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Hemodynamic (fNIRS) and EEG (N200) correlates of emotional inter-species interactions modulated by visual and auditory stimulation

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The brain activity, considered in its hemodynamic (optical imaging: functional Near-Infrared Spectroscopy, fNIRS) and electrophysiological components (event-related potentials, ERPs, N200) was monitored when subjects observed (visual stimulation, V) or observed and heard (visual + auditory stimulation, VU) situations which represented inter-species (human-animal) interactions, with an emotional positive (cooperative) or negative (uncooperative) content. In addition, the cortical lateralization effect (more left or right dorsolateral prefrontal cortex, DLPFC) was explored. Both ERP and fNIRS showed significant effects due to emotional interactions which were discussed at light of cross-modal integration effects. The significance of inter-species effect for the emotional behavior was considered. In addition, hemodynamic and EEG consonant results and their value as integrated measures were discussed at light of valence effect.
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Scientific RepoRts | 6:23083 | DOI: 10.1038/srep23083
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Hemodynamic (fNIRS) and EEG
(N200) correlates of emotional
inter-species interactions
modulated by visual and auditory
stimulation
Michela Balconi
1,2
& Maria Elide Vanutelli
1,2
The brain activity, considered in its hemodynamic (optical imaging: functional Near-Infrared
Spectroscopy, fNIRS) and electrophysiological components (event-related potentials, ERPs, N200)
was monitored when subjects observed (visual stimulation, V) or observed and heard (visual + auditory
stimulation, VU) situations which represented inter-species (human-animal) interactions, with
an emotional positive (cooperative) or negative (uncooperative) content. In addition, the cortical
lateralization eect (more left or right dorsolateral prefrontal cortex, DLPFC) was explored. Both ERP
and fNIRS showed signicant eects due to emotional interactions which were discussed at light of
cross-modal integration eects. The signicance of inter-species eect for the emotional behavior
was considered. In addition, hemodynamic and EEG consonant results and their value as integrated
measures were discussed at light of valence eect.
Previous research has revealed that the processing of emotional visual and auditory stimuli leads to increased
activation of various cortical areas, including the amygdala, the prefrontal cortex (PFC), the dorsolateral pre-
frontal cortex (DLPFC) and the specic sensory areas
1–3
. More recent studies have identied the DLPFC as a key
region in the experience and regulation of visual emotional responses
4–8
. Also, auditory emotional stimulation
was examined, showing a similar eect to that found for the visual condition. However, in some studies which
focalized on EEG frequency band analysis or event-related potentials (ERPs), it was found that frontal areas are
responsive to some specic valence
9,10
and, in other cases, mainly to arousal of auditory stimuli more than to their
specic valence
11
.
Limited research explored the eect of combined emotional visual and auditory stimulation. A main caveat
of previous studies was that they were focalized on typical human conditions or situations (stimuli with emo-
tional value, i.e. human faces and voices)
12–15
, and limited research considered the eect of visual and auditory
emotional stimulation in human/non-human social interactions. Some of them focalized on the empathic emo-
tional response by humans to dierent species
16,17
, or on the brain correlates of pain perception in observing
animals
18
.
erefore, actually there is a need to improve our knowledge about the nature and the cortical correlates of
the emotional behavior in response to inter-species emotional condition. In the present study we specically con-
sidered the cortical response to emotional interactions induced by visual and visual-auditory stimulation more
directly related to inter-species relationships, where an emotionally positive or negative human-animal interac-
tions were represented. Indeed the great majority of previous studies focused only on human-human context,
even if we dont exclusively interact with other people: in fact, as part of our everyday life, we share our social con-
texts with also non-human animals. Few previous studies explored emotions in inter-species contexts, examining
the dierences between the emotional response for other humans or animals, but none of them, at our knowledge,
considered the social meaning of intra- and inter-species contexts. More specically, the contribution of specic
1
Research Unit in Aective and Social Neuroscience, Department of Psychology, Catholic University of Milan, Milan,
Italy.
2
Department of Psychology, Catholic University of the Sacred Heart, Milan. Correspondence and requests for
materials should be addressed to M.B. (email: michela.balconi@unicatt.it)
received: 16 December 2015
accepted: 01 March 2016
Published: 15 March 2016
OPEN
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Scientific RepoRts | 6:23083 | DOI: 10.1038/srep23083
brain areas implicated in human/non-human interactions was scarcely considered. e comparison between dif-
ferent species could or could not support the homogeneity of the emotional behavior and of the emotional brain
response to the inter-species interactional context. In addition, the specicity of visual and auditory stimulation
was not explored, since many studies focused on each stimulation condition separately, or took into consideration
only the inter-species condition
19
.
