Prefrontal activation through task requirements of emotional induction measured with NIRS

Biological Psychology 64 (2003) 255–263

Prefrontal activation through task requirements of emotional induction measured with NIRS M.J. Herrmann∗ , A.-C. Ehlis, A.J. Fallgatter Psychiatric Neurophysiology, Department of Psychiatry and Psychotherapy, University Hospital Würzburg, Fuechsleinstraße 15, 97080 Wuerzburg, Germany Received 17 June 2002; accepted 1 December 2002

Abstract The medial prefrontal cortex is believed to be involved in emotional experiences, but also in situations in which attention and self-monitoring is required. Therefore, it might be that the medial prefrontal cortex is not only activated by the emotional state per se, but rather through the task requirements that were used to induce emotions in the laboratory. The present study investigated the change of oxygenation in the left and right prefrontal cortex measured with near-infrared spectroscopy (NIRS) from 14 subjects during two kinds of emotional induction, which differed in the self-monitoring requirements. The task with the higher self-monitoring requirements resulted in an increased concentration of oxygenated hemoglobin (O2 HB). This activation pattern was not observed during the emotional induction with the fewer self-monitoring requirements, although the subjective ratings indicated that both tasks induced comparable emotional states. The results indicate that task requirements should be taken into account when investigating the neural substrate of emotions. © 2003 Elsevier B.V. All rights reserved. Keywords: Emotion; Prefrontal cortex; NIRS; Spectroscopy

1. Introduction The investigation of the neural substrate of human emotion has received considerable attention during the past few years. By means of new brain imaging technologies such as positron emission tomography (PET) or functional Magnetic Resonance Imaging (fMRI) it is now possible to relate experimental findings in animals or brain-damaged patients to functioning in the intact human brain. Beside subcortical areas like the amygdala, the prefrontal cortex has been shown to be involved in the regulation of emotions (Davidson ∗

Corresponding author. Tel.: +49-931-201-77440; fax: +49-931-203-77550. E-mail address: [email protected] (M.J. Herrmann).

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and Irwin, 1999). According to the valence hypothesis, the left prefrontal cortex is activated during positive emotions whereas the right prefrontal cortex is activated during negative emotions. Although studies about alpha asymmetry of resting EEG measured over the dorsolateral prefrontal cortex (Davidson, 2002; Schmidt and Trainor, 2001; Waldstein et al., 2000) and fMRI (Canli et al., 1998) support this hypothesis, Lane et al. (1997a,b) reported increased activity in the left medial prefrontal cortex (Brodman Area 9) for both positive and negative emotions measured by PET. As the medial prefrontal region is supposed to be involved in representing and maintaining the attentional demands of a task (MacDonald et al., 2000) or action-monitoring (Luu et al., 2000), the reported activation in the medial prefrontal cortex might be caused by the task requirements that are used to induce emotion. To test this hypothesis, we measured the brain activity of the left and right prefrontal cortex by means of near-infrared spectroscopy (NIRS) during two emotional induction tasks, which differ with regard to their self-monitoring requirements. NIRS is a relatively new, optical method to investigate the oxygenation of brain tissue. In contrast to visible light, light from the near-infrared spectrum (700–1000 nm wave length) can penetrate the skull and is absorbed mainly by two chromophores (oxygenated hemoglobin (O2 HB) and reduced hemoglobin (HHB)) which have different absorption spectra. Therefore, concentrations of O2 HB and HHB in living brain tissue can theoretically be calculated from the amount of absorbed near-infrared light. Generally, activation of the brain leads to an increased oxygen metabolism and to an initial deoxygenation of the tissue. In contrast, NIRS measures show an increase in O2 HB and a corresponding decrease in HHB (Obrig et al., 2000). This phenomenon was also found in a PET investigation where it has been interpreted as a regional perfusion overshoot with a delay of a few seconds induced by an initial decrease in O2 HB caused by the oxygen consumption due to the activation (Fox and Raichle, 1986). It has been shown that NIRS is able to detect even small changes in blood oxygenation caused by cognitive demands (Fallgatter and Strik, 1997, 1998; Fallgatter et al., 1997, 1998, 2000; Herrmann et al., 2003; Herrmann et al., in press, Hoshi and Tamura, 1997; Hoshi et al., 1994; Villringer et al., 1993). The first method we used to induce emotions was the presentation of emotional pictures from the International Affective Picture System (Lang et al., 1995), during which the subjects were instructed only to look at the pictures (task = “picture”). The second method we employed was the presentation of facial expressions with the direct instruction to try to feel like the mood expressed by the person on the picture (task = “face”; Schneider et al., 1994). If the prefrontal activation reported by Lane et al. (1997a,b) was due to the self-monitoring requirements of the task, the task “face” and the task “picture” in our study should differ, with “face” producing a significantly higher cortical activation, indicated by an increase in O2 HB and a corresponding decrease in HHB compared to baseline. 2. Methods 2.1. Subjects Fourteen subjects (seven female and seven male, mean age 31.7 years ± 6.2) participated in the present study after written informed consent was obtained. All subjects were healthy, medication-free and right-handed according to Oldfield (1971).

