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Modulation of Physiological Responses as

Indices of Attentional Bias in Dysphoria

Article in International Journal of Mental Health and Addiction · May 2017

DOI: 10.1007/s11469-017-9774-7

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Int J Ment Health Addiction
DOI 10.1007/s11469-017-9774-7

O R I G I N A L A RT I C L E

Modulation of Physiological Responses as Indices

of Attentional Bias in Dysphoria

Carlos Gantiva 1 & Andrés Araujo 1 &

Narayana Aragão 1 & Nohelia Hewitt 1

# Springer Science+Business Media New York 2017

Abstract The experimental results on attentional bias in depression have been contradictory.
Research on physiological correlates that validate attentional bias have been scarce. The aim of
the present study was to evaluate physiological responses associated with attentional bias in
dysphoria. Heart rate and the galvanic skin response were recorded in 30 dysphoric individuals
and 30 nondysphoric individuals while they performed an emotional Stroop task. Dysphoric
individuals exhibited attentional bias and heart rate deceleration in response to unpleasant
words. Nondysphoric individuals exhibited attentional bias toward pleasant words, accompa-
nied by a higher skin conductance response. These results suggest that heart rate deceleration
in response to unpleasant words correlated with attentional bias in dysphoric individuals.

Keywords Attentional bias . Dysphoria . Heart rate . Skin conductance response . Stroop

Dysphoria is a state that is characterized by overall discomfort, disability, anxiety, depression,

and hostility, generally indicating a negative affective state. This global feeling of dysphoria
has been shown to be correlated with greater self-consciousness and somatic symptoms
(Barsky et al. 1988). Mood-congruent attentional bias has been proposed to be a variable that
can explain the etiology and maintenance of different disorders, including generalized anxiety
disorder and depression (Mogg and Bradley 2005). Studies that utilized the classic Stroop task
(Stroop 1935) and variations as Bemotional Stroop^ (MacLeod 1991) have reported consistent
results regarding the presence of attentional bias in anxiety but contradictory results regarding
memory bias. The results of studies of depression have been consistent regarding memory and
interpretation biases but contradictory regarding attentional bias (Dalgleish and Watts 1990;
Mathews and MacLeod 1994; Mineka et al. 1998; Mogg and Bradley 2005).

* Carlos Gantiva
cgantiva@usbbog.edu.co; cgantiva@gmail.com

1
Department of Psychology, University of San Buenaventura, Cr 8 H # 172-20, Bogotá, Colombia
 Int J Ment Health Addiction

