You are on page 1of 14

TecnoLógicas Artículo de Investigación/Research Article

ISSN-p 0123-7799
ISSN-e 2256-5337
Vol. 20, No. 40, pp. 83-96
Sep-dic de 2017

Detecting atypical functioning of


emotional processing in Colombian
ex-combatants

Detección de procesamiento atípico de


emociones en excombatientes colombianos

Mónica V. Rodríguez-Calvache1, Andrés Quintero-Zea2,


Sandra P. Trujillo-Orrego3, Natalia Trujillo-Orrego4 y
José D. López-Hincapié5

Recibido: 12 de junio de 2017


Aceptado: 23 de agosto de 2017

Cómo citar / How to cite

M.V. Rodríguez-Calvache, A. Quintero-Zea, S.P. Trujillo-Orrego, N.


Trujillo-Orrego, y J.D. López-Hincapié, Detecting Atypical functioning
of Emotional processing in Colombian Ex-combatants. TecnoLógicas,
vol. 20, no. 40, pp. 83-96, 2017.

1
Electronic engineer, SISTEMIC, Engineering Faculty, University of
Antioquia (UDEA), Medellín-Colombia, viviana.rodriguez@udea.edu.co
2
Electronic engineer, SISTEMIC, Engineering Faculty, University of
Antioquia (UDEA), Medellín-Colombia, andres.quintero@udea.edu.co
© Copyright 2015 por 3
autores y Tecno Lógicas
Psychologist, Department of Psychology, Universidad de Granada, Granada-
Este trabajo está licenciado bajo una España, sandra.trujillo@udea.edu.co
Licencia Internacional Creative 4
PhD. in Neuroscience, Psychologist, Mental Health Group, School of Public
Commons Atribución (CC BY) Health, University of Antioquia (UDEA), Medellín-Colombia,
natalia.trujillo@udea.edu.co
5
PhD. in Engineering ,Electronic engineer, SISTEMIC, Engineering Faculty, ,
University of Antioquia (UDEA), Medellín-Colombia, josedavid@udea.edu.co
Detecting Atypical functioning of Emotional processing in Colombian Ex-combatants

Abstract
The reincorporation process of Colombian ex-combatants is hindered by their chronic
exposure to violence, which affects their Emotional Processing (EP). Characterizing their
EP will contribute to their reinsertion. The objective of this work is to define an EEG-based
brain connectivity approach to identify differences in EP between Colombian ex-combatants
and individuals who were not directly exposed to the armed conflict. The proposed approach
involves defining the Regions of Interest (ROI) and selecting one of five commonly used
brain connectivity metrics: Correlation, Cross-Correlation, Coherence, Imaginary part of
Coherency, and Phase-Lag Index. Significant differences were found in the positive valence
stimuli in the Beta frequency band. These results support the previously reported trend in
the literature regarding the difficulties ex-combatants have to process emotional
information with positive valence.

Keywords
Brain Connectivity, Colombian Ex-combatants, EEG, Emotional Processing, ROI
selection.

Resumen
El proceso de reincorporación social de los excombatientes colombianos, se dificulta
debido a que la exposición crónica a la violencia afecta su procesamiento emocional (PE).
Este proceso de reincorporación se puede facilitar mediante la caracterización de su PE. El
objetivo de este artículo es definir una metodología de conectividad con EEG que permita
identificar diferencias entre el EP de excombatientes y personas no directamente expuestas
al conflicto armado. La metodología propuesta consiste en definir las Regiones de Interés
(ROI) y seleccionar una de cinco métricas de conectividad funcional cerebral comúnmente
utilizadas: correlación, correlación cruzada, coherencia, parte imaginaria de la coherencia y
el índice de desfase. Se encontraron diferencias significativas en los estímulos con valencia
positiva en la banda de frecuencias Beta. Estos resultados apoyan la tendencia previamente
reportada en la literatura hacia las dificultades de los excombatientes para procesar
información emocional con valencia positiva.

Palabras clave
Conectividad cerebral, excombatientes colombianos, EEG, procesamiento emocional,
selección de las ROI.

[84] TecnoLógicas, ISSN-p 0123-7799 / ISSN-e 2256-5337, Vol. 20, No. 40, sep-dic de 2017, pp. 83-96
Detecting atypical functioning of emotional processing in colombian excombatants

1. INTRODUCTION tioning of similar mechanisms is hypothe-


sized. In [2], the authors proposed psycho-
Reincorporation is a process whereby logical tests to evaluate how Colombian ex-
Colombian ex-combatants adapt to society combatants are processing emotional in-
after being part of an illegal armed group. formation. They found a slight tendency of
This process is affected by their chronic ex-combatants to poorly recognize positive
exposure to violence, which is evidenced in emotional valence (specifically, recognizing
changes in the expression of personality happy faces), but it did not reach statistical
traits, social and cognitive behavior [1]. In significance compared to the control group.
the cognitive domain, some ex-combatants Another way to study EP consists in
describe functional illiteracy or exhibit evaluating the Event Related Potentials
deficits in the executive function [2]. To- (ERP) modulation [3, 6, 7]. In [6], the au-
gether, these findings suggest that the thors found associations between the ex-
exposition to combat experiences increases combatants’ ERPs responses to emotional
the expression of atypical socio-cognitive images from the International Affective
processes, especially in Emotional Pro- Picture System (IAPS) system and their
cessing (EP). EP is a neurocognitive mech- empathy levels. In a previous work [7], it
anism in charge of the perception, recogni- was found that when using ERP modula-
tion, evaluation and generation of a re- tions and the analysis of aggressive re-
sponse to stimuli and relevant emotional sponses and social interactions, both
information in the environment. It is cru- groups (ex-combatant and civilian) could
cial for human adaptation and survival [3]. be automatically separated by applying
This process begins by identifying changes supervised machine learning techniques.
in internal and external circumstances However, we only used psychological tests
with different valences that act as trigger- and ERPs modulations in response to visu-
ing situations in emotional recognition [4]. al stimuli [3]. Based on these approaches,
This process activates multiple sources of it is not possible to recognize how different
cortical and subcortical brain structures functional areas contribute to the expres-
during the observation of a stimuli and sion of failures in emotional processing of
facilitates a rapid response appropriate to ex-combatants.
the social context [4]. Brain connectivity analysis has been
The assessment of their cognitive and proposed as a useful methodology to evalu-
behavioral EP profile is crucial to charac- ate interconnected activation during EP [8,
terize ex-combatants after chronic exposi- 9]. This technique focuses on how the brain
tion to war. Moreover, the characterization processes the information to establish the
of EP will contribute to design cognitive pattern of activation required to generate a
training aimed to help ex-combatants in cognitive process [10]. Connectivity can be
their reintegration process [1]. With this described at several levels: anatomical or
purpose, in this work we propose the use of structural, functional, and effective [11].
brain connectivity analysis to detect atypi- Functional connectivity is modified by life
cal functioning in the EP of Colombian ex- experiences [11] and has been employed to
combatants. evaluate the EP of clinical populations
Studies in veterans have shown that with psychiatric disorders [12]. Thus, func-
experiences of combat and trauma during tional connectivity analysis can be useful
deployment were strongly associated with for the evaluation of the EP of subjects
aggressive and violent behaviors. Veterans without clinical conditions but with special
mainly manifest differences in emotional characteristics, such as exposure to armed
information processing [5]. Regarding Co- conflict [11].
lombian ex-combatants, an atypical func-