Previous ndings on human-human interactions provided compelling evidence of an early integration of
visual (i.e. face) and auditory (i.e. voice) information while processing emotional features
20–23
. Both behavioral
and electroencephalographic (ERPs) data revealed some, although non-identical, patterns of cross-modal inu-
ences: for example, a modulation of P200 ERP-component suggested the presence of a relatively early integration
process
24
. Also, congruous and incongruous cross-modal stimulation was found to induce specic and distinct
eects
22,23,25
. e largest EEG alpha-power-density was observed for the sound conditions, with intermediate
values for the picture conditions, and the lowest ones for the combined conditions, thus indicating the strong-
est activation (alpha decreasing) in the combined condition within a distributed emotion and arousal network
comprising frontal, temporal, parietal and occipital neural structures
26
. Also, strong similarities in alpha and
beta bands during visual and audiovisual conditions were found, suggesting the intervention of a strong visual
processing component in the perception of audiovisual stimuli
27
.
In addition, recent results mainly focused on visual stimulation indicated a signicant and specic laterali-
zation eect of PFC activation, based on positive (more directly processed by the le hemisphere) and negative
(more directly processed by the right hemisphere) valence of emotions
28,29
. Indeed, the valence model supposes
that cortical dierences between the two hemispheres are attributable to positive vs. negative valence of emo-
tions
29–31
. However, some other perspectives suggested a dichotomy on approach/avoidance motivation to emo-
tions, the rst being more le frontal-related and the second more right frontal-related
32–34
. Indeed, based on the
approach-withdrawal model of emotion regulation, the emotional behavior should be associated with a balanced
activity in the le and right frontal brain areas which can be explained in an asymmetry measurement
35,36
.
However, previous research did not verify simultaneously the specic visual and auditory lateralization eect
based on valence, but more oen only auditory
37
or visual stimuli
4,38
were used.
Among the different modalities available for monitoring brain activity, EEG/ERPs and Near-Infrared
Spectroscopy (NIRS) are non-invasive and particularly well-suited for evaluating the PFC activity. In fact,
although studies have provided functional images of activated brain areas associated with emotional tasks, they
have seldom addressed the temporal course of such activation. Due to its fast temporal evolution and its rep-
resentation and integration among widespread neural networks, emotion representation, together with its neu-
robiological correlates, should preferably be examined by means of imaging and EEG methods that oer good
resolution in both temporal and spatial domains.
To verify these eects, we applied ERPs analysis to investigate the neural correlates in response to emotional
contexts and the relation between these brain-based potentials and the simple (only visual) or cross-modal (visual
and auditory) stimulation. One specic ERP deection was analyzed, that is the N200 eect. is deection was
considered a specic marker of the emotional value, the relevance and the salience of the situation, as well as of
the emotional involvement (arousal) induced by the aective condition. Indeed, the motivational signicance of
emotions aects subjects’ cortical responses also at longer latencies, since it was found that emotionally salient
stimuli generate greater amplitudes of ERP response for N200
39,40
, for the positive deection P300
41,42
, and also
for late positivity (LPP) measures
43–45
.
In some studies that examined contextual emotional impact on behavior, the specic ERP component N200
was found to be directly related to the emotional content of stimuli or situations
13,46–49
. Specically, it was previ-
ously related to the degree of the attentional and emotional relevance of the context
50
, and it was observed to be
related to subjects’ emotional involvement in terms of arousal
4,51
. More specically, N200 was found to be induced
by the emotional cues (such as faces) more than neutral cues for explicit
51
or implicit tasks
52
, and it was inter-
preted as a task-specic emotional index
53,54
, able to highlight the comprehension of the emotional signicance
of the stimulus. Indeed, this ERP component was found to be modulated by the judgment of aective arousal and
valence of emotional stimuli
55–59
.
About the second measure, the temporal resolution of fNIRS is high enough for measuring event-related
hemodynamic responses. In fact, one of the most relevant features of NIRS is its high temporal resolution com-
pared to other imaging techniques
60,61
. is is an important feature for the present study, since the integration
between EEG and hemodynamic measure requires an adequate comparable temporal resolution. Previous studies
have provided functional images of activated areas in the brain which are associated to emotional tasks, but they
have seldom addressed the temporal course of such activation. erefore, to study the integration between elec-
trophysiological and hemodynamic data, these specic measures seem indicated.
