988) • Emotional response to negative affective information ( (Pavlova et al., 2014(Pavlova et al., , 2015 • Parental response (Seifritz et al., 2003;Sander et al., 2007) ...
... This piece of evidence fits with the Baron-Cohen model of sexual dimorphism in empathy and facial expression coding ability (Baron-Cohen et al., 2001;Baron-Cohen and Wheelwright, 2004). In the light of this framework, it can be proposed that the higher female ratings of valence and arousal found in the present study might reflect a greater attentional allocation to (or interest for) human faces as sensory signals (Pavlova et al., 2014(Pavlova et al., , 2015. ...
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Full-text available
Embodiment has been discussed in the context of social, affective, and cognitive psychology, and also in the investigations of neuroscience in order to understand the relationship between biological mechanisms, body and cognitive, and social and affective processes. New theoretical models have been presented by researchers considering not only the sensory–motor interaction and the environment but also biological mechanisms regulating homeostasis and neural processes (Tsakiris M, Q J Exp Psychol 70(4):597–609, 2017). Historically, the body and the mind were comprehended as separate entities. The body was considered to function as a machine, responsible for providing sensory information to the mind and executing its commands. The mind, however, would process information in an isolated way, similar to a computer (Pecher D, Zwaan RA, Grounding cognition: the role of perception and action in memory, language, and thinking. Cambridge University Press, 2005). This mind and body perspective (Marmeleira J, Duarte Santos G, Percept Motor Skills 126, 2019; Marshall PJ, Child Dev Perspect 10(4):245–250, 2016), for many years, was the basis for studies in social and cognitive areas, in neuroscience, and clinical psychology.
... • Hemispheric lateralization for face processing (Bourne, 2005;Proverbio et al., 2006aProverbio et al., , b, 2010aProverbio et al., , b, c, 2011aProverbio et al., , b, c, 2012 • Facial expression decoding (e.g., Orozco & Ehlers, 1988) • Emotional response to negative affective information ( (Pavlova et al., 2014(Pavlova et al., , 2015 • Parental response (Seifritz et al., 2003;Sander et al., 2007) ...
... This piece of evidence fits with the Baron-Cohen model of sexual dimorphism in empathy and facial expression coding ability (Baron-Cohen et al., 2001;Baron-Cohen and Wheelwright, 2004). In the light of this framework, it can be proposed that the higher female ratings of valence and arousal found in the present study might reflect a greater attentional allocation to (or interest for) human faces as sensory signals (Pavlova et al., 2014(Pavlova et al., , 2015. ...
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Emotions modulate behavioral priorities via central and peripheral nervous systems. Understanding emotions from the perspective of specific neurotransmitter systems is critical, because of the central role of affect in multiple psychopathologies and the role of specific neuroreceptor systems as corresponding drug targets. Here, we provide an integrative overview of molecular imaging studies that have targeted the human emotion circuit at the level of specific neuroreceptors and transmitters. We focus specifically on opioid, dopamine, and serotonin systems, given their key role in modulating motivation and emotions, and discuss how they contribute to both healthy and pathological emotions.Keywords Molecular imaging Human emotions Dopamine systemSerotonin systemOpioid system
... • Hemispheric lateralization for face processing (Bourne, 2005;Proverbio et al., 2006aProverbio et al., , b, 2010aProverbio et al., , b, c, 2011aProverbio et al., , b, c, 2012 • Facial expression decoding (e.g., Orozco & Ehlers, 1988) • Emotional response to negative affective information ( (Pavlova et al., 2014(Pavlova et al., , 2015 • Parental response (Seifritz et al., 2003;Sander et al., 2007) ...
... This piece of evidence fits with the Baron-Cohen model of sexual dimorphism in empathy and facial expression coding ability (Baron-Cohen et al., 2001;Baron-Cohen and Wheelwright, 2004). In the light of this framework, it can be proposed that the higher female ratings of valence and arousal found in the present study might reflect a greater attentional allocation to (or interest for) human faces as sensory signals (Pavlova et al., 2014(Pavlova et al., , 2015. ...
