Abstract

To investigate the influence of stimulus duration on emotional processing, we measured changes of regional cerebral blood flow (rCBF) in 14 healthy subjects who viewed neutral or emotional images presented for 3 or 6 s. Presentation for 3 s reproduced the previous result of higher rCBF in inferior medial prefrontal cortex (IMPC) during neutral than emotional stimulation. Six-second presentation reverted this relationship, with activity in IMPC being higher during emotional stimulation. Prolonged stimulus presentation attenuated the rise of rCBF associated with emotions in left parietal cortex and cerebellar hemisphere. We speculate that the different rCBF during neutral and emotional stimulation for 6 s is a consequence of attention divided between the emotional stimuli and their associations. Thus, prefrontal activity rises when a cognitive task accompanies emotional stimulation because several cognitive processes compete for attention. The IMPC may serve the mechanism of attention underlying the concept of a default mode of brain function, selecting among competitive inputs from multiple brain regions rather than just processing emotions. The results emphasize the importance of implicit cognitive processing during emotional activation, however, unintended.

Introduction

Since Harlow's (1848, 1868) description of the damage inflicted on Phineas Gage's brain and the profound consequences for his social behavior, the importance of inferior medial prefrontal cortex (IMPC) has been well recognized (Bechara et al. 2000). However, the exact function of this region is far from firmly established. Bechara et al. (2000) claimed that this region is critical to the integration of emotion and cognition by somatic markers. Rolls (1990, 2000a), on the other hand, focused on the region's role in emotionally related learning and suggested that the main function of IMPC is to represent the magnitude of reward or punishment. IMPC is the brain area most frequently activated in brain-mapping studies of responses to emotional stimuli (Phan et al. 2002; Amodio and Frith 2006). The majority of the studies report increased regional cerebral blood flow (rCBF) in this region during the processing of emotions (Damasio 1994; Lane et al. 1997a, 1997b; Reiman et al. 1997; Rolls 2000b; Iidaka et al. 2001). Two studies show that processing of emotional visual stimuli lowers rCBF in the IMPC compared with neutral stimuli (Paradiso et al. 1999; Geday et al. 2003). The common denominators in these studies include a stimulus duration of 3 s or less and the absence of an explicit task during the stimulus presentation.

Studies of longer stimulus presentations yield different results. During a 6-s presentation of affective images, blink inhibition wanes after 3 s (Bradley et al. 1993). Codispoti et al. (2001) showed that startle reflex potentiation by briefly (500 ms) displayed aversive pictures reaches the maximum in 3 s. Pöppel (1997, 2004) concluded that attention to a stimulus allows entry of stimulus-related information for no more than 2–3 s. When presentation of the same image persists, associations begin to compete for access to consciousness. Pöppel claims that an endogenously generated question, “what is new?,” arises every second to third second. To be consistent with Pöppel's conclusion, any stimulus presentation that exceeds 3 s necessarily involves the implicit alternative cognitive tasks of interpretation and association evoked by the stimulus. During prolonged presentation of an emotional stimulus, the subject divides attention among the emotions evoked by the stimulus and their secondary cognitive associations. In the postulation of a default mode of brain function, Raichle et al. (2001) propose that the major task of the IMPC is to maintain attention and facilitate the entry into consciousness of salient inputs from other brain areas (Drevets and Raichle 1998; Simpson et al. 2001a, 2001b). According to this theory, divided attention is linked to higher activity in the IMPC than undivided attention. Consistent with the theory, in a study of divided versus sustained attention in patients with Alzheimer's disease, Johannsen et al. (1999) found that activity declined in the IMPC during sustained successful attention to a single task whereas no decline was observed when attention was divided between 2 tasks. In the subsequent study of 3-s emotional stimulation, Geday et al. (2003) speculated that IMPC deactivation during short emotional stimulus presentation reflects involvement of IMPC in attentional processing rather than the processing of the emotional stimulus itself.