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2.2. Procedure To manipulate the emotional state of the subjects, two different tasks of emotional induction were performed. One task consisted of pictures of facial affect and the second consisted of pictures of the International Affective Picture System (IAPS). Both tasks were varied in sequence subject-by-subject. After each condition of both tasks the actual emotional state was assessed by using two visual analogue scales, one for the extent of the positive and one for the extent of the negative affect. Each of them ranged from the pole “no positive/negative affect” to the pole “very strong positive/negative affect”. Between these two poles no further formulations or markings were given, and the subjects were instructed to mark the line (100 mm) somewhere according to their current affective state. The difference between the positive and the negative scale was used to describe the emotional state of the subjects after each condition. The beginning of the baseline and the different conditions of the emotional tasks were marked on the NIRO-300 monitor by the investigator. 2.3. Pictures of facial affect The task consisted of 12 pictures with sad, happy and neutral facial affect (four per condition) each displayed by four actors, two females and two males. The pictures were taken from the Pictures of Facial Affect (Ekman and Friesen, 1976; picture names of the neutral facial expression: JJ3-4, JM1-9, PE 2-4, PF1-2; picture names of the sad facial expression: JJ5-5, JM3-11, PE5-7, PF2-16; picture names of the happy facial expression: JJ4-7, JM1-4, PE 2-12, PF1-5). Each picture was presented twice for 7.5 s in a block design, which resulted in a sad, happy and neutral condition each lasting 60 s. The subjects were instructed to look at the pictures and to try to feel like the displayed facial expressions. The task started with a 1-min baseline condition, in which the subjects were instructed to close their eyes and to relax. After this baseline condition the subjects were instructed for the following task condition. The first and third block of the faces’ presentation consisted of the emotional expressions sad or happy, with a randomized sequence. As the second presentation block the neutral facial expressions were displayed. 2.4. Emotional pictures of the IAPS In this task 15 neutral, 15 negative and 15 positive pictures out of the IAPS (Lang et al., 1995) were presented for 6 s each in a block design (coding for negative pictures: 9220, 3350, 9560, 9320, 6370, 9280, 9571, 1300, 9300, 9910, 1120, 9340, 2205, 1930, 2800; coding for neutral pictures: 7002, 7185, 7000, 7060, 7035, 7130, 7050, 7187, 7150, 7040, 7010, 7004, 7006, 7034, 7009; coding for positive pictures: 1610, 2040, 1440, 1920, 5760, 2530, 8080, 1750, 2070, 8190, 5700, 7502, 1460, 1710, 5830). Mean pleasure ratings for the negative, neutral and positive pictures used were 2.5, 4.9 and 8.0, respectively, and mean arousal ratings were 5.6, 2.6, and 4.8 for the negative, neutral and positive pictures, based on the IAPS norms (Lang et al., 1995). After a baseline resting condition, the three emotional conditions were presented. The neutral pictures were always shown as the second block, whereas the emotional pictures were presented as the first and third condition with a varied sequence between subjects. The participants were instructed simply to look at the presented pictures.