Chapter
Full-text available
Emotions play a very important role in moral judgments. Hume argues that morality is determined by feelings that make us define whether an attitude is virtuous or criminal. This implies that an individual relies on their past experience to make a moral judgment, so that when the mind contemplates what it knows, it may trigger emotions such as disgust, contempt, affection, admiration, anger, shame, and guilt (Hume D. An enquiry concerning the principles of morals, 1777 ed. Sec. VI, Part I, para, 196, 1777). Thus, even so-called “basic” emotions can be considered as moral emotions. As Haidt (The moral emotions. In: Handbook of affective sciences, vol 11, 852–870, Oxford University Press, 2003) points out, all emotional processing that leads to the establishment and maintenance of the integrity of human social structures can be considered as moral emotion. Consequently, the construct of “morality” is often characterized by a summation of both emotion and cognitive elaboration (Haidt J. Psychol Rev, 108(4):814, 2001).
... • Hemispheric lateralization for face processing (Bourne, 2005;Proverbio et al., 2006aProverbio et al., , b, 2010aProverbio et al., , b, c, 2011aProverbio et al., , b, c, 2012 • Facial expression decoding (e.g., Orozco & Ehlers, 1988) • Emotional response to negative affective information ( (Pavlova et al., 2014(Pavlova et al., , 2015 • Parental response (Seifritz et al., 2003;Sander et al., 2007) ...
... This piece of evidence fits with the Baron-Cohen model of sexual dimorphism in empathy and facial expression coding ability (Baron-Cohen et al., 2001;Baron-Cohen and Wheelwright, 2004). In the light of this framework, it can be proposed that the higher female ratings of valence and arousal found in the present study might reflect a greater attentional allocation to (or interest for) human faces as sensory signals (Pavlova et al., 2014(Pavlova et al., , 2015. ...
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Full-text available
Social cognition refers to a wide range of cognitive abilities that allow individuals to understand themselves and others and also communicate in social interaction contexts (Adolphs, Curr Opin Neurobiol 11(2):231–239, 2001). According to Adolphs (Annu Rev Psychol 60(1):693–716, 2009), social cognition deals with psychological processes that allow us to make inferences about what is happening inside other people—their intentions, feelings, and thoughts. Although the term can be defined in many ways, it is clear that it must be safeguarded for the mental operations underlying social interactions. The most investigated cognitive processes of social cognition are emotion recognition and theory of mind (ToM), given that a whole range of socio-affective and interpersonal skills, such as empathy, derive from them (Mitchell RL, Phillips LH, Neuropsychologia, 70:1–10, 2015). Theory of mind is an intuitive ability to attribute thoughts and feelings to other people, and this ability usually matures in children in preschool age (Wellman HM, The child’s theory of mind. Bradford Books/MIT, 1990), whereas emotional recognition refers to an individual’s ability to identify others’ emotions and affective states, usually based on their facial or vocal expressions, it is a critical skill that develops early and supports the development of other social skills (Mitchell RL, Phillips LH, Neuropsychologia, 70:1–10, 2015).
... • Hemispheric lateralization for face processing (Bourne, 2005;Proverbio et al., 2006aProverbio et al., , b, 2010aProverbio et al., , b, c, 2011aProverbio et al., , b, c, 2012 • Facial expression decoding (e.g., Orozco & Ehlers, 1988) • Emotional response to negative affective information ( (Pavlova et al., 2014(Pavlova et al., , 2015 • Parental response (Seifritz et al., 2003;Sander et al., 2007) ...
... This piece of evidence fits with the Baron-Cohen model of sexual dimorphism in empathy and facial expression coding ability (Baron-Cohen et al., 2001;Baron-Cohen and Wheelwright, 2004). In the light of this framework, it can be proposed that the higher female ratings of valence and arousal found in the present study might reflect a greater attentional allocation to (or interest for) human faces as sensory signals (Pavlova et al., 2014(Pavlova et al., , 2015. ...
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Transcranial brain stimulation (TBS) is a term that denotes different noninvasive techniques which aim to modulate brain cortical activity through an external source, usually an electric or magnetic one. Currently, there are several techniques categorized as TBS. However, two are more used for scientific research, the transcranial magnetic stimulation (TMS) and the transcranial direct current stimulation (tDCS), which stimulate brain areas with a high-intensity magnetic field or a weak electric current on the scalp, respectively. They represent an enormous contribution to behavioral, cognitive, and social neuroscience since they reveal how delimited brain cortical areas contribute to some behavior or cognition. They have also been proposed as a feasible tool in the clinical setting since they can modulate abnormal cognition or behavior due to brain activity modulation. This chapter will present the standard methods of transcranial stimulation, their contributions to social and affective neuroscience through a few main topics, and the studies that adopted those techniques, also summing their findings.