For example, recent studies found no evidence of attentional bias in an emotional Stroop
task in patients with depression and dysphoria (Cheng et al. 2015; Sass et al. 2014). However,
other studies have reported the presence of attentional bias in comorbid depression and PTSD,
specifically in response to words that were associated with the traumatic event (Hauschildt
et al. 2013). Attentional bias toward suicide-related words was recently reported in individuals
who attempted suicide, but no attentional bias toward aversive words was found (Richard-
Devantoy et al. 2016). Other studies evaluated dysphoric individuals and found evidence of
attentional bias toward aversive words and coherence between attentional and memory biases
toward aversive words; in nondysphoric individuals, attentional bias toward positive words
was observed (Koster et al. 2005; Koster et al. 2010).
A meta-analysis of 47 studies that used the Stroop task in individuals with depression,
depressive symptoms, and sadness (Epp et al. 2012) reported quantitative evidence of atten-
tional bias in depression, based on statistical measurement techniques and comparisons of effect
sizes. The results of the meta-analysis showed a large interference effect in the emotional Stroop
task in response to negative words in participants with clinical depression compared with
controls. The study also found significant effects in both dysphoric individuals and participants
with induced sadness under experimental conditions compared with controls. Attentional bias
toward positive words was found in control groups compared with individuals with clinical
depression and dysphoria but not in participants with induced sadness. The results also showed
that attentional bias increased as the level of depression increased, indicating that an increase in
attentional bias is an indicator of an increase in depressive symptoms. These results were found
even without using depression-related words and only pleasant, neutral, and unpleasant words.
Attentional bias in depression can be explained by theories of emotional networks that were
proposed by Lang (1979) and Bower (1981). These theories posit a strong association between
emotion and cognition, in which emotional states influence associative processes, memory, the
interpretation of ambiguous situations, and the salience of stimuli that are consistent with the
emotional state. Thus, attention and learning increase in response to congruent mood-related
stimuli. This leads people to actively attend to stimuli that are consistent with their mood.
Stimuli that are congruent with their emotions are more salient than those that are not (Clark
et al. 1999). These models are complemented by the Parallel Distributed Process model
(Cohen et al. 1990), which states that there are two cognitive pathways that are involved in
Stroop tasks, one for the color name and one for the meaning of the word, in which greater
attentional resources are devoted to one pathway as the other pathway loses relevance.
Previous studies sought to identify autonomic responses that characterize the emotion of
sadness. Sadness that is accompanied by the physiological response of crying is characterized
by an increase in cardiovascular sympathetic control and changes in respiratory activity. When
not accompanied by crying, sadness is characterized by sympathetic withdrawal (Kreibig
2010). A recent study found elevated skin temperature and accentuated respiratory frequency
in depressed individuals, suggesting an increase in physiological arousal (Wenzler et al. 2017).
Some studies suggested that a lower galvanic skin response is a biomarker of depression
(Storrie et al. 1981; Ward et al. 1983), whereas other studies suggested the opposite
(Schneider et al. 2012; Toone et al. 1981). In fact, affective disorders have been repeatedly
linked to alterations of the patterns of autonomic nervous system function, particularly with
regard to changes in the cardiac response (Bassett 2016; Brunoni et al. 2013).
Some physiological responses have proven to be indicators of cognitive processes, including
the skin conductance for orientation (Mathersul et al. 2013) and heart rate deceleration for
attention (Bradley et al. 2001; Guerra et al. 2016; Klorman et al. 1977). Although evidence
Int J Ment Health Addiction

suggests the presence of attentional bias in depression and dysphoria, few studies have evaluated
the underlying physiological mechanisms (Epp et al. 2012). Blanchette and Richards (2013)
found differences in attentional bias among anxious individuals and a control group, but no
differences were found between groups in the skin conductance or activity of the corrugator
muscle during exposure to threatening stimuli, suggesting differences within cognitive processes
rather than emotional reactions to stimuli that indicate a threat. In patients with major depressive
disorder, Jin et al. (2015) found lower heart rate reactivity in response to images and videos with
different emotional content, but these authors did not evaluate possible relationships to attentional
bias. Although attentional bias is clearly seen in individuals with dysphoria, the underlying
physiological mechanisms that are related to attentional processes are poorly understood and
could provide valuable information for the evaluation and treatment of dysphoria and depression.
Therefore, the objective of the present study was to evaluate the physiological responses
associated with attentional bias in individuals with dysphoria using an emotional Stroop task.

Methods

Participants

The sample consisted of 60 university students who were selected through non-probabilistic
sampling. The participants were distributed into two groups according to scores on the Beck
Depression Inventory-II (BDI-II; Beck et al. 1996): one group of dysphoric participants
(n = 30) based on a BDI-II cutoff score >9 and one group of nondysphoric participants based
on a BDI-II cutoff score <5 (n = 30) (as proposed by Kendall et al. 1987). The participants only
differed in BDI-II scores. They did not differ by sex or age between the two groups (Table 1).
The sample size was determined based on a power analysis using G*POWER 3 software
(Erdfelder et al. 1996) and standard statistical criteria (α = .05, 1-β = .80, moderate effect
size = .25). All of the participants were right-handed and had normal or corrected-to-normal
vision. The exclusion criteria were current medical or psychological treatment and visual/
auditory problems without correction. All of the participants provided written informed
consent. The study was approved by the University of San Buenaventura Review Board.

Self-Report Measures

The Spanish version of the BDI-II for university students (Sanz et al. 2003) was used to
measure depression. The BDI-II is a 21-item, self-report measure of the severity of depressive
symptoms. The reliability and validity of the Spanish version of the BDI-II for university

Table 1 Demographic variables and BDI-II scores by group

Nondysphoric Dysphoric t or χ2 df p

Age, years (mean [SD]) 21.3 (2.7) 20.1 (1.8) 2.32 78 .20
Female (n) 16 13 1.80 1 .17
Male (n) 14 17
BDI-II (mean [SD]) 2.85 (2.03) 15.8 (7.2) −10.89 78 < .0001

p < .05
SD standard deviation
 Int J Ment Health Addiction

students were .71 and .89, respectively. The internal consistency of this scale in the present
study was excellent (α = .93).