To test the hypothesis that stimulus duration is a crucial factor in IMPC activation during emotional stimulation, functional positron emission tomography (PET) scans were completed in 14 normal healthy controls who viewed neutral and emotional images. We adopted the experimental procedures previously reported in detail (Geday et al. 2001, 2003) but extended the stimulus duration from 3 to 6 s in half of the tomography sessions. We specifically predicted that the extension of the stimulus duration would revert the deactivation of the IMPC elicited by the short duration. Regions of interest (ROIs) were right IMPC, and right inferior temporal and left occipitotemporal cortices, all significantly activated or deactivated in a previous study (Geday et al. 2003).

Material and Methods

Participants

Fourteen healthy subjects (7 men and 7 women, mean age 43.7 years, standard deviation [SD] 12.5 years) gave written informed consent to the study approved by the regional science ethics committee in Aarhus County, Denmark. All subjects were unmedicated and without known psychiatric or neurological illness. Two subjects (1 man and 1 woman) were excluded from the final PET analysis, due to an urgent need to micturate during the scanning.

Visual Stimuli

We used the standard empathy picture system (EPS), which was developed in our laboratory (Geday et al. 2001, 2003, 2006). The EPS consists of 12 independent series of images, each containing 30 images of real-life persons placed in real-life events. The images were originally selected from international newspaper and private photo. Six series show mainly faces, and the 6 remaining series show scenes. The series of images were further subdivided according to emotional valence (positive, negative, or neutral). We defined a low-complexity image as a picture in which the emotional valence is predominately dictated by the overt facial expression and not by the situation in the image. A high-complexity stimulus was defined as the opposite, that is, a picture in which the emotional valence is predominately dictated by the social situation and not by the overt facial expressions of the people in the image. Great care was taken to match the complexity of the images to the 3 emotional valence categories; that is, numbers of persons depicted were the same across series. No person appeared more than once. As the number of persons per image naturally is higher in scenes than in presentations of faces, the former tend to be more complex. All scenes are third-person perspectives of which the observers are never part. No image has an erotic content or implies a direct threat or reward to the observer. Originally, a panel of 10 healthy controls verified the classification, and an image was only included in the EPS if all 10 agreed on the level of complexity and emotional valence. The pleasant or unpleasant series show more than 1 positive/negative emotion. For faces, the negative expressions may be categorized as sadness or despair and the positive as joy or happiness. For the neutral valence, neutral facial expressions were shown. The scenes show situations that may be conceived as disgusting, horrible, neutral, pleasant, or happy. Examples from the EPS are available on http://www.geday.net/EPS—for further information about validation of the EPS, see Geday et al. (2006) and Supplementary Material.

Procedure

During PET tomography, 12 series of images were presented in randomized order. The images were presented one at a time on a 21-inch color monitor placed 70 cm from the subjects' eyes. Half of the images were shown for 3 s and the other half for 6 s. There was no intermission between images in any series. The series were matched so that the 12 subjects included in the PET analysis as a group viewed the same images during the 3-s presentation as during the 6-s presentation. One EPS series was presented during each 3-s scan and half a series (intermittently the first and the last) during the 6-s presentation. Thus, each subject in total saw 180 images presented for 3 s and 90 images presented for 6 s. Subjects were told to view the images but were not further instructed prior to the scanning sessions. Immediately after each scan, the subjects were asked “how they felt about the pictures they had just seen.” All stimuli were completely novel to the subjects as results from a previous study (Geday et al. 2002) indicated that prior knowledge might interact with emotional content by raising cerebral blood flow in the IMPC. After the whole PET investigation, the subjects were shown the pictures again and they had to evaluate each of the images on a scale from −3 to 3 with −3 as most unpleasant, 0 as neutral, and 3 as most pleasant. Notations of 1 and −1 refer to the value “a little,” 2 and −2 to “rather,” and 3 and −3 to “more.”