TecnoLógicas, ISSN-p 0123-7799 / ISSN-e 2256-5337, Vol. 20, No. 40, sep-dic de 2017, pp. 83-96 [85]
Detecting atypical functioning of emotional processing in colombian excombatants

Functional connectivity is defined as chronized with EEG recordings. In general,


the temporal dependency of neural activa- these stimuli can generate emotional acti-
tion patterns of brain areas. It does not vation in a similar way to real conditions
include directionality information. It relies [16]. Using this dataset, we generated
on statistical measures such as correlation, connectivity maps based on the metrics
covariance, spectral coherence or phase previously mentioned to compare their
locking. Commonly, the computation of performance in group analysis. Finally, by
functional connectivity requires high tem- using statistical tests we identified signifi-
poral resolution and, for this specific popu- cant differences between the emotional
lation, it should be portable; therefore, processing of ex-combatants and civilians.
electroencephalography (EEG) is a viable
recording option [11].
The interpretation of the connectivity 2. METHODOLOGY
analysis performed on scalp-level EEG
data is difficult and error-prone, because 2.1 Experiment set-up
any neurophysiological interpretation of
EEG data is hindered by the volume con- 2.1.1 Participants
duction problem [13]. Volume conduction
can lead to uncertainties for many but not Fifty participants took part in the ex-
all connectivity analysis. Uncertainties periment: 30 Colombian ex-combatants
exist because the connectivity could come (Two female) recruited from the govern-
from electrodes measuring activity from a ment's ARN (Reincorporation and Normal-
single brain source, and not from true in- ization Agency, former ACR) program and
teractions between electrodes [13]. 20 civilian people with no combat back-
There are several metrics to estimate ground (paired by gender, age and educa-
functional connectivity, each of them af- tional level). All the participants read and
fected to different degrees by this phenom- signed an informed consent form before the
enon. In this work, we propose to select one beginning of the study. The study's proce-
of five functional connectivity metrics: dures and informed consent were approved
Correlation, Cross-Correlation, Coherence, by the Bioethical Committee of the Faculty
Imaginary part of Coherency and the of Medicine of University of Antioquia in
Phase-Lag Index [14]. To achieve this, we Medellín, Colombia. None of the partici-
provide an explanation of how these con- pants manifested to have psychiatric, neu-
nectivity metrics work, including their rological or drug abuse disorders. Their
quantitative definition. demographic information is provided in
To assess the EP in ex-combatants, Table 1 (M= Mean, SD= Standard Devia-
thirty Colombian ex-combatants and 20 tion). A Wilcoxon signed-rank test was
Colombian individuals participated in the performed to ensure consistency in age,
study. They performed an emotional gender and educational level differences
recognition computerized task that used across groups; the p-values are reported in
visual stimuli from the IAPS [15], syn- the last column of Table 1.
Table 1. Descriptive statistics of demographic variables. Source: Authors.
Ex-combatants n=30 Civilians n=20 p-values
Gender (Female: Male) 2:28 2:18 0.678
Age (years) M=37.5 M=36.17 0.589
SD=8.22 SD=9.17

Educational level (years) M=10.33 M=11.05 0.373


SD=3.10 SD=2.14

[86] TecnoLógicas, ISSN-p 0123-7799 / ISSN-e 2256-5337, Vol. 20, No. 40, sep-dic de 2017, pp. 83-96
Detecting atypical functioning of emotional processing in colombian excombatants