Emotional Stroop Task

The emotional Stroop task was design using E-Prime 2.0 software (Psychology Software
Tools, PA, USA). We selected 12 words (four pleasant, four neutral, and four unpleasant) from
the Affective Norms for English Words1 (ANEW; Bradley and Lang 1999), which were
translated to Spanish by Redondo et al. (2007) and used in previous studies in the Colombian
population (Gantiva et al. 2015; Gantiva and Camacho 2016). In each word category, the
length of the words was controlled; two two-syllable words and two three-syllable words were
selected. For the ANEW words that were selected, significant differences were found between
word categories in the valence dimension (all p < .001). For the arousal dimension, significant
differences were found between affective words (pleasant and unpleasant) and neutral words
(both p = .001).
The words were presented in red, blue, green, and yellow on a black background on a 19-in.
flat-screen monitor that was located approximately 60 cm from the participant. The participant
was asked to press with his right hand the key on the keyboard that was the same color as the
word, regardless of the word’s meaning. The experimental session was composed of 192 trials
that were divided into three blocks (one for each word’s category).
Each block included the four words of one word category, which were repeated
four times for each color in a pseudorandom order to ensure that neither the same
word nor the same color was presented in direct sequence, for a total of 64 trials per
block. The presentation of a word-stimulus lasted 1500 ms, followed by an intertrial
interval of 350 ms. Between each block, the participants had a resting period of 30 s,
during which time a white cross appeared on the black screen. The emotional Stroop
task lasted an average of 10 min. Three different block presentation orders were
prepared to avoid sequence bias. Before testing, five training trails were conducted
to rehearse dexterity to minimize error variance.

Physiological Measures

All of the physiological measures were recorded using PowerLab 26T equipment
(ADInstruments, Australia). A computer that ran E-Prime 2.0 software was synchro-
nized with the PowerLab 26 T equipment via a parallel port. Heart rate was derived
from the electrocardiogram using three large Sensormedic electrodes that were filled
with electrolyte paste at lead III. R-waves were detected from the electrocardiogram
data using a software peak detector (LabChart 7.3, ADInstruments, Australia). R-R
intervals were then converted into heart rate (in beats per minute). Skin conductance
was recorded from two dry, bright-plated bipolar electrodes that were placed on the
intermediate phalanges of digits II and IV of the non-dominant hand. The signal was
calibrated before each session to detect activity in the range of 0–40 μS
(microSiemens) and recorded using an ADInstruments Model ML116 GSRAmp. All
of the signals were acquired at a sampling rate of 1000 Hz.

1
Pleasant words: kiss, orgasm, love, caress. Neutral words: pencil, paper, board, cell. Unpleasant words: war,
bomb, abuse, torture.
Int J Ment Health Addiction

Data Reduction and Analysis

Reaction time (RT) was calculated in milliseconds (ms). To discard impulsive responses and
according to the methodology of Blanchette and Richards (2013), RTs <300 ms were excluded
from the analyses. This resulted in the exclusion of 1.2% of the data. Accurate responses were
recorded when correspondence was observed between the color of the word and the color of
the selected key on the keyboard. Only accurate responses were included in the analyses
(98.7%). The percent accuracy for each word category (pleasant, neutral, and unpleasant) was
calculated. According to the methodology of Blanchette and Richards (2013) and Fridrici et al.
(2014), for each participant, we calculated an index of Stroop interference for pleasant words
(RTpleasant words – RTneutral words) and unpleasant words (RTunpleasant words – RTneutral words).
Positive values indicated interference and thus an attentional bias.
The heart rate response and skin conductance level (SCL) were determined by subtracting
the average activity during the 5 s before each block from the average activity during each
block of word presentation.
Reaction time, percent accuracy, the heart rate response, and the SCL were
analyzed using a 2 × 3 analysis of variance (ANOVA), with Group (dysphoric vs.
nondysphoric) as the between-group factor and Word category (pleasant, neutral, and
unpleasant) as the repeated measure. The index of Stroop interference was analyzed
using a 2 × 2 ANOVA, with Group (dysphoric vs. nondysphoric) as the between-
group factor and Word category (pleasant and unpleasant) as the repeated measure.
When the assumption of sphericity was not met, Greenhouse-Geisser correction was
applied to the degrees of freedom in all cases. Post hoc analyses of the mean values
were performed using paired multiple comparisons, adjusted with Bonferroni correc-
tion. Finally, a Pearson correlation was used to analyze the association between BDI-
II scores and RTs, the index of Stroop interference, accuracy rate, the heart rate
response, and the SCL. The level of significance was p ≤ .05 for all of the analyses,
and the effect size (ηp2 and R2) is reported. All of the statistical analyses were
performed using Statistical Package for Social Sciences (SPSS) 20.0 software.