PET Data Acquisition and Analysis

The rCBF was measured with an ECAT Exact HR47 PET camera (Siemens/CTI, Knoxville, TN) in 3-dimensional mode following fast bolus injections of 500 MBq of H215O into the left antecubital vein. A single 60-s frame was acquired, starting at 60 000 true counts/s. Successive scans were separated by at least 10-min intervals. Visual stimuli were presented throughout the entire scanning window. Subjects were scanned in 12 different experimental conditions (see above). PET images were reconstructed after correction for scatter (Watson et al. 1996) and measured attenuation correction. Forty-seven 3.1-mm thick slices were filtered to 12 mm full width half maximum isotropic (Hanning filter cutoff frequency = 0.15 cycles/s). PET images were realigned using Automatic Image Registration software to correct for head movements between scans (Woods et al. 1992). For anatomical localization of activation sites, T1-weighted magnetic resonance imaging (MRI) was performed on a GE Sigma 1-T scanner providing slices of 1.5-mm thickness. The first PET image was coregistered to each individual's MRI. PET and MRI data were mapped into standardized stereotaxic space (Talairach and Tournoux 1988), using a 9-parameter affine transformation. After a pixel-by-pixel regression of PET volumes using the local voxel SD, t-statistical maps were calculated. The rCBF measured during the emotional (pleasant and unpleasant) picture series was regressed on a voxel-by-voxel basis against rCBF measured during the neutral pictures. The same was done for timing, where rCBF measured during the 6-s picture presentation was regressed against rCBF measured during the 3-s picture presentation. Corrected P values for local maxima were calculated according to the method described by Worsley et al. (1996) for image volumes with a nonuniform SD. It should be noted that the t-threshold values for significance differ with search volume and the number of degrees of freedom according to the number of scans and regressors used in each analysis.

Two separate analyses were completed. ROIs were identified in the right IMPC and inferior temporal and occipital cortices as significant areas of activations and deactivations in a previous study (Geday et al. 2003), that is, right middle frontal gyrus with maximum at 15, 49, −9 mm; right fusiform gyrus at 42, −72, −9 mm; and left inferior temporal gyrus at −42, −75, and −2 mm. In addition, we performed a global search for sites of significant change in the entire brain gray matter.

To rule out that stimulus complexity represents an unaccounted confound, we finally performed an interaction analyses between emotional content and complexity (face or situation) for 3 and 6 s separately and similar separate interaction analyses between emotional content and presentation time for low (faces) and high complexity (situations). This was done as a ROI analysis as well as a global search analysis.

Results

Behavioral Data

When informally asked how they felt about the EPS series after each scan, all 14 subjects for all 12 picture series confirmed the a priori classification of emotional valence (pleasant, unpleasant, and neutral). Half of the subjects spontaneously reported that prolonged compared with short presentation made them feel different during the stimulation, although it was inconsistent whether prolonged presentation made the elicited emotions more or less intense.

The individual rating of each image after the PET study confirmed the high agreement in terms of grouping (Table 1), unpleasant (scores < −1), pleasant (scores > 1), and neutral (−1 ≤ scores ≤ 1). When comparing the scoring of images displayed for 3 s with the images displayed for 6 s, we found no significant differences between the 2 groups or between each of the 2 groups and earlier scores from 34 normal healthy controls (2-way analysis of variance).

Table 1

Emotional scores from 14 healthy subjects

Valence Images to be displayed for 3 s Images to be displayed for 6 s 
 Neutral Pleasant Unpleasant Neutral Pleasant Unpleasant 
    Mean 0.09 1.08 −1.21 0.41 1.02 −1.62 
    SD 0.47 0.51 0.53 0.35 0.48 0.60 
Average 34 controls 0.32 1.12 −1.62 0.32 1.12 −1.62 
Valence Images to be displayed for 3 s Images to be displayed for 6 s 
 Neutral Pleasant Unpleasant Neutral Pleasant Unpleasant 
    Mean 0.09 1.08 −1.21 0.41 1.02 −1.62 
    SD 0.47 0.51 0.53 0.35 0.48 0.60 
Average 34 controls 0.32 1.12 −1.62 0.32 1.12 −1.62 

Note. 2-way analysis of variance; valence as source of variation (neutral, pleasant, and unpleasant) P < 0.0001, grouping (3 or 6 s) P = 0.6453.