2.1.2 Emotional processing - experimental Fig. 1 shows the task pipeline; it con-
task sists of four steps per trial. At first, a fixa-
tion cross is presented for 1000 ms to pro-
Participants performed an emotional mote attentional focus on the center. Sec-
categorization task based on the Interna- ond, there is an inter-stimulus interval
tional Affective Picture System (IAPS) [15] ranging from 700 to 1000 ms. This step
validated for Colombian population [17]. avoids habituation and the prediction of
This system consists of a set of visual the next stimulus. Third, the stimulus is
stimuli with a wide range of semantic cat- presented: IAPS images with different
egories (positive, negative and neutral); valence (positive, negative or neutral). This
positive and negative images contain high step lasts 500 ms. Finally, a response time
emotional intensity. These visual stimuli of maximum 10 s was set.
generate emotional activation in a similar
way to real conditions: induction of mental 2.1.3 Data acquisition
representations, psycho-physiological
changes, and facial action [16]. The task EEG recordings were acquired with a
was designed in E-prime Software [18]. 64-electrode NeuroScan EEG SynAmps2
The participants were asked to categorize amplifier [19] at a sample rate of 1000 Hz.
the stimulus displayed on a computer The electrodes were placed in accordance
screen according to their valence, respond- with the international 10-20 system. The
ing whether the stimuli were positive, impedances were maintained below 10 kΩ
neutral or negative as quickly as possible. to obtain a good conductivity between the
In total, 60 images were selected from the scalp and the electrodes. Scan 4.5 software
IAPS, in accordance according with their was used for data recording [19]. The par-
Colombian validation [17]. The task was ticipants were seated in a comfortable
divided into four blocks. Each block con- chair in front of a computer monitor, at a
sisted of 60 trials with images (20 posi- distance of 60 cm, inside a Faraday cage
tives, 20 neutrals and 20 negatives). Each with the lights off for guaranteeing isolat-
stimulus was presented randomly present- ed electric conditions. The participants
ed per block, in total 240 stimuli were pre- were asked to try not to blink, move, or
sented. The IAPS images were controlled speak while performing the task.
in terms of brightness, color and intensity.
They were presented in a 17-inch screen,
60 cm away from the participant.

Fig. 1. Stimulus design. The trial starts with a fixation cross, followed by a random Inter-Stimulus Interval (ISI) between
700 and 1000 ms. The target stimulus is presented for 500 ms. The participants must respond within 10 s. Source: Authors.

TecnoLógicas, ISSN-p 0123-7799 / ISSN-e 2256-5337, Vol. 20, No. 40, sep-dic de 2017, pp. 83-96 [87]
Detecting atypical functioning of emotional processing in colombian excombatants

2.1.4 Signals preprocessing are connected during an experimental


task. Functional connectivity is assessed
EEG recordings were preprocessed in by metrics that establish the existence of
EEGLab toolbox for MATLAB [20]. The any type of covariance between two neuro-
first step in the preprocessing was to physiological signals without providing any
down-sample the signal from 1000 Hz to causal information. Below, five metrics
500 Hz. They were re-referenced using divided into three different categories are
Mastoids as a common reference for all described (see Fig. 2).
channels. Then, a band-pass IIR digital As shown in Fig. 2, not all functional
filter was applied from 0.1 to 60 Hz to re- connectivity metrics are represented in the
duce environmental artifacts (power line frequency domain. Then, before computing
noise) in the EEG data and to extract spe- the non-frequency-based ones, it was nec-
cific frequency bands associated with hu- essary to extract specific frequency bands
man cognition. associated with human cognition. Five
To distinguish between artifacts and band-pass IIR digital filters (with orders
neural components of EEG signals, an varying from 9 to 12, depending on the
automatic method described in [21] was band) were applied to the previously pre-
employed. The automatic method is based processed EEG signals to divide them into
on Independent Component Analysis (ICA) different frequency bands of interest: Delta
and Support Vector Machine (SVM). This (0.10 Hz-3.99 Hz), Theta (4.00 Hz-7.99Hz),
method has the ability to isolate artifact Alpha (8.00 Hz-13.99 Hz), Beta (14.00 Hz-
components such as eye blinking, eye 29.99 Hz) and Gamma (30.00 Hz-59.9 Hz).
movements (EOG), muscular contractions The Pearson’s Correlation Coefficient
(EMG) or cardiac signals (ECG) with high (COR) and the Cross-Correlation Function
accuracy [21]. (XCOR) are time-domain-based. The COR
After identifying the artifacts’ inde- is defined as the covariance of two signals
pendent components, they were removed scaled by the variance of each one of them
and the original configuration (64-channel and it estimates the linear correlation
EEG) of the signals was reconstructed. between them [22]. If (𝑡) ∈ ℝ𝑇 and 𝑦(𝑡) ∈
Then, the recordings were segmented from ℝ𝑇 are EEG signals at two different elec-
200 ms before the stimulus to 800 ms after trodes, and 𝑇 is the number of time sam-
it. For each trial, the stimulus was tagged ples per epoch ( 𝑡 = 1,2, … , 𝑇) the COR 𝑅𝑥𝑦 is
as negative, neutral or positive for the defined as:
emotional processing task. Baseline correc- 𝑻
∑𝒕=𝟏(𝑥(𝑡) − 𝑥̅ )(𝑦(𝑡) − 𝑦̅)
tion was performed by subtracting the 𝑅𝑥𝑦 = (1)
mean of the signal during the time window 𝑻 𝑻
√∑𝒕=𝟏(𝑥(𝑡) − 𝑥̅ )2 ∑𝒕=𝟏(𝑦(𝑡) − 𝑦̅)2
from -200 to 0 ms before the stimulus.
Then, each trial was inspected for leftover
Where 𝑥̅ and 𝑦̅ are the sample mean of
noise in the signals to make sure only
𝑥(𝑡) and 𝑦(𝑡) respectively. The result of
clean segments underwent further analy-
computing 𝑅𝑥𝑦 is a scalar value at a given
sis. Finally, four electrodes (HEO, VEO,
time window. The range of COR is 0 ≤
CB1 and CB2) were excluded as they do
𝑅𝑥𝑦 ≤ 1. When 𝑅𝑥𝑦 = 0, signals 𝑥(𝑡)
not record neural activity.
and 𝑦(𝑡) have no linear interdependence,
2.2 Selection of the functional connectivity while 𝑅𝑥𝑦 = 1 means complete linear direct
metric correlation between the two signals. There-
fore, higher correlations indicate stronger
There are several connectivity metrics functional connection between the related
used to estimate how different brain areas signals.

[88] TecnoLógicas, ISSN-p 0123-7799 / ISSN-e 2256-5337, Vol. 20, No. 40, sep-dic de 2017, pp. 83-96
Detecting atypical functioning of emotional processing in colombian excombatants

Functional Connectivity

Time Domain Frequency Domain Phase Domain


Pearson’s Correlation Imaginary Part of Co-
Coefficient herency
Coherence Function
Cross-Correlation func- Phase Lag Index
tion

Fig. 2. Functional connectivity metrics are divided into three categories. Metrics computed from time, frequency or phase
domain of EEG signals. Source: Authors.