Results

Reaction Time

The ANOVA of the RT data revealed a significant Group × Word category interaction
(F2,156 = 6.47, p = .003, ηp2 = .07). Dysphoric participants had longer RTs in response to
unpleasant words compared with pleasant words (p = .017; Fig. 1a). Nondysphoric participants
had longer RTs in response to pleasant words compared with unpleasant words (p = .001;
Fig. 1a). No significant main effects were found (both p > .70). The ANOVA of percent
accuracy revealed a trend toward a main effect of Group (F1,78 = 3.54, p = .06, ηp2 = .04).
Dysphoric individuals had a higher percent accuracy (97.3%) than nondysphoric individuals
(96.2%). The ANOVA of the Stroop interference index revealed a significant Group × Word
category interaction (F1,78 = 21.13, p < .0001, ηp2 = .21). Dysphoric participants exhibited
greater interference in response to unpleasant words compared with pleasant words (p = .006;
Fig. 1b). Nondysphoric participants exhibited greater interference in response to pleasant
words compared with unpleasant words (p < .001; Fig. 1b). Nondysphoric participants
 Int J Ment Health Addiction

Fig. 1 a Mean reaction times to pleasant, neutral, and unpleasant words in dysphoric and nondysphoric
participants. b Stroop interference effect in dysphoric and nondysphoric participants. Bars are standard error of
the mean. **p < .05, *p = .06

exhibited a trend toward greater interference in response to pleasant words compared with
dysphoric participants (p = .06; Fig. 1b).

Heart Rate Response

The ANOVA of the heart rate data revealed a significant main effect of Word category
(F2,156 = 3.93, p = .02, ηp2 = .02). Pleasant words produced greater heart rate deceleration
(M = −2.86, SD = .64) than unpleasant words (M = −.05, SD = .78, p = .01). The Group ×
Word category interaction was significant (F2,156 = 5.18, p = .007, ηp2 = .03). Unpleasant
words produced heart rate deceleration in dysphoric participants and heart rate acceleration in
nondysphoric participants (p = .001; Fig. 2).

Skin Conductance Level

The ANOVA of the SCL revealed a significant main effect of Word category (F2,156 = 10.25,
p < .001, ηp2 = .06). Pleasant words produced a significantly larger SCL (M = .02, SD = .004)
compared with neutral words (M = .007, SD = .004) and unpleasant words (M = .001,
SD = .007; both p < .001). The Group × Word category interaction was significant
(F2,156 = 3.18, p = .05, ηp2 = .02). Pleasant words produced a significantly larger SCL in
nondysphoric participants compared with dysphoric participants (p = .02; Fig. 3).

Correlation Analysis

The subjects’ BDI-II scores were negatively and significantly correlated with the heart rate
response to unpleasant words (r = −.24, p = .002, R2 = .06), RT to pleasant words (r = −.16,
p = .03, R2 = .02) and with index of Stroop interference to pleasant words (r = −.17, p = .02,
R2 = .03). This suggests that higher scores on the BDI-II were associated with greater heart rate
deceleration in response to unpleasant words and lower scores on the BDI-II were associated
with longer RTs in response to pleasant words and with greater interference in response to
pleasant words.
Int J Ment Health Addiction

Fig. 2 Heart rate responses to pleasant, neutral, and unpleasant words in dysphoric and nondysphoric partici-
pants. Bars are standard error of the mean. **p < .05