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2.5. NIRS We measured the changes of O2 HB and HHB from starting baseline with a NIRO-300 (Hamamatsu, Japan) monitor with two channels. Each channel consisted of a light emitter and detector which were placed 4 cm apart on the scalp of the subjects using a double faced adhesive tape. The light emitter was placed at the EEG position Fp1 for the left side (at Fp2 for the right side) and the light detector was placed between F7 and F3 on the left (between F4 and F8 on the right) according to the international 10-20 system for EEG electrode placement (Jasper, 1958). NIRS measures oxygenation in the cortex area between these two points, corresponding to Brodman Area 10 and Brodman Area 46 in the frontal cortex. The emitter (8 mm diameter) emitted infrared light of 775, 810, 850 and 910 nm wavelength, with an impulse duration of 100 ns and an impulse frequency of 2 kHz. The light detector had a side length of 20 mm. The measurement principles of the NIRO-300 monitor mainly based on the modified Beer–Lambert law, which calculates the O2 HB and HHB concentration changes from the light attenuation change at a given measured point. With a pathlength (i.e. mean distance along which the emitted light travels until it reaches the detection point) of 24 (constant) van der Zee et al., 1992) of adult head = 5.93 × distance between emitter and detector = 4 cm) the concentration changes of O2 HB and HHB are given in the unit ␮m = 10e-6 mol/l. Although the exact size and location of the volume of tissue cannot be precisely defined, it can be assumed that NIRS measures changes in O2 Hb and HHb concentrations in brain tissue inside a volume of several cubic centimeters encompassing predominantly cortical structures and being situated directly under the sensors (Chance, 1991; Gratton et al., 1994; Hock et al., 1995). The sample rate was 2 Hz. The data were online transferred from the NIRO-300 monitor to a PC via the RS232C interface, and further analyzed offline. 2.6. Data analysis and statistics The length of the different task conditions was normalized according to the respective minimal length for the segment over all subjects (face condition: baseline = 113 s, happy = 62 s, sad = 63 s, neutral = 62 s; emotional pictures condition: baseline = 113 s, positive = 94 s, negative = 91 s, neutral = 93 s). The average concentration of O2 HB and HHB for all four segments was calculated for both hemispheres and each subject. For statistical purposes a 2 × 2 × 4 (task × hemisphere × condition) analysis of variance for repeated measurements was calculated for the variables “O2 HB”, “HHB” and “emotional state” for both tasks. When necessary, Greenhouse-Geisser correction was applied to the degrees of freedom. Post-hoc analyses were calculated using 2 × 4 ANOVAs with the factors “hemisphere” and “condition”.

3. Results 3.1. Emotional induction The induced emotional states did not differ between both tasks (Ftask (1,13) = 0.46, n.s) but differed significantly between conditions (Fcondition (1.8,23.9) = 26.0, P < 0.0001;

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Ftask × condition (1.7,22.5) = 1.35, n.s). Post-hoc ANOVAs indicated that the subjective emotional state after the different task conditions differed significantly both in the “face” task (F(3,39) = 21.4, P < 0.0001) and in the “emotional pictures” task (F(1.8,24.7) = 15.2, P < 0.0001). In the emotional pictures task, the subjects rated their emotional state after the positive condition (m = 57.5 ± 25.3) as more positive than after the neutral (m = 45.7 ± 20.5; t(13) = 2.90, P < 0.05) and after the negative condition (m = 13.1 ± 32.8; t(13) = 4.44, P < 0.001), and after the neutral condition as more positive than after the negative condition (t(13) = 4.09, P < 0.001). The rating after the baseline condition (m = 58.9 ± 23.5) was significantly higher and, therefore, more positive than after the negative condition (t(13) = 4.72, P < 0.001). Similar results were obtained for the “face” task. The subjects rated their emotional state after the positive condition (m = 58.3 ± 23.9) as more positive than after the neutral (m = 37.0 ± 25.6; t(13) = 3.73, P < 0.01) and after the negative condition (m = 17.8 ± 33.7; t(13) = 6.14, P < 0.0001), and after the neutral condition as more positive than after the negative condition (t(13) = 3.51, P < 0.01). The rating after the baseline condition (m = 51.1 ± 29.3) was significantly more positive than after the negative condition (t(13)=7.02, P < 0.001) and after the neutral condition (t(13) = 2.46, P < 0.05).