Although other neuroimaging techniques (such as fMRI) may offer a complete view of the cortical and
sub-cortical areas implicated in emotional processing, their low temporal resolution prevents a deep exploration
of the dynamic of the emotional experience. erefore, neither the classical neuroimaging nor the electrophysio-
logical measures seem to completely describe in depth the nature of the emotional correlates. For this reason the
integration of the hemodynamic and EEG measures may oer a complete overview of the brain activity modula-
tion with a more adequate spatial and temporal resolution
62–64
.
In addition, some specic areas more directly related to emotional processing, i.e. the PFC, are easily acces-
sible for fNIRS measurements. Interestingly, recent studies using fNIRS investigating the neural correlates of
emotion regulation processes also described an activation of the PFC
65–67
. Recently, fNIRS has been successfully
applied to investigate the emotional modulation of the visual cortex
66,68
, but further investigations on the auditory
domain are pending. It should be noted that some advantages are related to fNIRS studies with auditory stimula-
tions
69
, whereas it can be dicult to explore the eects of emotional sounds in conventional functional Magnetic
Resonance Imaging (fMRI) scanners. As shown by Plichta et al.
69
the auditory cortex activation is modulated by
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emotionally arousing complex auditory stimuli. Consistent with this hypothesis, pleasant as well as unpleasant
sounds led to higher auditory cortex activation, as compared to neutral sounds. is nding is in line with pre-
vious functional imaging studies on visual stimuli, where occipital regions were found to be more activated by
emotionally arousing compared to neutral stimuli
66
.
However, at present no specic fNIRS study analyzed the PFC contribution in auditory emotional process-
ing. In addition, no previous research by ERP and fNIRS considered the eect of auditory and visual condition
together in the case emotional interactive situations where inter-species relationships are represented. us, the
rst goal of this study was to investigate the brain response to interpersonal inter-species contexts with dierent
emotional valence by examining ERPs and fNIRS components elicited in individuals’ responses. Specically, three
dierent emotional situations were included: a rst condition where subjects observed a conictual and emotion-
ally discomfortable situation (negative situations); a second condition where the subject observed a cooperative
and emotionally comfortable situation (positive situations); and a third condition (control condition) where a
more neutral interaction was represented (no positive or negative emotional situation). Moreover, the eect of
simple visual (V) stimulation and combined visual and auditory (VU) stimulation was considered during these
dierently valenced situations.
We hypothesized that N200 and fNIRS-measured oxygenated haemoglobin (O2Hb) changes may be related
to the emotional content of the stimuli when subjects have to observe emotional inter-species interactions.
Specically, based on previous evidence, we supposed an increased le or right PFC activity as a function of
valence. Indeed we expected signicant dierences in response to dierent valenced situations: based on valence
and approach/withdrawal models of emotions, a signicant and consistent higher le prefrontal activation
(increased O2Hb; higher N200) was supposed for positive emotional conditions, whereas a consistent higher
right prefrontal activation was expected in response to negative conditions
28,30
. Moreover, this relationship should
be accompanied by a specic stimulation eect: compared to V, VU could show an increased brain response
for both ERP and fNIRS in concomitance with valence, since the cross-modal perception could increase and
strength the basic eects expected for the simple emotional visual condition. Finally, a signicant correlation was
supposed between ERP and fNIRS components, considered as markers of electrophysiological and hemodynamic
measures, respectively.
Results
e following set of analyses was performed on the data: a rst repeated measures ANOVA was applied to the
ERP peak amplitude (N200); a second analysis was applied to O2Hb d values. Finally correlational analysis was
applied to N200 and d measures.
A preliminary analysis tested the signicant dierences between the baseline (neutral) and emotional con-
dition. For both EEG and NIRS measures the negative and positive conditions revealed signicant dierences
compared (P 0.01) with neutral condition. Due to the systematic eect and the preliminary value of this com-
parison, we did not included the neutral condition in the successive analyses.
EEG. ERPs data were entered into four-ways repeated measure ANOVAs, with factors condition (2,
V-VU) × lateralization (2, left-right) × valence (2, positive-negative) × localization (3, frontal-temporo/
central-parietal) applied to the peak amplitude. Type I errors associated with inhomogeneity of variance were
controlled by decreasing the degrees of freedom using the Greenhouse-Geiser epsilon. Bonferroni correction was
applied to the statistical data for multiple comparisons. Post hoc comparisons were successively applied to the
data (contrast analyses for repeated measure ANOVA).
As shown by ANOVA, the peak amplitude was modulated by localization (F(1,14) = 7.09, P 0.001,
η
2
= 0.34), valence (F(1,14) = 6.56, P 0.001, η
2
= 0.33), and valence × condition × l ateralization (F(1,28) = 9.13,
P 0.001, η
2
= 0.42). No other main or interaction eect was statistically signicant. As observed, peak ampli-
tude was higher for negative than positive stimuli. In addition, post-hoc comparison revealed that the frontal
areas showed higher peak amplitude compared to other cortical sites: respectively compared to temporo-central
(F(1,14) = 8.71, P 0.001, η
2
= 0.39) and to parietal (F(1,14) = 7.56, P 0.001, η
2
= 0.37) sites (Fig.1).