The XCOR is the cross-covariance of In Eq. (3), 𝑆𝑥𝑥 (𝑓) and 𝑆𝑦𝑦 (𝑓) are the au-
two EEG signals, 𝑥(𝑡) and 𝑦(𝑡), scaled by to-spectral densities of 𝑥(𝑡) and 𝑦(𝑡), re-
their individual variance [22]. The XCOR spectively. Then, COH coefficients are
appraises the linear correlation between computed for each frequency f as follows:
the signals as a function of time (𝑡 =
1,2, … , 𝑇 − 𝜏): |𝑆𝑥𝑦(𝑓)|2 (4)
𝛤𝑥𝑦 (𝑓) =
𝑻−𝜏
𝑆𝑥𝑥 (𝑓)𝑆𝑦𝑦 (𝑓)
∑𝒕=𝟏 (𝑥(𝑡−𝜏)−𝑥̅ )(𝑦(𝑡)−𝑦̅)
𝐶𝑥𝑦 (𝜏) = (2)
√∑
𝑻−𝜏
𝒕=𝟏
𝑻−𝜏
(𝑥(𝑡)−𝑥̅ )2 ∑𝒕=𝟏 (𝑦(𝑡)−𝑦̅)2 The normalization factor puts coher-
ence on a scale from 0 to 1, where one
Where 𝜏 is the time lag determined by means complete coherence and zero, com-
the argument of the maximum XCOR plete independence between 𝑥(𝑡) and
When 𝜏 = 0, XCOR is equal to the Pear- 𝑦(𝑡) at frequency 𝑓.
son’s correlation coefficient. The result of The Imaginary Part of Coherency
𝐶𝑥𝑦 is a scalar value at a given time win- (ICOH) is obtained when complex values of
dow. XCOR values ranges between 0 ≤ the coherence are projected onto the imag-
𝐶𝑥𝑦 (𝜏) ≤ 1. When 𝐶𝑥𝑦 (𝜏) = 0, signals 𝑥(𝑡) inary axis [24]. ICOH is a metric of phase-
synchronization between two signals
and 𝑦(𝑡) have no linear interdependence at
𝑥(𝑡) and 𝑦(𝑡) that uses the same equation
time lag𝜏, and 𝐶𝑥𝑦 (𝜏) = 1 represents com-
as COH (Eq. 3), except that the imaginary
plete linear direct correlation at time lag 𝜏. part of coherence is selected before compu-
In the frequency domain, the Coherence ting the magnitude. ICOH is zero when the
Function (COH) quantifies the linear rela- cross-spectrum between the two EEG sig-
tions between signals at a specific frequen- nals, 𝑥(𝑡) and 𝑦(𝑡), has a 0° or 180° phase,
cy. COH is defined as the absolute value of and maximum when the cross-spectrum
the complex coherence [23]. Coherence has a phase of ±90°. Then, ICOH is not
estimates how the phases in two different affected by the 0° or 180° cross-spectral
channels are coupled to each other. Coher- relationship between the volume-
ence is calculated by the cross-spectral conducted activities of a single source at
density function 𝑆𝑥𝑦 of the two EEG sig- two separate sensors. Discarding contribu-
nals, normalized by their individual auto- tions to the connectivity estimate along the
spectral density functions. Complex coher- real axis explicitly removes instantaneous
ence is calculated as follows: potentially-spurious interactions due to
field spread of volume conduction. Thus,
𝑆𝑥𝑦 (𝑓) (3) ICOH captures true source interactions at
𝐶𝐶𝑥𝑦 =
√𝑆𝑥𝑥 (𝑓)𝑆𝑦𝑦 (𝑓) a given time lag [24].

TecnoLógicas, ISSN-p 0123-7799 / ISSN-e 2256-5337, Vol. 20, No. 40, sep-dic de 2017, pp. 83-96 [89]
Detecting atypical functioning of emotional processing in colombian excombatants

Phase-Lag Index (PLI) is a phase- tion (i.e. affective style, aggressive and
synchronization metric that quantifies the violent behavior, emotional processing and
asymmetry of the distribution of phase emotion regulation),. The circuit involves
differences between two signals [25]. PLI is not only subcortical areas (e.g., amygdala
based on the imaginary component of the or the basal ganglia), but also cortical are-
cross-spectrum; then, it is not spuriously as, mainly Prefrontal Cortex (PFC), Ante-
affected by volume conduction or by a rior Cingulate Cortex (ACC), as well tem-
common reference. PLI is computed by poral and medial parietal cortices [26].
averaging the sign of the estimated phase Considering these findings, we defined 10
difference between 𝑥(𝑡) and 𝑦(𝑡) per obser- initial regions of interest (ROI) for further
vation: connectivity analysis of interaction pat-
terns. Subsequently, the connectivity spa-
𝑃𝐿𝐼𝑥𝑦 = 𝖤[sgn[(∆𝜑𝑡 )]] (5) tial patterns of the selected metric and the
results of a Wilcoxon Rank-Sum statistical
Where 𝖤[·] is the expected value opera- test were analyzed to eliminate the regions
tor, sgn[⋅] is the sign function, and ∆𝜑𝑡 is where no significant differences were
the phase angle difference between the found between ex-combatants and controls
signals at time instant t. The range of PLI for any of the connections across these and
is 0 ≤ 𝑃𝐿𝐼𝑥𝑦 ≤ 1. When 𝑃𝐿𝐼𝑥𝑦 = 0 there is other regions. The initial ROIs are depict-
no coupling between the signals 𝑥(𝑡) and ed in Fig. 3.
𝑦(𝑡), when 𝑃𝐿𝐼𝑥𝑦 = 1, there is perfect phase Linear Discriminant Analysis LDA [27]
locking at a value of ∆𝜑𝑡 between both was used to compare the performance of
signals. the functional connectivity metrics when
classifying ex-combatants vs. civilians for
2.3 Selection of the Regions of Interest each condition of the emotional processing
(ROIs) experimental task (negative, neutral and
positive) in the previously described ROIs
Several studies have reported that a and for each tested frequency band.
circuit of activated or deactivated brain
regions is involved in many aspects of emo-

Fig. 3. ROIs and related electrodes defined for the connectivity analysis. Source: Authors.