Table 1 Mean and standard deviation of left and right hemispherical O2 HB and HHB concentration [␮M] for the “emotional pictures” and the “facial expression” tasks and F values of the ANOVAs with H, main effect hemisphere; C, main effect condition and H × C, interaction effect hemisphere × condition Condition

Left (m ± S.D.)

Right (m ± S.D.)

Facial expressions (F-values) O2 HB Baseline Negative Neutral Positive HHB Baseline Negative Neutral Positive

0.13 ± 0.81 1.13 ± 1.25* 0.92 ± 1.41* 1.01 ± 1.38* 0.00 ± 0.24 0.00 ± 0.66 −0.03 ± 0.59 0.00 ± 0.57

0.30 ± 0.80 0.85 ± 1.08 0.80 ± 1.51 0.76 ± 1.38 −0.11 ± 0.33 −0.12 ± 0.75 −0.22 ± 0.75 −0.15 ± 0.69

Emotional pictures O2 HB Baseline Negative Neutral Positive HHB Baseline Negative Neutral Positive

−0.18 ± 0.63 0.34 ± 0.96* 0.31 ± 0.84* 0.13 ± 1.06 0.07 ± 0.24 0.25 ± 0.43 0.20 ± 0.38 0.22 ± 0.34

−0.24 ± 0.53 0.07 ± 0.86 0.19 ± 0.87 −0.15 ± 0.89 0.02 ± 0.20 0.19 ± 0.45 0.12 ± 0.44 0.20 ± 0.49

2 × 4 ANOVA H

C

H×C

0.45

3.68*

2.79+

2.77

0.14

0.92

0.51

2.19

0.69

0.47

1.49

0.46

The levels of significance for the ANOVA and for the comparison “task conditions vs. baseline” are indicated with *P < 0.05, +P < 0.10.

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3.2. NIRS data The 2 × 2 × 4 ANOVA for the O2 HB concentration revealed significant main effects of the factors “task” (F(1,13) = 5.07, P < 0.05) and “condition” (F(1.8,23.5) = 5.77, P < 0.05). For the variable “HHB concentration” no significant main effects or interactions were observed. To further analyze the main effect “condition” a 2 × 4 (two hemispheres, four task conditions) ANOVA for repeated measurements for the variable “O2 HB concentration” was conducted for both tasks separately. Only for the face task a significant main effect of the factor “condition” was observed (face: F(1.7,22.5) = 3.68, P < 0.05; pictures: F(3,39) = 2.19, n.s.). The condition × hemisphere interaction for the face task was only marginally significant (F(1.7,22.2) = 2.78, P < 0.10). Subsequently conducted posthoc tests revealed that mean O2 HB concentration in each of the three “face” conditions was significantly increased when compared with the pretask baseline level, but only for the left hemisphere. No differences were observed between the three “face” conditions (Table 1). To analyze the main effect “task”, a 2 × 2 ANOVA (hemisphere × task) was calculated for baseline and each of the three conditions of both tasks. For the negative condition (Ftask (1,13) = 5.24, P < 0.05) and as a trend for the positive condition (Ftask (1,13) = 4.37, P < 0.10), but not for baseline (Ftask (1,13) = 2.63, n.s.) nor for the neutral condition (Ftask (1,13) = 2.25, n.s.), significant main effects of the factor “task” were found, indicating higher O2 HB concentrations for the emotional facial expressions compared with the corresponding emotional conditions in the picture task.