In addition, about the simple eects for the three-way interaction, signicant dierences were observed
between VU (higher peak deection) and V in response to negative stimuli within the right side (F(1,14) = 6.98,
P 0.001, η
2
= 0.35). Secondly, in VU signicant dierences were found between positive and negative stimuli
within the right side (F(1,14) = 8.87, P 0.001, η
2
= 0.41), with increased peak amplitude for negative than pos-
itive stimuli.
fNIRS. e statistical analysis was applied to d dependent measure for O2Hb concentration. Since at the anal-
ysis HHb was not signicant, we report only results for O2Hb-values. D was subjected to three factor (condition,
2 × l ateralization, 2 × valence, 2) repeated measures ANOVA. Data were averaged over le (Ch 1: AF3-F3; Ch2:
AF3-AFF1; Ch3: F5-F3) and right (Ch4: AF4-F4; Ch5: AF4-AFF2; Ch6: F6-F4) channels.
As shown by ANOVA, interaction eect condition × va lence (F(1,14) = 6.92, P 0.001, η
2
= 0.33) was sig-
nicant (Fig.2). No other main or interaction eect was signicant. Indeed, as shown by paired comparisons,
for VU negative stimuli in comparison to positive stimuli revealed increased d values (F(1,14) = 6.79, P 0.001,
η
2
= 0.33). In contrast, for V positive stimuli in comparison with negative stimuli showed increased d values
(F(1,14) = 6.13, P 0.001, η
2
= 0.32).
Correlational analysis between fNIRS and EEG. Pearsons correlation analysis (across-subject corre-
lations) was applied to N200 and d values. Correlational values were calculated distinctly for each condition
(V/VU) emotional valence (positive/negative stimuli) and lateralization (le/right).
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ere was a signicant positive correlation between d values and N200 for negative patterns within the right
site for VU (r = 0.513; P 0.01). at is, in case of increased peak amplitude a concomitant O2Hb increasing was
observed within the right hemisphere in response to negative stimuli. No other correlation was signicant at the
analysis (Fig.3).
Discussion
e present research explored the role of the prefrontal cortex while processing inter-species emotional interac-
tions. Visual and visuo-auditory emotional stimulation was provided in dierent relational contexts (positive,
negative and neutral). DLPFC was mainly implicated in aective response to inter-species emotional relation-
ship. However, signicant dierences were found in inter-species relationships based on stimulation type, with
increased cortical response for cross-modal stimulation than simple visual stimulation. Moreover, stimulus
Figure 1. N200 peak amplitude (mvolt) for le (up) and right (down) side in response to positive and
negative interactions as a function of V and VU.
Figure 2. Cortical maps of O2Hb as a function of VU (up) and V (down) in response to positive (right
heads) and negative (le heads) interactions.
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valence aected both the N200 ERP and the hemodynamic response, with a more relevant impact of the negative
valence. is cortical activity was shown to be lateralized within the right hemisphere in response to negative
situations. Finally, the systematic relationship between hemodynamic and EEG measures was elucidated.
In general, the present results conrmed the crucial role of the PFC in processing emotional interactions also
in case of inter-species condition. Indeed, for the rst time this study demonstrated the contribution of this cor-
tical areas in response to human-non human interactions, considering both O2Hb and N200 eect. e specic
DLPFC contribution in processing emotional interactions was supported by the hemodynamic (increased O2Hb)
and ERP (higher N200 peak amplitude) proles. is result conrmed previous research within the visual domain
in the case of human contexts, which found that the PFC plays a crucial role in the integration of dierent aspects
of emotional regulation by managing the cognitive control over emotional stimuli and behavior
70–74
. erefore
we may suggest that a specic prefrontal cortical area may mediate the emotional processing and behavior of
subjects who are observing inter-subjective interactions, independently from the human specicity of such inter-
action. In fact, whereas in previous research only human conditions (single subjects or interactive situations) were
monitored, in the present study the aspecic human-animal interactions were analyzed. In addition, previous
study which included inter-species condition did not considered visuo-auditory stimulation. erefore, a direct
comparison between these two stimulation types was not considered
19
. Based on our results we may suppose that
the DLPFC is involved in processing situations where emotions are represented independently from the exclusive
presence of human actors
75
.