PET Data

The ROI analysis of blood flow change revealed a significant interaction between emotions and stimulus duration in the right IMPC (Fig. 1, Table 3). Compared with neutral, images with emotional content (positive and negative emotions collapsed) raised the rCBF when displayed for 6 s but lowered the rCBF when displayed for only 3 s (Table 2). The ROI analysis of the 3-s exposure confirmed the deactivation of the right IMPC elicited by emotional content of the images (Fig. 2, Table 2) in the same place as previously reported (Geday et al. 2003), now with significance at P < 0.01 (corrected for multiple comparisons). In the 6-s exposure, the response switched to activation, and analysis at the coordinates of maximal interaction in the ROI revealed that longer exposure to the stimuli raised rCBF in IMPC for the emotional images (positive and negative alike), whereas rCBF for the neutral images was lowered by extending stimulus exposure from 3 to 6 s (Fig. 3). Emotional content in general significantly activated occipitotemporal ROIs bilaterally, regardless of stimulus duration. When comparing unpleasant and neutral stimuli, both occipitotemporal ROIs were significantly activated by images displayed for 3 s alone (Table 2).

Table 2

Main effect of emotional content

Anatomical region BA Talairach coordinates Emotional − neutral 
  x y z 3 s 6 s Both 
     t P t P t P 
Global search           
    Left inferior occipital gyrus 18 −38 −85 4.40 NS 2.55 NS 5.02 0.01 
ROI analysis           
    Right middle frontal gyrus 11 15 47 −15 −4.16 0.01 1.38 NS −1.35 NS 
    Right middle occipital gyrusa 19 47 −72 −8 4.24 0.05 2.23 NS 4.64 0.01b,c 
    Left inferior occipital gyrus 18 −38 −85 4.40 0.01 2.55 NS 5.02 0.001 
    Left inferior temporal gyrusa 19 −45 −76 3.21 NS 2.31 NS 4.24 0.01b 
    Left inferior occipital gyrusa 18 −43 −76 4.44 0.01 1.48 NS 4.01 0.02b 
Anatomical region BA Talairach coordinates Emotional − neutral 
  x y z 3 s 6 s Both 
     t P t P t P 
Global search           
    Left inferior occipital gyrus 18 −38 −85 4.40 NS 2.55 NS 5.02 0.01 
ROI analysis           
    Right middle frontal gyrus 11 15 47 −15 −4.16 0.01 1.38 NS −1.35 NS 
    Right middle occipital gyrusa 19 47 −72 −8 4.24 0.05 2.23 NS 4.64 0.01b,c 
    Left inferior occipital gyrus 18 −38 −85 4.40 0.01 2.55 NS 5.02 0.001 
    Left inferior temporal gyrusa 19 −45 −76 3.21 NS 2.31 NS 4.24 0.01b 
    Left inferior occipital gyrusa 18 −43 −76 4.44 0.01 1.48 NS 4.01 0.02b 

Note. NS, not significant.

a

Unpleasant versus neutral for all calculations.

b

Significant also at P <0.05 for all emotional versus neutral.

c

Subthreshold, t > 4.84 for P <0.05 in global search.

Table 3

Interaction between emotional content and stimulus duration

Anatomical region BA Talairach coordinates (emo − neu)6 s−(emo − neu)3 s 
  x y z t P 
Global search       
    Left cerebellum — −11 −81 −23 −5 0.02 
    Left superior parietal lobule −28 −57 44 −4.53 NSa 
ROI analysis       
    Right middle frontal gyrus (IMPC) 11 14 45 −17 0.01 
Anatomical region BA Talairach coordinates (emo − neu)6 s−(emo − neu)3 s 
  x y z t P 
Global search       
    Left cerebellum — −11 −81 −23 −5 0.02 
    Left superior parietal lobule −28 −57 44 −4.53 NSa 
ROI analysis       
    Right middle frontal gyrus (IMPC) 11 14 45 −17 0.01 

Note. NS, not significant.

a

Subthreshold, t < −4.59 for P <0.05 in global search.