[90] TecnoLógicas, ISSN-p 0123-7799 / ISSN-e 2256-5337, Vol. 20, No. 40, sep-dic de 2017, pp. 83-96
Detecting atypical functioning of emotional processing in colombian excombatants

We used the Wilcoxon rank-sum test one had higher accuracy for one or two out
[28] to identify the group differences in of five frequency bands, except for COH
functional connectivity between ex- with none.
combatants and civilians. Three between- For the positive condition, Table. 4
group Wilcoxon Rank-Sum tests were cal- shows that the performance of ICOH was
culated: 1. Group (Ex-combatants vs. Con- considerably better in the Beta band than
trols), 2. Condition × Group, and 3. Condi- the other metrics. Additionally, ICOH had
tion × Band × Group. Statistical analyses a better performance in Theta and Gamma
were performed using MATLAB and a bands. COH showed better performance in
significance level of p < 0.05. All the tests the Delta band and PLI showed better
were subjected to correction for multiple performance in the Alpha band.
comparison. With these comparisons, we
expected to find significant differences 3.2 Representation of spatial patterns
between Colombian ex-combatants and
individuals not directly exposed to the The topographical connectivity maps
armed conflict for Alpha and Beta frequency bands across
each condition are depicted in Fig. 4. Each
map represents the within-group average
3. RESULTS AND DISCUSSION value of the connectivity metric per elec-
trode. The strongest connection is depicted
3.1 Selection of the functional connectivity in red color and the weakest in dark blue.
metric All the maps were plotted using the topo-
graphic plot function of EEGLab toolbox
The connectivity metrics presented [20]. Based on Fig. 4, the connectivity spa-
above were analyzed. Different LDAs were tial patterns of COR, XCOR and COH
implemented for task conditions and fre- suggest that their results were affected by
quency bands. Forty-five features for LDA volume conduction. Besides, the ICOH and
were obtained by averaging the connectivi- PLI patterns were similar to each other in
ty values from all electrodes from one ROI both groups, concentrated in the occipital-
to another. For instance, the connectivity parietal brain areas. Together with LDA
from left frontal-central to right frontal- results, ICOH had the best performance
central regions (RoI 3 and RoI 4 in Fig. 3) when classifying ex-combatants vs. civil-
is the average connectivity of all pairs from ians. Thus, ICOH was selected for further
(F1, Fc1, F3 and Fc3) to (F2, F4, Fc2 and analysis.
Fc4). Then, a vector of 45 features per
subject was the input for each LDA classi- 3.3 Selection of the brain region of interest
fier. The LDA performances were evaluat-
ed using a 10-fold cross-validation for each Regarding the ROI, the connectivity spa-
class. LDA classification accuracy for nega- tial patterns of ICOH exhibit low connec-
tive, neutral and positive conditions is tivity in the frontal regions in most fre-
shown in Tables 2, 3 and 4, respectively. quency bands (See Fig. S1-S5) for every
For the negative condition, Table 2 task condition. Additionally, no significant
shows that the metric with highest per- differences were found between ex-
formance was ICOH in three out of five combatants and controls in any of the con-
(Delta, Theta and Alpha) frequency bands. nections across the frontal regions (ROI1 to
COH had a better performance for Beta ROI4) and the remaining area. Even
and Gamma bands. For the neutral condi- though the frontal lobe is crucial for cogni-
tion, Table. 3 shows no concrete results tive control functioning, there is no evi-
about which metric was better, since each dence of a difference in this dimension in

TecnoLógicas, ISSN-p 0123-7799 / ISSN-e 2256-5337, Vol. 20, No. 40, sep-dic de 2017, pp. 83-96 [91]
Detecting atypical functioning of emotional processing in colombian excombatants

Fig. 4. Topographic plots. Spatial patters of five connectivity metrics for ex-combatants and civilians by condition (negative,
neutral and positive) and frequency band (Alpha and Beta). Source: Authors.

ex-combatants. Indeed, previous studies ROI4= P1, P3, Po3 and Po5, ROI5= PZ and
have suggested a reorganization of posteri- PoZ, and ROI6= P2, P4, Po4 and PO6.
or neural regions during the processing of
social cognition among ex-combatants [3, 3.4 Statistical test results
6]. Particularly, N170 is a posterior ERP
component that has been associated with Group (Ex-combatants vs. Controls): In
valence recognition of faces and words. In this test, the full information (all frequency
this line, studies in ex-combatants have bands and all conditions) was included. No
suggested a larger activation across parie- significant differences were found in each
tal regions during face processing and pair. However, the p-values suggested a
limited modulation for the emotional con- tendency to differentiate the connectivity
tent of words. This kind of modulation has of both groups between pairs: ROI1-ROI2
not been reported in frontal areas. It (p=0.021, q=0.173), ROI2-ROI3 (p=0.023,
should be noted that this is an emotional q=0.173) and ROI3-ROI5 (p=0.049,
recognition task designed to modulate and q=0.245). In these three cases, the median
activate posterior and central areas, i.e., connectivity between ROIs was higher in
the task does not include an explicit cogni- the controls than in the ex-combatants
tive control instruction necessary to elicit group, and the percentages of difference in
more robust anterior activation. connectivity were 11%, 8% and 10%, re-
Then, the four frontal ROIs were reject- spectively (See Table S1).
ed for the final model. The new ROIs were Condition × Group: No significant dif-
ROI1= C1, Cp1, C3 and Cp3, ROI2= Cz ferences were found between ex-
and CpZ, ROI3= C2, Cp2, C4 and Cp4, combatants and controls for negative and
neutral conditions. Significant differences