Specically, about EEG, within this prefrontal network, the N200 amplitude appeared to be signicantly mod-
ulated over the anterior brain sectors and to be valence-related. Indeed, the N200 higher amplitude within the
anterior brain region was directly associated with negatively valenced situations. Based on previous results, and in
accordance with its frontal localization, we may suggest that the N200 is involved in the detection and evaluation
of relevant and threatening patterns
76–78
. is observation is in accordance with other ndings which showed that
the N200 is most pronounced over the frontal cortex for negative related stimuli
58,76
. About the fNIRS, the PFC
contribution in processing emotional interactions was conrmed by the hemodynamic measure. Indeed a similar
prole was observed for O2Hb, with more intense DLPFC responses for negative categories. As shown in previous
research on visual stimulation, negative emotional conditions produced increased cortical response
65,66,79–81
, pro-
cessed as being more salient for the subjective safeguard
82
. ese results appear partially in contrast with a previ-
ous study, which more directly compared intra- and inter-species stimuli
19
. Indeed it was found that intra-species
compared to inter-species conditions elicited higher responses for negative stimuli, whereas the opposite result
was found for positive stimuli (with higher response in the case of inter-species interactions). However, also due
to the specic empathic task, in that case it was supposed that in negative situations human-human interactions
may produce higher controlled cortical activity than human-animal ones, because they could raise more cogni-
tive and mediated processes to represent higher social and culture-based interactions. In addition, in the present
study we did not directly compare intra- and inter-species interactions and, therefore, the direction of potential
dierences between these two specie-specic and specie-aspecic situations cannot be appropriately discussed.
Finally, only visual stimulation was included in this previous study, choice that may prevent to produce a com-
plete comparison between the results.
A second main factor able to aect the prefrontal response was related to stimulation type in integration
with the stimulus valence, that is the presence of a simple visual emotional display or a cross-modal stimula-
tion. Indeed, the integrated visual-auditory condition was able to induce a sort of “reinforce eect” for specic
situations, that is the negative ones. Whereas the negative stimuli generally supported an increased prefrontal
response, in the case of VU subjects showed a higher N200 peak amplitude and an O2Hb increasing during inter-
actions processing compared to simple visual stimulation.
e correlational results reinforced this hypothesis. Indeed we found a higher and coherent response across
EEG and fNIRS in concomitance with the cross-modal stimulation when negative situations were represented. In
contrast positive valence revealed a signicant eect only for the hemodynamic prole, with an O2Hb increasing
for the positive category in the case of simple V. For the rst time, by using two specic cortical measures, which
were able to allow an adequate spatial and temporal resolution, we demonstrated the direct implication of the
DLPFC in response to inter-species interactions when dierent stimulus modalities were considered (V and VU).
Figure 3. Scatterplot of EEG (N200 amplitude) and fNIRS (d values) measures in relationship with
negative interactions for VU within the right side.
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erefore, as shown in previous studies
9
we may suppose the auditory component may induce a higher emo-
tional value in the subjective perception of the interactions, especially when the represented emotional content is
negative and aversive. However for the rst time this eect was shown in the case of cross-modal integration and
not exclusively related to visual or auditory stimulation per se. Specically, we may suppose that the negative and
aggressive valence of the integrated VU conditions made the emotional relevance of those contexts as more sali-
ent. is result is consistent with the position that it may exist an approach motivational tendency toward stimuli
with negative emotional valence
34,83
, and, more generally, an active response may be associated with approach
motivation, in case of more prominent emotional cues, such as negative and unpleasant situations which the
subject is processing.
is may be also due to the specicity of the inter-species context which produces the potential uncontrolled
situation which the subject is faced with: in that case the unpredictable outcomes of the aggressive inter-species
interactions may be evaluated as more dangerous than the positive interactions. In addition, in relation to the
prefrontal localization of the cortical network, the general electrophysiological response and the hemodynamic
increased responsiveness for VU in concomitance with negative patters may suggest the existence of frontally
distributed vigilance mechanism activated during the detection and evaluation of potentially more dangerous
emotional interactions, which is likely to be located at the extended anterior sites. at is, an attentional network
involving the frontal site is argued to maintain a state of alertness when salient and more negative interpersonal
conditions are encountered
84
.
It has to be noted that, compared with some previous research on neuroimaging and NIRS
66,85
, we found
that valence was more relevant to process emotional cue, and it may be in relation to hemispheric lateralization.