4. Discussion The results indicate that it is feasible to induce different emotional states by the use of the two tasks of emotional induction. As expected, the subjects reported a more positive mood after the positive conditions of both tasks than after the negative and neutral conditions, with their emotional state being most negative after the negative task conditions. Overall, both tasks of emotional induction, i.e. the one using facial expressions and the one using emotional pictures, were equally suited to induce positive and negative emotional states. The main effects of the factors “task” and “condition” for the O2 HB concentration indicate that both tasks differed in their influence on frontal blood oxygenation. While there was no significant main effect of condition in the emotional pictures task (and hence no reliable/consistent effect of the different emotional conditions on cerebral blood oxygenation in this task), all conditions of the facial expression task evoked a significant increase in left-hemispheric O2 HB when compared to pre-task baseline. This increase during the emotional faces task lead to significantly higher O2 HB concentrations during the sad and happy facial expression condition when compared to the corresponding negative and positive condition in the emotional pictures task, whereas both tasks did not differ significantly in the baseline and the neutral condition. Altogether, the emotional faces task seems to have had a markedly stronger influence on frontal O2 HB concentration (it lead to more pronounced

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task-induced changes in blood oxygenation) than the emotional pictures task. Since both tasks most notably differ with regard to their self-monitoring requirements, these might indeed—as assumed in the study’s hypothesis-have contributed to the observed differences in the effects of both tasks. Nevertheless, the emotional pictures task also had some influence on frontal blood oxygenation, that resulted in significantly higher O2 HB concentrations in the neutral and the negative task condition when compared with pre-task baseline (Table 1), but that was not strong enough to lead to a significant main effect of the factor “condition” in this task. Thus, the emotional pictures task lead to an increase in frontal oxygenation— a finding also reported by Canli et al. (1998)—but this change did not reach significance and was much less pronounced than the change induced by the emotional faces task that additionally includes some sort of self-monitoring component. As the subjective data of emotional state after baseline and task conditions between the two tasks were on a comparable level, differences between the two tasks regarding their influence on frontal O2 HB might indeed be caused by the suggested differences in task requirements. As we did not measure hemodynamics, especially sympathetic activation, one may argue that the increased O2 HB concentrations might be the consequence of a changed cardiac output caused by the emotional tasks. This argument was not supported by the subjective data, as the self-reports did not indicate any differences in emotional experiences between the both investigated emotional tasks, other than the O2 HB concentrations. It should be mentioned that the effect of an increased O2 HB concentration measured in this study must be seen as a compensatory mechanism of the brain tissue after an initial deoxygenation caused by the task (Fox and Raichle, 1986), which was also described as an “initial dip” in fMRI studies. The present findings indicate that self-monitoring processes involved in certain tasks of emotional induction might contribute to frontal activation observed with various methods. As we found that the oxygenation concentration, discussed as the hemodynamic response caused by regional brain activation, was significantly higher in the face task than in the pictures task although both tasks similarly induced different emotional states, it can be assumed that task-requirements can affect the amount of frontal brain activation and should be further analyzed. The fact that we did not observe any hemispheric differences related to the kind of emotion induced (positive vs. negative) might have its cause in the localization of the sensors in our study, which were clearly located more dorsally than in studies describing hemispheric differences. The missing significant change in HHB might be caused by the fact that the effects of HHB are often smaller than in O2 HB. Therefore, it might be that due to the small sample size the statistical power was too weak to lead to significant differences in HHB. The present study aimed at comparing the effects of two tasks of emotional induction— one implying a self-monitoring component and one inducing different emotional states only. Both tasks were suited to evoke different emotional states (subjective report), whereas only the task that additionally required self-monitoring processes resulted in a significant frontal activation as assessed by NIRS. Therefore, the specific task requirements, especially the self-monitoring component, must be taken into account when the neural substrate of emotions is under investigation.

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