[92] TecnoLógicas, ISSN-p 0123-7799 / ISSN-e 2256-5337, Vol. 20, No. 40, sep-dic de 2017, pp. 83-96
Detecting atypical functioning of emotional processing in colombian excombatants

Table 2. LDA classification accuracy (95% confidence) for the negative condition. Source: Authors.
Negative DELTA THETA ALPHA BETA GAMMA
54 % 50 % 54 % 56 % 52 %
COR (39, 45 % - 67, 9 7 %) (35, 71 % - 64, 28 %) (39, 45 % - 67, 97 %) (41, 34 % - 69, 7 9 %) (37, 57% - 66, 13 %)
58 % 50 % 52 % 54 % 52 %
XCOR (43, 26 % - 71, 5 9 %) (35, 7 1 % - 64, 28 %) (37, 57 % - 66, 13 %) (39, 45 % - 67, 97 %) (37, 57 % - 66, 13 %)

50 % 52 % 52 % 62 % 56 %
COH (35, 71 % - 64, 28 %) (37, 57 % - 66, 13 %) (37, 57 % - 66, 13 %) (47, 16 % - 75, 12 %) (41, 34 % - 69, 79 %)

64% 64 % 68 % 56 % 54 %
ICOH (49, 14 % - 76, 85 %) (49, 14 % - 76, 85 %) (53, 1 6 % - 80, 26 %) (41, 34 % - 69, 79 %) (39, 45 % - 67, 97 %)

52 % 54 % 58 % 54 % 54 %
PLI (37, 57 % - 66, 13 %) (39, 45 % - 67, 97 %) (43, 26 % - 71, 59 %) (39, 45 % - 67, 97 %) (39, 45 % - 67, 97%)

Table 3. LDA classification accuracy (95% confidence) for the neutral condition. Source: Authors.
Neutral DELTA THETA ALPHA BETA GAMMA
64 % 58 % 62 % 50 % 54 %
COR (49, 14 % - 76, 85 %) (43, 26 % - 71, 59 %) (47, 16 % - 75, 12 %) (35, 71 % - 64, 28 %) (39, 45 % - 67, 97 %)

52 % 62 % 52 % 66 % 54 %
XCOR (37, 57 % - 66, 13 %) (47, 16 % - 75, 12 %) (37, 57 % - 66, 13 %) (51, 14 % - 78, 57 %) (39, 45 % - 67, 97 %)

52 % 52 % 50 % 52 % 52 %
COH (37, 5 7 % - 66, 13 %) (37, 57 % - 66, 13 %) (35, 71 % - 64, 28 %) (37, 57 % - 66, 13 %) (37, 57 % - 66, 13 %)

52 % 54 % 58 % 54 % 58 %
ICOH (37, 57 % - 66, 13 %) (39, 45 % - 67, 97 %) (43, 26 % - 71, 59 %) (39, 45 % - 67, 97 %) (43, 26 % - 71, 59 %)

58 % 52 % 54 % 66 % 54 %
PLI (43, 26 % - 71, 59 %) (37, 57 % - 66, 13 %) (39, 45 % - 67, 97 %) (51, 14 % - 78, 57 %) (39, 45 % - 67, 97 %)

Table 4. LDA classification accuracy (95% confidence) for the positive condition. Source: Authors.
Positive DELTA THETA ALPHA BETA GAMMA
60 % 56 % 52 % 50 % 50%
COR (45, 2 % - 73, 36 %) (41, 34 % - 69, 79 %) (37, 57 % - 66, 13 %) (35, 71 % - 64, 28 %) (35, 71% - 64, 28%)
60 % 58 % 50 % 68 % 52 %
XCOR (45, 2 % - 73, 36 %) (43, 26 % - 71, 59 %) (35, 71 % - 64, 28 %) (53, 16 % - 80, 26 %) (37, 57 % - 66, 13 %)

62 % 54 % 56 % 62 % 50 %
COH (47, 16 % - 75, 12 %) (39, 45 % - 67, 97 %) (41, 34 % - 69, 79 %) (47, 16 % - 75, 12 %) (35, 71 % - 64, 28 %)

52 % 60% 50% 76 % 56 %
ICOH (37, 57 % - 66, 13 %) (45, 2% - 73, 36%) (35, 71% - 64, 28%) (61, 51 % - 86, 77 %) (41, 34 % - 69, 79 %)

54 % 56 % 64 % 56 % 52 %
PLI (39, 45 % - 67, 97 %) (41, 34 % - 69, 79 %) (49, 14 % - 76, 85 %) (41, 34 % - 69, 79 %) (37, 57 % - 66, 13 %)

between ex-combatants and controls were ROI4 was 26.79% higher in the control
found in the connectivity across ROI1- group (See Table S2).
ROI4 (p=0.0027, q=0.0209) and ROI3-ROI4 Condition × Band × Group: No signifi-
(p=0.0010, q=0.0152) for the positive condi- cant differences between ex-combatants
tion. Consistently with the differences and controls were found in Delta, Theta,
found in the first test, the connectivity Alpha, and Gamma bands for any condi-
across these regions was higher in controls. tion. In the Beta band, significant differ-
The connectivity across regions ROI1 and ences between ex-combatants and controls
ROI4 was 17.42%, and across ROI3 and were found for positive condition in the