Indeed, about the contribution of the two hemispheres, the specic right lateralization found in response to
negative stimuli, as shown by N200 peak distribution, may indicate that a clearer cortical lateralization regards
largely this specic negative valence category. Indeed, this eect was observed not indistinctly, but it was noted
mainly in response to certain emotional categories, such aggressive negative conditions, that is emotions with a
potentially involving arousing power by the subjects
23,50
. To summarize, a general right/negative association was
observed in the subjects and it was mainly supported by EEG modulation. at is, negative, aversive interactions
showed a more consistent lateralized brain activation in comparison with other emotional categories (i.e. positive
emotions).
is fact may be explained taking into account the impact of threatening and negative interactions which
may be more “salient” for the subject’s safeguard, with a more specific contribution of the right DLPFC.
erefore, based on these eects, it should be noted that the valence model with an expected lateralized response
(right-negative; le-positive distinction) is only partially supported by the present results. is “lateralized mech-
anism” may be represented as nalized to alert the emotional behavior in response to highly signicant emotional
situations subjects are faced with. However, due to the partial verication of the underlying valence model of
emotions, future research should better explore the signicance of the positive/negative valence distinction in
concomitance with the approach/avoidance attitude model of emotions, to better clarify the contribution of the
le vs. right hemisphere in response to emotional visual/auditory cues. In addition, the specic role that arousal
may have in aecting the lateralized emotional response should be considered to explain these data more deeply
11
.
A relevant result was also the presence of a general direct link between the dierent levels of analysis (ERP and
fNIRS measures), taking into account that EEG activity was systematically associated with the cortical hemod-
ynamic responsiveness to the emotional situations. Indeed, important eects were derived from to the correla-
tional analyses between hemodynamic and cortical EEG. e joined EEG-NIRS couple revealed signicant linear
associations between the hemodynamic O2Hb values and N200 peak amplitude. e signicant and consistent
positive relation between NIRS and EEG measures mainly in response to negative stimuli may suggest, from one
hand a strength relation between the PFC and emotional stimuli processing, with signicant eect of valence
(more for negative) factor; from the other hand, it may support the consistence of these two brain measures.
More generally, the simultaneous application of EEG and fNIRS was found to be particularly useful for emotional
studies. Specically, the use of fNIRS in a topographic approach for measuring responses to emotions allows to
investigate regional cortical activation changes that are related to emotional manipulations in general, and to
link certain EEG eects to the regional hemodynamic changes
65,66
. e latter strategy enabled us to investigate
whether and how specic emotion-related electrophysiological eects are associated with distinct cortical activa-
tion patterns within the emotion perception network
86
.
However, some limitations of the present research should be underlined. Firstly, the limited number of sub-
jects implicated in the study required further research to generalize the present results. Secondly, a more direct
comparison between dierent types of relationships (i.e. intra-species and inter-species) should be included to
better distinguish the two domains and to extend our results to dierent human-human/human-animal contexts.
Finally, a complete research design, which may add to V and UV condition also a simple U condition, could fur-
nish important elements to discriminate between simple sensory or cross-modal perception.
Method
Subjects. 15 subjects, 8 females and 7 males (M age = 26.33; SD = 2.5; range = 23–33) participated at the
experiment. All subjects were right-handed, with normal or corrected-to-normal visual acuity. Exclusion cri-
teria were neurological or psychiatric pathologies. ey gave informed written consent for participating in the
study, and the research protocol was approved by the Ethical Committee institution where the work was carried
out (Department of Catholic University of Milan, Italy). e experiment was conducted in accordance with the
Declaration of Helsinki and all the procedure were carried out with adequate understanding of the subjects.
Research Consent Form was submitted before participating in this research). No payment was provided for their
performance.
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Stimuli. Subjects were required to view aective pictures depicting human-animal (for animals: cats and dogs)
interactions. 48 colored pictures were selected representing positive (24) and negative (24) interactions. Positive
pictures represented emotionally comfortable interactions between humans and animals; negative pictures rep-
resented emotionally uncomfortable interactions between humans animals. 24 Neutral stimuli (interactions
without a specic emotional signicance) were used as control condition. Other 48 pictures (positive; negative)
associated with sounds which simulated animals’ positive (for cat meow/purr; for dog barks of joy) or negative
(for cat growl; for dog snarl) noise (Fig.4). Neutral condition included both visual and auditory neutral stimuli.
erefore each subject was submitted to visual (72) or visual/auditory (72) condition for a total of 144 stimuli.
All pictures had same size (14 cm in weight × 10 cm in height) and were similar for perceptual features (lumi-
nance; complexity, i.e. number of details in the scene; characters’ gender: half males and half females actors; ani-
mals’ species: half dogs and half cats). Sounds were taken from some internet databases and downloaded as wav
les. ey were reproduced taking into account some acoustic parameters (pitch; intensity; range) to guarantee
similar prole across the noises.
