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Study 3: Brain structures involved in the incidental processing of emotional words

1.5. Individual differences in emotion processing

Emotional processing depends on many aspects including effects of emotional arousal, task demands and participants` intentions, affective and motivational states. Regarding subjective factors, individual differences account for fundamental differences in responsiveness to either unpleasant or pleasant stimuli. People with mood disorders (e.g., anxiety, depression) and high-levels of negative affect show a processing bias toward unpleasant material that is associated with enhanced perceptual vigilance and enhanced neural responses in the amygdala (e.g., Abercrombie, Schaefer, Larson, Oakes, Lindgren et al., Davis & Whalen, 2001 for review;

Sabatinelli et al., 2005). By contrast, there is reason from imaging data to assume that the opposite activation pattern may hold for healthy subjects (e.g., Canli et al., 2001, 2002, 2004) who are characterized by positive affect and a stronger preference for pleasant than unpleasant stimuli.

Extending findings from active to passive viewing conditions, the current fMRI study aimed to elucidate whether the processing of highly arousing unpleasant and pleasant words compared to low arousing neutral words initially enhances attention and perceptual word processing by activating the amygdala. To explore whether pleasant and unpleasant words elicit differential neural responses at similar levels of emotional arousal, words from the two emotional categories were carefully matched for perceived emotional arousal. Methodologically, event-related fMRI was used to study brain activity patterns attributable to differences in initial word recognition between emotional and neutral words. In contrast to blocked stimulus designs indicating tonic changes in hemodynamic brain responses, event-related designs have proven sensitive to detect subtle changes in brain activation associated with stimulus-locked, perceptual processing (e.g., Henson, 2003; Kleinschmidt et al., 1998). To examine whether passive viewing of emotional words had long-term effects on information processing, memory performance was tested by a surprise free recall task, 50 minutes after scanning.

2. Methods 2.1. Participants

Fifteen healthy, right-handed native speakers of German (8 males, 7 females; mean age: 26 years) without history of drug abuse, chronic bodily or neurological and psychiatric diseases or medication for any of these participated in the fMRI experiment. All subjects showed low levels

Personality Questionnaire (Laux, Glanzmann, Schaffner, & Spielberger, 1981) as well as the Beck Depression Inventory (Hautzinger, Bailer, Worall, & Keller, 1994). All subjects had normal or corrected to normal vision. Handedness was determined using the Edinburgh Handedness Inventory (Oldfield, 1971). After being informed about potential risks associated with scanning participants gave written informed consent approved by the Neurological Department of the University of Tübingen Institutional Review Boards. Participant were payed a financial bonus of 15 Euros in return for participation.

Table 1: Mean trait and state anxiety scores and BDI depression scores. Standard deviations are in parentheses. Data was acquired after scanning.

Mean Subjects (n = 15) Trait Anxiety 32.7 (6.1) State Anxiety 34.4 (7.1) BDI Depression 4.7 (3.6)

2.2. Stimulus Material

The experimental stimuli comprised 102 adjectives. Adjectives were taken from a pool of about 500 German adjectives previously rated by 45 student subjects of the University of Konstanz.

Ratings were obtained on the dimensions of perceived arousal and valence using the Self-Assessment Manikin scale (e.g., Lang, 1980; Lang et al., 1997b). Pleasant and unpleasant adjectives described a broad range of affective traits and states (e.g., successful, happy, in love, chilling, brutal, tortured, anxious, nervous, sick, etc.) whereas neutral adjectives described traits and states rated as less arousing and salient (e.g., neutral, normal, civilian, formal, etc.).

Unpleasant and pleasant adjectives as well as neutral adjectives differed significantly in mean valence ratings (F(2,99) = 391.3, p <.001). Pleasant and unpleasant adjectives did not differ significantly in mean arousal but differed significantly from the neutral adjectives on this dimension (F(2,99) = 349.2, p <.001). Table 2 shows mean valence and arousal ratings of the highly arousing and low arousing emotional adjectives, respectively. Additionally, word categories (unpleasant, pleasant and neutral) were controlled for word length (F(2,99) = 3.7, p