TecnoLógicas, ISSN-p 0123-7799 / ISSN-e 2256-5337, Vol. 20, No. 40, sep-dic de 2017, pp. 83-96 [93]
Detecting atypical functioning of emotional processing in colombian excombatants

connectivity between regions ROI2-ROI4 Their connectivity spatial pattern repre-


(p=0.0044, q=0.0336), and between regions sentations were affected and several LDA
ROI3-ROI4 (p=0.0005, q=0.0088). The were implemented. As a result, we identi-
connectivity of controls in ROI2-ROI4 and fied that COR, XCOR and COH metrics
ROI3-ROI4 was 17.63% and 27.46% higher were influenced by the volume conduction,
than the ex-combatants’ connectivity, re- because their patterns revealed that the
spectively (See Table S3-S7). connectivity was dominated by local con-
With the proposed methodology, signifi- nections among adjacent sensors. In con-
cant differences between ex-combatants trast, PLI and ICOH patterns were similar
and civilian people were obtained. Differ- to each other. Additionally, local connec-
ences in the connectivity were found in the tions were absent in ICOH and PLI. Then,
stimulus with positive valence in the Beta with the results of the LDA we concluded
frequency band. Even though neutral va- that ICOH presented the best perfor-
lence is commonly misclassified as nega- mance, because using this metric we ob-
tive in normal population, the recognition tained higher accuracy values for two out
of emotional stimuli that refers to potential of the three task conditions.
negative/neutral information is necessary By using the ICOH metric, ex-
for evolutionary purposes [29]. In this combatants presented significant differ-
sense, combat experience might preserve ences in the processing of emotional infor-
the ability to categorize images with con- mation with positive valence. These differ-
tent. ences were found in the connectivity across
The overall results are consistent with two pairs in the Beta frequency band: the
Table. 4, in which the best performance for first is composed of the medial central-
the ICOH metric in the beta band corre- parietal (Cz-Cpz) and the right central-
sponded to the positive stimulus. The Beta parietal (C2, Cp2, C4, Cp4) regions, and
band has been associated with emotional the second one comprises the right central-
processing in the evaluation of all types of parietal and left parietal-occipital (P1, P3,
valence [30]. Some studies demonstrated a Po3, Po5) regions. Based on these results,
wide posterior and anterior synchroniza- we conclude that Colombian ex-combatants
tion associated with the evaluation of posi- and civilians present a similar processing
tive content [30]. The authors found that of emotional information for stimuli with
the Beta band was more strongly involved neutral and negative valence, but there are
in the evaluation of positive content than differences in the stimuli with positive
negative-valence content [31]. Additionally, valence. This atypical connectivity may be
these findings support the literature re- due to the conditions experienced in the
garding the difficulties Colombian ex- armed conflict. There is potential in using
combatants have to process emotional these functional markers in diagnosis and
information with positive valence [6, 7]. as a first step in the development of future
intervention treatments. The use of biolog-
ical markers obtained with this method
4. CONCLUSIONS might help to complement neuropsychiat-
ric evaluation of chronic exposition to com-
In this work, we presented a methodol- bat (i.e., Post-traumatic Stress Disorder)
ogy to find atypical functioning in the EP and be the basis for future intervention
of Colombian ex-combatants using brain treatments, not only for ex-combatants,
connectivity analysis. First, we presented but for population directly exposed to
the advantages and drawbacks of five armed conflicts.
widely used functional connectivity met-
rics: COR, XCOR, COH, ICOH, and PLI.

[94] TecnoLógicas, ISSN-p 0123-7799 / ISSN-e 2256-5337, Vol. 20, No. 40, sep-dic de 2017, pp. 83-96
Detecting atypical functioning of emotional processing in colombian excombatants