A pre-experimental procedure was adopted to validate the picture/sound dataset. Each stimulus (visual or
auditory) was evaluated by six judges on valence and arousal dimensions, using the Self-Assessment Manikin
Scale with a ve-point Likert Scale
55,87
. Ratings were averaged across all presented pictures/sounds for each
valence.
As shown by statistical analysis (repeated measures ANOVA), both visual and auditory stimuli diered in
term of valence (for all signicant contrast comparisons P = 0.01), it being more positive for positive pictures/
sounds than the other two categories; more negative for negative pictures/sounds than the other two categories;
with intermediate values for neutral pictures/sounds than the other two categories. About arousal, positive and
negative pictures/sounds were more arousing than neutral pictures/sounds. However, negative and positive stim-
uli did not dier in terms of arousal. e cross-modal stimulation was perceived as coherent in term of valence
(negative valenced for negative stimuli combination; positive valence for positive stimuli combination).
Procedure. Subjects were seated in a dimly lit room, facing a computer monitor that was placed 70 cm from
the subject. Stimuli were presented using E-Prime 2.0 soware (Psychology Soware Tools, Inc., Sharpsburg, PA,
USA) running on a personal computer with a 15-inch screen. Participants were required to process each stimulus
during fNIRS/EEG measures recording, and they should attend to the pictures/sounds the entire time of exposi-
tion, focalizing on the emotional conditions which characterize the represented human actors. Subjects were sub-
mitted to V and VU blocks with a random order to avoid condition order eects (randomization of the six blocks
across-subjects). Within each block, pictures or pictures/sound were displayed in a random order across-subject
in the center of a computer monitor for 6 seconds, with an inter-stimulus interval of 8 seconds (Fig.5). Auditory
stimuli were reproduced by the PC loudspeakers at a listening level of approximatively 70dB. V and VU condi-
tions were randomized across-subjects.
120 seconds resting period was registered at the beginning of the experiment before the picture/sounds series.
Aer the experimental phase, subjects were required to rate pictures/sounds on SAM evaluating valence and
arousal on a ve-point Likert scale. As shown by statistical analysis (repeated measures ANOVAs) pictures/
Figure 4. Examples of stimuli (neutral, positive, negative) (photographed by Maria Elide Vanutelli).
Figure 5. Experimental procedure (EEG and fNIRS acquisition) (photographed by Maria Elide Vanutelli).
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Scientific RepoRts | 6:23083 | DOI: 10.1038/srep23083
sounds diered in term of valence (for all paired comparisons P = 0.01; for visual, positive M = 4.22 SD = 0.06;
negative M = 2.08 SD = 0.07; neutral M = 3.17 SD = 0.05, for auditory, positive M = 4.32 SD = 0.04; negative
M = 2.13 SD = 0.05; neutral M = 3.12 SD = 0.08) and arousal (signicant dierences between neutral/positive and
neutral/negative comparisons for both visual and auditory, P = 0.01; for visual, positive M = 4.21 SD = 0.07;
negative M = 4.72 SD = 0.03; neutral M = 3.11 SD = 0.04, for auditory, positive M = 4.02 SD = 0.04; negative
M = 4.80 SD = 0.08; neutral M = 3.44 SD = 0.09). In contrast no dierences were found between positive and
negative stimuli for both visual and auditory condition in term of arousal.
EEG recordings and data reduction. A 32-channel portable EEG-System (V-AMP: Brain Products,
München) was used for data acquisition. A NIRS-EEG compatible ElectroCap with Ag/AgCl electrodes was used
to record EEG from active scalp sites referred to earlobe (10/5 system of electrode placement). EEG activity was
recorded from channels on the following positions: AFF3, AFF4, Fz, AFp1, AFp2, C3, C4, Cz, P3, P4, Pz, T7, T8,
O1, O2 (Fig.6). e cap was xed with a chin strap to prevent shiing during the task. e data were recorded
during the stimulation using sampling rate of 500 Hz, with a frequency band of 0.01–50 Hz and with a notch lter
of 50 Hz. e impedance of recording electrodes was monitored for each subject prior to data collection and it
was always kept below 5 k. Additionally, one EOG electrodes was sited on the outer canthus to detect eye move-
ments. Ocular artefacts (eye movements and blinks) were corrected using an eye-movement correction algorithm
that employs a regression analysis in combination with artifact averaging. Aer performing EOG correction and
visual inspection, only artifact-free trials were considered (rejected epochs, 4%). e signal was visually scored,
and portion of the data that contained artifacts were removed to increase specicity. Artifact-free epochs (850 ms)
were considered. An averaged waveform (o-line) was obtained for each condition (not less than 22 epochs were
averaged). e peak amplitude (higher peak amplitude from the baseline) was quantied relative to the 150 ms
pre-stimulus. e onset was coincident with the appearance of the stimulus on the monitor, taking into account
the most negative peak-value within the temporal window of 150–250 ms post-stimulus, since the morphological
analysis of EEG prole revealed that the peak deection was within this time range. Since the latency measure
was previously tested without showing signicant dierences across condition, we did not include this variable
within the nal analysis. e mean latency of N200 was approximately 210 ms. Successively, localization (three
Figure 6. Locations of measurement channels. fNIRS: Emmiters were placed on positions AF3-AF4 and
F5-F6 (red dots), while detectors were placed on AFF1-AFF2 and F3-F4 (pink dots). e 6 resulting channels
are displayed with yellow dots. EEG: EEG activity was recorded from channels on the following positions: AFF3,
AFF4, Fz, AFp1, AFp2, C3, C4, Cz, P3, P4, Pz, T7, T8, O1, O2 (green dots). fNIRS optodes and EEG channels
were attached to the subject’s head using a NIRS-EEG compatible cup, with respect to the international 10/5
system.