>.02), word frequency and concreteness. Concreteness of words was controlled by ratings of 31 student subjects of the University of Konstanz who did not take part in the current study. The

three valence categories did not differ significantly (F(2,99 = 3.0, p >.06). Word frequency was controlled by using frequency counts of the normative CELEX database for written German words (Baayen et al., 1995). Table 3 - 5 shows mean word length, word frequency and mean concreteness values obtained for unpleasant, pleasant and neutral adjectives, respectively. As can be seen in Table 3, unpleasant and pleasant adjectives had lower frequency counts as opposed to neutral adjectives but unpleasant and pleasant adjectives did not differ significantly in word frequency. The higher frequency count for neutral adjectives was primarily due to seven neutral adjectives having extremely high word frequency counts. When these outliers were excluded from statistical comparisons, unpleasant, pleasant and neutral adjectives did not differ in word frequency (word frequency: F(2,99) = 8.3, p <.005*; without outliers: F(2,92) = 2.7, p >.07).

Table 2: SAM mean valence and arousal ratings of pleasant, neutral, and unpleasant adjectives rated by 45 students of the University of Konstanz.

Mean

Valence and Arousal Ratings

Adjectives

Pleasant Neutral Unpleasant

Valence 6.6 (.14) 5.2 (.09) 2.5 (.06)

Arousal 6.0 (.11) 3.0 (.06) 6.1 (.10)

The range and direction of the SAM ratings are as follows: pleasure = 9 (extremely pleasant) to 1 (extremely unpleasant), arousal = 9 (extremely arousing) to 1 (not at all arousing). Standard errors are in parentheses.

Table 3: Frequency counts of written language (MannW) from the standardized word-database CELEX for pleasant, neutral, and unpleasant adjectives.

Mean Word frequency

Adjectives

MannW Pleasant Neutral Unpleasant

without outliers

24.0 (6.2) 95.5 (25.6) 35.2 (7.1)*

16.0 (4.2)

Standard errors are in parentheses. *: Frequency counts after correcting for outliers.

Table 4: Mean word length of pleasant, neutral, and unpleasant adjectives.

Mean Word length

Adjectives

Pleasant Neutral Unpleasant

8.9 (.46) 7.4 (.36) 8.4 (.34)

Standard errors are in parentheses.

Table 5: Mean concreteness of pleasant, neutral, and unpleasant adjectives obtained from ratings of 31 student subjects of the University of Konstanz.

Mean Concreteness Adjectives

Pleasant Neutral Unpleasant

4.7 (.16) 4.6 (.29) 4.0 (.20)

The range and direction of the concreteness ratings are as follows: concreteness = 1 (extremley concrete) to 9 extremely abstract. Standard errors are in parentheses.

2.3. Experimental Design

Adjectives were divided into two sets of experimental stimuli, which were presented in two separate sessions of silent word reading. Each session contained 17 highly arousing pleasant, 17 highly arousing unpleasant and 17 low arousing neutral adjectives. In each session words were presented event-related, in fifty-one randomly assigned trials of unpleasant, pleasant and neutral adjectives. No word occurred twice to avoid habituation effects due to word repetition. Each word was presented for one second and was followed by a baseline trial, consisting of an array of letter strings matched with the mean word length of the adjectives. To improve signal-to-noise ratio, word onset was jittered relative to the scan onset, resulting in variable baseline intervals ranging from 7.5 seconds to 12.75 seconds. Figure 1 displays a schematic overview of the experimental design.

Figure 1: Schematic overview of the experimental design.

Stimulus presentation order was randomized across sessions and session order was counterbalanced over subjects. Experimental stimuli were presented parafoveally on a back-projection screen positioned in the scanner’s head coil. Each session began with a baseline trial of random letter strings presented for 5 seconds to account for scanner drifts. Subjects were instructed to read each word silently.

Experimental runs were generated and controlled by ‘Presentation’ software (Neurobehavioral Systems Inc.).

Fifty minutes after scanning subjects were confronted with a surprise free recall memory test.

Before scanning subjects were not informed about the subsequent memory test so as not to confound activations during silent word reading with cognitive processing related to memory rehearsal. Participants were asked to remember as many of the presented adjectives. In the free recall test adjectives had to be recalled along the three dimension of affective valence (unpleasant, pleasant and neutral words). An example of the free recall task can be found in the appendix section.

2.4. Physiological Data Collection and Reduction