... • Hemispheric lateralization for face processing (Bourne, 2005;Proverbio et al., 2006aProverbio et al., , b, 2010aProverbio et al., , b, c, 2011aProverbio et al., , b, c, 2012 • Facial expression decoding (e.g., Orozco & Ehlers, 1988) • Emotional response to negative affective information ( (Pavlova et al., 2014(Pavlova et al., , 2015 • Parental response (Seifritz et al., 2003;Sander et al., 2007) ...
... This piece of evidence fits with the Baron-Cohen model of sexual dimorphism in empathy and facial expression coding ability (Baron-Cohen et al., 2001;Baron-Cohen and Wheelwright, 2004). In the light of this framework, it can be proposed that the higher female ratings of valence and arousal found in the present study might reflect a greater attentional allocation to (or interest for) human faces as sensory signals (Pavlova et al., 2014(Pavlova et al., , 2015. ...
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No matter how hard you try—pinching different parts of your body, slapping your face, or moving restlessly in your seat—you cannot prevent your mind from occasionally escaping from the present experience as you enter into a mental navigation mode. Sometimes spontaneously, others deliberately, your mind may move to a different time—you may see yourself running an experiment inspired by the chapter you just finished reading or you may imagine yourself on a quantum leap into the future as you fantasize about the delivery of your Nobel Prize acceptance speech. Your mind may move to a distinct space, for example, as you replay last weekend’s party or anticipate a most desirable date, and may even venture into the mind of another (e.g., as you embody the mind of the author you are currently reading). Our minds can accomplish all this mental navigation in fractions of a second, allowing us to see ourselves or even impersonate different people across space and time. While teleportation and time travel may never be physically possible, our wandering minds are indeed very accomplished “time machines” (Suddendorf T, Corballis MC, Behav Brain Sci 30(3), 2007).
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Biological motion, the typical movement of vertebrates, is perceptually salient for many animal species. Newly hatched domestic chicks and human newborns show a spontaneous preference for simple biological motion stimuli (point-light displays) at birth prior to any visual learning. Despite evidence of such preference at birth, neural studies performed so far have focused on a specialized neural network involving primarily cortical areas. Here, we presented newly hatched visually naïve domestic chicks to either biological or rigid motion stimuli and measured for the first time their brain activation. Immediate Early Gene (c-Fos) expression revealed selective activation in the preoptic area of the hypothalamus and the nucleus taeniae of the amygdala. These results suggest that subpallial/subcortical regions play a crucial role in biological motion perception at hatching, paving the way for future studies on adult animals, including humans.
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Extensive research has shown that observers are able to efficiently extract summary information from groups of people. However, little is known about the cues that determine whether multiple people are represented as a social group or as independent individuals. Initial research on this topic has primarily focused on the role of static cues. Here, we instead investigate the role of dynamic cues. In two experiments with male and female human participants, we use EEG frequency tagging to investigate the influence of two fundamental Gestalt principles ‐ synchrony and common fate ‐ on the grouping of biological movements. In Experiment 1, we find that brain responses coupled to four point‐light figures walking together are enhanced when they move in sync vs. out of sync, but only when they are presented upright. In contrast, we found no effect of movement direction (i.e., common fate). In Experiment 2, we rule out that synchrony takes precedence over common fate by replicating the null effect of movement direction while keeping synchrony constant. These results suggest that synchrony plays an important role in the processing of biological group movements. In contrast, the role of common fate is less clear and will require further research.
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Several studies have revealed the role of motor experience when humans have to judge human actions. However, the possible influence of motor knowledge on attentional processes has been neglected. This study used a flanker paradigm (Eriksen & Eriksen, 1974) to analyze the attentional responses of male and female participants during the judgment of running movements. Three running actions appeared simultaneously on a computer screen, with the target in the center and the flankers in the periphery. The target and flankers could be compatible or incompatible concerning both the direction of the movement and the sex of the runner. Moreover, flankers were presented upright or upside-down. The results indicate that the distracting effect of the flankers was different for male and female participants. Whereas directionincompatible flankers systematically disturbed the female participants’ performance, regardless of the sex and the orientation of the flanker, male participants were only distracted when the flankers were upright males. This finding offers new directions to explain sex differences in the judgment of human action.
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Chapter
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