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sites: frontal, AFF3/AFF4 and AFp1/AFp2; temporo-central, C3/C4 and T7/T8 and parietal, P3/P4 and P7/P8)
and lateralization (two sides: le channels and right channels) factors were considered to apply statistical analyses.
fNIRS. fNIRS measurements were conducted with the NIRScout System (NIRx Medical Technologies, LLC.
Los Angeles, California) using a 6-channel array of optodes (4 light sources/emitters and 4 detectors) covering
the prefrontal area. Emmiters were placed on positions AF3-AF4 and F5-F6, while detectors were placed on
AFF1-AFF2 and F3-F4. Emitter-detector distance was 30 mm for contiguous optodes and near-infrared light of
two wavelengths (760 and 850 nm) was used. NIRS optodes were attached to the subjects head using a NIRS-EEG
compatible cup, with respect to the international 10/5 system
88
(Fig.6).
With NIRStar Acquisition Soware, changes in the concentration of oxygenated (O2Hb) and deoxygenated
haemoglobin (HHb) were recorded from a 120 s starting resting phase. Signals obtained from the 6 NIRS chan-
nels were measured with a sampling rate of 6.25 Hz, and analyzed and transformed according to their wavelength
and location, resulting in values for the changes in the concentration of oxygenated and deoxygenated hemo-
globin for each channel. Hemoglobin quantity is scaled in mmol mm, implying that all concentration changes
depend on the path length of the NIR light in the brain.
e raw data of O2Hb, and HHb from individual channels were digitally band-pass ltered at 0.01–0.3 Hz.
en, the mean concentration of each channel within a subject was calculated by averaging data across the trials
from the trial onset for 6 s. Based on the mean concentrations in the time series, we calculated the eect size in
every condition for each channel within a subject. e eect sizes (Cohens d) were calculated as the dierence
of the means of the baseline and trial divided by the standard deviation (Sd) of the baseline: d = (m1 m2)/s.
Accordingly, m1 and m2 are the mean concentration values during the baseline and trial, and s means the
Sd of the baseline. en, the eect sizes obtained from the 6 channels were averaged in order to increase the
signal-to-noise ratio. Although the raw data of NIRS were originally relative values and could not be averaged
directly across subjects or channels, the normalized data such as the eect size could be averaged regardless of the
unit
89–91
. In fact, the eect size is not aected by dierential pathlength factor (DPF)
90
.
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Author Contributions
M.B. supervised the experimental paradigms, M.E.V. executed the experiments. M.B. wrote the main manuscript
text and MEV prepared gures. All authors reviewed the manuscript. e submission has been approved by all
of the authors and by the institution where the work was carried out (catholic University of Milan), and all the
subjects who participated to the experiment gave their informed consent. All the methods were in accordance
with the approved guidelines. e manuscript was not submitted elsewhere for publication.
Additional Information
Competing nancial interests: e authors declare no competing nancial interests.
How to cite this article: Balconi, M. and Vanutelli, M. E. Hemodynamic (fNIRS) and EEG (N200) correlates
of emotional inter-species interactions modulated by visual and auditory stimulation. Sci. Rep. 6, 23083;
doi: 10.1038/srep23083 (2016).
is work is licensed under a Creative Commons Attribution 4.0 International License. e images
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unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license,
users will need to obtain permission from the license holder to reproduce the material. To view a copy of this
license, visit http://creativecommons.org/licenses/by/4.0/
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