Figure 1.

Altering image duration from 3 to 6 s significantly interacted with emotional activation of the IMPC, changing the significant deactivation of the area found during 3 s to activation.

Figure 1.

Altering image duration from 3 to 6 s significantly interacted with emotional activation of the IMPC, changing the significant deactivation of the area found during 3 s to activation.

Figure 2.

When images were displayed for 3 s, emotional content decreased rCBF in the IMPC at the right middle frontal gyrus compared with neutral.

Figure 2.

When images were displayed for 3 s, emotional content decreased rCBF in the IMPC at the right middle frontal gyrus compared with neutral.

Figure 3.

At coordinates of maximum interaction in the ROI changing stimulus duration from 3 to 6 s for emotional images increased rCBF in IMPC (P value [2 tailed] = 0.0242), whereas extended exposure for the neutral stimuli decreased rCBF (P value [2 tailed] = 0.0015). Stratifying for emotional content versus neutral, rCBF falls, when images are displayed for 3 s (P value [2 tailed] = 0.0021) and rises for 6 s (P value [2 tailed] = 0.0236).

Figure 3.

At coordinates of maximum interaction in the ROI changing stimulus duration from 3 to 6 s for emotional images increased rCBF in IMPC (P value [2 tailed] = 0.0242), whereas extended exposure for the neutral stimuli decreased rCBF (P value [2 tailed] = 0.0015). Stratifying for emotional content versus neutral, rCBF falls, when images are displayed for 3 s (P value [2 tailed] = 0.0021) and rises for 6 s (P value [2 tailed] = 0.0236).

In global search of significantly altered activity in any voxel of the image volume, the general effect of emotional content was a significant increase of rCBF in the middle occipital gyrus (Fig. 4) in the same place as previously observed (Geday et al. 2003). Longer exposures interacted with emotional processing by attenuating the emotionally induced rise of rCBF in the left cerebellum (Fig. 5) and nearly significantly (P < 0.06) reducing the rCBF in the left parietal cortex.

Figure 4.

Compared with neutral images, regardless of stimulus duration, emotional content increased rCBF in the left inferior occipital gyrus.

Figure 4.

Compared with neutral images, regardless of stimulus duration, emotional content increased rCBF in the left inferior occipital gyrus.

Figure 5.

Emotion-induced activation in the left cerebellar hemisphere was significantly reduced when image duration went up from 3 to 6 s.

Figure 5.

Emotion-induced activation in the left cerebellar hemisphere was significantly reduced when image duration went up from 3 to 6 s.

The separate interaction analyses revealed in the ROI analysis no interaction between complexity and emotional content in the IMPC. In global search, we found for presentation time 6 s a significant interaction (t = 5.03, P < 0.05) between emotional content and complexity in left medial frontal gyrus (Brodmann area [BA] 8, Talairach coordinates: −16, 29, 43), where emotional content raised rCBF during more complex stimuli. No significant interactions were found elsewhere in any of the analyses.

Discussion

Physiological studies indicate that 3 s may represent a threshold of primary processing of an emotional visual stimulus. As examples, startle response, skin conductance, and heart rate peak at 3–4 s after presentation of an emotional stimulus (Bradley et al. 1993; Codispodi et al. 2001). Psychologically, 3 s is a reasonable threshold because Pöppel (1997, 2004) argues that multiple cognitive processes of interpretation and association compete when a stimulus is presented for more than 3 s. It is a consequence of this claim that long exposures must resemble situations in which subjects perform 2 tasks in parallel because the subject must be aware of the emotional input and at the same time pay attention to the associations evoked by an emotional stimulus. Conversely, neutral stimuli evoke associations in the absence of (strong) emotions. Thus, attention is divided during emotional but not neutral stimulation.