5. REFERENCES connectivity in emotion processing neural


circuitry to angry and happy faces in
adolescents with and without suicide
attempt,” Psychol. Med., vol. 43, no. 10, pp.
[1] S. Trujillo, N. Trujillo, J. D. Lopez, D. Gomez, 2129–2142, Oct. 2013.
S. Valencia, J. Rendon, D. A. Pineda, and M. [10] S. Haufe, V. V Nikulin, K.-R. Müller, and G.
A. Parra, “Social Cognitive Training Improves Nolte, “A critical assessment of connectivity
Emotional Processing and Reduces measures for EEG data: A simulation study,”
Aggressive Attitudes in Ex-combatants,” Neuroimage, vol. 64, pp. 120–133, Jan. 2013.
Front. Psychol., vol. 8, p. 510, Apr. 2017. [11] K. J. Friston, “Functional and Effective
[2] C. Tobón, D. C. Aguirre-Acevedo, L. Velilla, J. Connectivity: A Review,” Brain Connect., vol.
Duque, C. P. Ramos, and D. Pineda, “Perfil 1, no. 1, pp. 13–36, Jan. 2011.
psiquiátrico, cognitivo y de reconocimiento de [12] N. M. Kleinhans, T. Richards, L. Sterling, K.
características emocionales de un grupo de C. Stegbauer, R. Mahurin, L. C. Johnson, J.
excombatientes de los grupos armados Greenson, G. Dawson, and E. Aylward,
ilegales en Colombia,” Rev. Colomb. “Abnormal functional connectivity in autism
Psiquiatr., vol. 45, no. 1, pp. 28–36, Jan. 2016. spectrum disorders during face processing,”
[3] S. P. Trujillo, S. Valencia, N. Trujillo, J. E. Brain, vol. 131, no. 4, pp. 1000–1012, Apr.
Ugarriza, M. V. Rodríguez, J. Rendón, D. A. 2008.
Pineda, J. D. López, A. Ibañez, and M. A. [13] M. X. Cohen, Analyzing neural time series
Parra, “Atypical Modulations of N170 data: theory and practice. MIT Press, 2014.
Component during Emotional Processing and [14] E. W. Lang, A. M. Tomé, I. R. Keck, J. M.
Their Links to Social Behaviors in Ex- Górriz-Sáez, and C. G. Puntonet, “Brain
combatants,” Front. Hum. Neurosci., vol. 11, Connectivity Analysis: A Short Survey,”
p. 244, May 2017. Comput. Intell. Neurosci., vol. 2012, pp. 1–
[4] M. Batty and M. J. Taylor, “Early processing 21, 2012.
of the six basic facial emotional expressions,” [15] P. Lang and M. M. Bradley, The
Cogn. Brain Res., vol. 17, no. 3, pp. 613–620, International Affective Picture System (IAPS)
Oct. 2003. in the study of emotion and attention, vol. 29.
[5] R. A. Morey, C. M. Petty, D. A. Cooper, K. S. Oxford University Press USA New-York, NY,
LaBar, and G. McCarthy, “Neural systems for USA, 2007.
executive and emotional processing are [16] J. A. Mikels, B. L. Fredrickson, G. R. Larkin,
modulated by symptoms of posttraumatic C. M. Lindberg, S. J. Maglio, and P. A.
stress disorder in Iraq War veterans,” Reuter-Lorenz, “Emotional category data on
Psychiatry Res. Neuroimaging, vol. 162, no. 1, images from the international affective
pp. 59–72, Jan. 2008. picture system,” Behav. Res. Methods, vol.
[6] C. Tobón, A. Ibañez, L. Velilla, J. Duque, J. 37, no. 4, pp. 626–630, Nov. 2005.
Ochoa, N. Trujillo, J. Decety, and D. Pineda, [17] C. A. Gantiva Díaz, P. Guerra Muñoz, and J.
“Emotional processing in Colombian ex- Vila Castellar, “Colombian validation of the
combatants and its relationship with empathy international affective picture system:
and executive functions,” Soc. Neurosci., vol. Evidence of cross-cultural origins of
10, no. 2, pp. 153–165, Mar. 2015. emotion,” Acta Colomb. Psicol., vol. 14, no. 2,
[7] A. Quintero-Zea, L. M. Sepúlveda-Cano, M. pp. 103–111, 2011.
Rodríguez Calvache, S. Trujillo Orrego, N. [18] W. Schneider, A. Eschman, and A.
Trujillo Orrego, and J. D. López, Zuccolotto, “E-prime, Version 1.1,”
“Characterization Framework for Ex- Pittsburgh, PA: Psychology Software Tools.
combatants Based on EEG and Behavioral 2002.
Features,” in VII Latin American Congress on [19] C. Neuroscan, “NeuroScan 4.5,” North
Biomedical Engineering CLAIB 2016, Carolina: Compumedics USA. 2008.
Bucaramanga, Santander, Colombia, October [20] A. Delorme and S. Makeig, “EEGLAB: an
26th-28th, 2016, 2017, pp. 205–208. open source toolbox for analysis of single-
[8] A. Carballedo, J. Scheuerecker, E. trial EEG dynamics including independent
Meisenzahl, V. Schoepf, A. Bokde, H.-J. component analysis,” J. Neurosci. Methods,
Möller, M. Doyle, M. Wiesmann, and T. Frodl, vol. 134, no. 1, pp. 9–21, Mar. 2004.
“Functional connectivity of emotional [21] M. R. Calvache, A. Quintero-Zea, S. T.
processing in depression,” J. Affect. Disord., Orrego, N. T. Orrego, and J. D. Lopez,
vol. 134, no. 1–3, pp. 272–279, Nov. 2011. “Classifying artifacts and neural EEG
[9] L. A. Pan, S. Hassel, A. M. Segreti, S. A. Nau, components using SVM,” in 2016 IEEE Latin
D. A. Brent, and M. L. Phillips, “Differential American Conference on Computational
patterns of activity and functional Intelligence (LA-CCI), 2016, pp. 1–5.

TecnoLógicas, ISSN-p 0123-7799 / ISSN-e 2256-5337, Vol. 20, No. 40, sep-dic de 2017, pp. 83-96 [95]
Detecting atypical functioning of emotional processing in colombian excombatants

time course of emotional processing,”


[22] M. A. B. Brazier and J. U. Casby, Neuroimage, vol. 21, no. 4, pp. 1189–1203,
“Crosscorrelation and autocorrelation studies Apr. 2004.
of electroencephalographic potentials,” [27] P. Xanthopoulos, P. M. Pardalos, and T. B.
Electroencephalogr. Clin. Neurophysiol., vol. Trafalis, “Linear Discriminant Analysis,” in
4, no. 2, pp. 201–211, May 1952. Robust Data Mining, Springer, 2013, pp. 27–
[23] G. Pfurtscheller and C. Andrew, “Event- 33.
Related changes of band power and [28] F. Wilcoxon, “Individual Comparisons by
coherence: methodology and interpretation.,” Ranking Methods,” Biometrics Bull., vol. 1,
J. Clin. Neurophysiol., vol. 16, no. 6, pp. 512– no. 6, p. 80, Dec. 1945.
519, Nov. 1999. [29] Y.-Y. Lee and S. Hsieh, “Classifying
[24] G. Nolte, O. Bai, L. Wheaton, Z. Mari, S. Different Emotional States by Means of
Vorbach, and M. Hallett, “Identifying true EEG-Based Functional Connectivity
brain interaction from EEG data using the Patterns,” PLoS One, vol. 9, no. 4, p. e95415,
imaginary part of coherency,” Clin. Apr. 2014.
Neurophysiol., vol. 115, no. 10, pp. 2292– [30] M. Balconi and C. Lucchiari, “EEG correlates
2307, Oct. 2004. (event-related desynchronization) of
[25] C. J. Stam, G. Nolte, and A. Daffertshofer, emotional face elaboration: A temporal
“Phase lag index: Assessment of functional analysis,” Neurosci. Lett., vol. 392, no. 1–2,
connectivity from multi channel EEG and pp. 118–123, Jan. 2006.
MEG with diminished bias from common [31] T. Costa, E. Rognoni, and D. Galati, “EEG
sources,” Hum. Brain Mapp., vol. 28, no. 11, phase synchronization during emotional
pp. 1178–1193, Nov. 2007. response to positive and negative film
[26] M. Esslen, R. . Pascual-Marqui, D. Hell, K. stimuli,” Neurosci. Lett., vol. 406, no. 3, pp.
Kochi, and D. Lehmann, “Brain areas and 159–164, Oct. 2006.

[96] TecnoLógicas, ISSN-p 0123-7799 / ISSN-e 2256-5337, Vol. 20, No. 40, sep-dic de 2017, pp. 83-96

You might also like