Discussion

The objective of the present study was to evaluate physiological responses associated with
attentional bias in dysphoria using an emotional Stroop task. The results revealed attentional
bias, a higher Stroop interference index, and heart rate deceleration in response to unpleasant
words in dysphoric participants. Nondysphoric participants exhibited attentional bias and a
greater SCL to pleasant words.
Our results are consistent with those reported previously in dysphoric individuals, in which
attentional bias toward unpleasant words was observed, whereas nondysphoric individuals
exhibited attentional bias toward pleasant words (Koster et al. 2005; Koster et al. 2010). These
results are also consistent with data from a meta-analysis by Epp et al. (2012), in which
attentional bias toward unpleasant words was identified in dysphoric participants. Altogether,
these results confirm the influence of emotional states on attentional responses (Bower 1981;
Lang 1979), in which individuals with depressive symptoms selectively attend to aversive
stimuli, and such stimuli are more salient.
The observation of heart rate deceleration in response to unpleasant words corroborates
attentional bias that is observed in dysphoria. Previous studies have shown that sustained heart
rate deceleration is an indicator of sustained attention (Bradley et al. 2001; Klorman et al.
1977). According to the defense cascade model (Lang et al. 1997), defensive responses begin
with a stage of oriented attention (e.g., distant threat) and progress to a stage of defensive
action (e.g., imminent attack). Heart rate deceleration is a characteristic physiological response
associated with the stage of attention. Sustained heart rate deceleration is the most common
 Int J Ment Health Addiction

Fig. 3 Skin conductance level to pleasant, neutral, and unpleasant words in dysphoric and nondysphoric
participants. Bars are standard error of the mean. **p < .05

initial response to a threatening stimulus (Campbell et al. 1997). Heart rate deceleration that
occurs through activation of the defensive motivational system is controlled by the parasym-
pathetic nervous system (Campbell et al. 1997). Our results suggest that dysphoric individuals
have a sustained attention response (i.e., heart rate deceleration) when exposed to unpleasant
words, which favors the emergence of attentional bias toward aversive stimuli in depression.
Different studies have shown that the galvanic skin response is an indicator of arousal (Bradley
et al. 2001; Critchley et al. 2000) and a component of the orientation response (Bradley 2009;
Sokolov 1963). We found a higher SCL in response to pleasant words in nondysphoric participants,
indicating a greater orienting response and greater arousal response to these stimuli (Bradley et al.
2001; Maltzman and Boyd 1984; Mathersul et al. 2013). A close relationship has been observed
between arousal and the orientation response. Previous studies reported that the increase in arousal
response to a stimulus generates a greater orientation response (Bradley 2009). Our results suggested
that the appetitive stimuli generated greater arousal and a greater orientation reflex in individuals
without dysphoria. This result corroborates the presence of attentional bias toward pleasant stimuli in
individuals without depression (Epp et al. 2012; Koster et al. 2005; Koster et al. 2010).
Overall, the present results confirm the existence of attentional bias toward unpleasant words
in dysphoria, corroborated by heart rate deceleration (i.e., a physiological correlate of attentional
bias) in response to these words. Additionally, nondysphoric individuals exhibited attentional bias
toward pleasant words and a greater SCL, indicating a greater orientation response.
Int J Ment Health Addiction

The present study has a few limitations. First, the sample consisted exclusively of dysphoric
and nondysphoric individuals. Similar studies should include individuals with major depres-
sive disorder to compare the results. Second, other behavioral tasks (e.g., dot probe task)
should be used to measure attentional bias, or eye-tracker technology could be utilized. The dot
probe task has received support in the literature as a more accurate measure of attentional bias
than the Stroop task (Epp et al. 2012). Third, future studies should perform electroencepha-
lography to objectively measure physiological responses of attention (e.g., event-related
potentials, such as P300) in the central nervous system.

Compliance with Ethical Standards

Conflict of Interest The authors declare that they have no conflict of interest.

Funding Funding for this study was provided by the University of San Buenaventura (Ref. PSI 011-015).Uni-
versity of San Buenaventura, had no role in the study design, collection, analysis or interpretation of the data,
writing the manuscript, or the decision to submit the paper for publication.

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