In this interpretation, neuronal activity (reflected in rCBF) is higher during prolonged presentation of a neutral stimulus than an emotional stimulus in brain areas mediating attention.

Prefrontal Cortex

According to the theory of default brain function, IMPC maintain attention and facilitate the entry into consciousness of salient inputs from other brain areas (Drevets and Raichle 1998; Raichle et al. 2001; Simpson et al. 2001a, 2001b). It is not clear whether this activity is the work of selection among competing inputs or whether it reflects a process of outcome monitoring, as recently hypothesized by Amodio and Frith (2006), or whether these descriptions of the activity in fact are conceptually distinct. If the IMPC is a primary center of attention, the influence of length of exposure explains the decrease of rCBF in this region reported by Paradiso et al. (1999) and Geday et al. (2003), whose stimuli lasted for 3 s or less, and may also explain the relative increase found with longer stimulus presentations or with explicit parallel tasks. The latter design has led to findings of increased rCBF in the IMPC when images are displayed for longer than 3 s (e.g., 5, 6, or 12 s) or are separated by a delay between successive stimuli that brings the total exposure to more than 3 s (Lane et al. 1997b; Lang et al. 1998; Blair et al. 1999; Taylor et al. 2000).

Consistent with this hypothesis, in the present study, we first reproduced the previous finding of emotionally linked deactivation of the IMPC during the 3-s presentation of a visual stimulus (Geday et al. 2003). Second, when we compared respective rCBF measures during presentation of emotional stimuli and neutral stimuli, extension of exposure from 3 to 6 s reverted the deactivation of the IMPC to an activation. During emotional stimulation, the rCBF was higher (albeit not significantly so) during the 6-s than during the 3-s presentation, whereas the rCBF during the neutral stimulation was significantly lower for the 6-s presentation than for the 3-s presentation.

This interaction between presentation time and emotional content in the IMPC was not influenced by stimulus complexity, but separate interaction analyses revealed in global search a significant interaction between emotion and complexity in the left medial frontal gyrus (BA8) for the 6-s presentation time. Gusnard et al. (2001) reported a similar activation when she compared internally cued conditions with externally cued conditions. We suggest that the higher blood flow caused by emotional content of the complex images presented for 6 s may reflect sufficient time for more detailed viewing of the emotional contents of the images.

We do not rule out the possibility that the reversal of activity in the IMPC could reflect variable activation by emotions in the entire 6-s period, but the finding of predicted rCBF change linked to neutral images and Taylor's (2003) observation of reversal of activity by a simultaneously executed explicit cognitive task make this possibility less plausible.

Occipitotemporal Cortices

Activity in occipitotemporal cortices followed emotional valence, as in previous neuroimaging studies (Dolan et al. 1996; Lane et al. 1997b; Paradiso et al. 1999; Halgren et al. 2000; Iidaka et al. 2001; Vuilleumier et al. 2001; Geday et al. 2003), which reported significant bilateral rCBF increase in the occipitotemporal cortex for unpleasant pictures compared with neutral. The stereotaxic coordinates of the right occipitotemporal activation (x = 48; y = −68; z = −4) match our previously reported activation (x = 47; y = −72; z = −8) (Geday et al. 2003) as well as that of Paradiso et al. (1999). At variance with our previous observation of a unilateral increase, the present bilateral increase matches that of Lane et al. (1997b). The testing of both men and women in the present study may explain the difference as women are known to engage both hemispheres in emotional activation (defined as the difference in rCBF during neutral and emotional stimulation), unlike males who activate primarily right-sided structures (Bremner et al. 2001; Wager et al. 2003; Hall et al. 2004).

Activations in the occipitotemporal areas (BA 18, 19) were more significant after 3 than 6 s. The variation implies that emotional processing in the ventral temporal stream begins shortly after the onset of a stimulus. In support of this interpretation, magnetoencephalography and electroencephalography records of event-related potentials in temporal cortex begin as early as 100–200 ms after stimulus onset (Eimer and Holmes 2002; Eger et al. 2003; Esslen et al. 2004).

Cerebellum

Cerebellum is frequently activated by emotions and more so in women than in men (Hall et al. 2004), who view images with emotional content (Lane et al. 1997a; Paradiso et al. 1999; Beauregard et al. 2001; Davis and Whalen 2001). The activation may arise from the direct connections between cerebellum and areas of the limbic system (Anand et al. 1959; Heath et al. 1978). Numerous animal and human lesion studies prove the involvement of cerebellum in associative learning of specific aversive reactions, for example, in eye blink conditioning (Yeo and Hesslow 1998). In humans, the left cerebellar hemisphere and vermis appear to be involved in fear-conditioned potentiation of the startle response, a form of associative learning of nonspecific aversive reactions (Frings et al. 2002). Startle at the onset of every new presentation of an emotionally loaded image may explain the higher rCBF in cerebellum. Thus, in 3-s scans, subjects confront twice as many stimuli as in 6-s scans and hence are likely to startle twice as often.

Superior Parietal Cortex

Regions close to the precuneus (BA 7) generally undergo activation during recall of unpleasant emotion (Lanius et al. 2003). We suggest that the higher rCBF after 3-s exposure to emotions reflects the confrontation of subjects with twice as many unpleasant images.

Limitations

The block design of the 15-O-water PET methodology is an intrinsic limitation. During PET runs with the 6-s presentation, subjects inevitably viewed only half of the stimuli presented in the 3-s runs. This difference per se may affect brain activity as habituation to emotional stimuli is higher during 3-s than during 6-s runs. This limitation is likely to be of minor importance as the predicted increase happened during the neutral stimulation as well as the emotional stimulation. In theory, event-related tomography would be preferable to address this limitation, but at present is possible only with functional magnetic resonance imaging (fMRI).

For the choice between PET and fMRI, it is a potential limitation that the 2 tomography environments are very different. In PET, the subjects reside in a short and open ring, the tomograph is almost soundless, the stimuli are presented on a large, high-resolution monitor, and subjects are not distracted by irrelevant sensory input during the tomography. In contrast, during fMRI subjects reside in a long narrow tube, the scanner is noisy, stimuli are typically presented in a small mirror or displayed in special goggles with limited resolution, and subjects may experience peripheral nerve stimulation during the scanning. Thus, fMRI has certain potential distractors and stressors that are not present in PET. For these reasons, we decided that fMRI would be less suitable to the experimental issues addressed here. For 2 subjects excluded from further analysis in the present study, because of an urge to micturate, the distraction inhibited or even reverted the temporal activation pattern observed in the IMPC. Results of fMRI further are susceptible to artifacts from air in nasal sinuses, resulting in signal loss in the inferior frontal cortex.

The present study tested the extent to which a change of stimulus duration would affect rCBF in the absence of a competing task. Therefore, subjects viewed the images presented without instructions or explanations. Likewise, between scans, we asked subjects only to confirm the image category rather than to assess image strength quantitatively as the latter request inevitably would influence the perception of the next image. Therefore, we have no formal, quantitative evidence of subjects' actual experiences during the tomography, but we do know that they paid attention to the images displayed. After each session, all subjects confirmed the prior classification into “pleasant,” “neutral,” or “unpleasant.”

The study design did not allow firm distinction between perception and experience of emotions, called emotions and feelings, respectively, by LeDoux (1996). Physiological responses are useful as objective measures of emotional experience (Hare et al. 1970) but are prone to habituation (Angela and Barry 1980) and therefore not suitable to a block design such as the present, where briefly presented stimuli of the same valence follow each other. We have therefore only the subject's own ratings after the tomography sessions of the feelings aroused by the images to indicate that the images did elicit an emotional experience. Previous studies of physiological responses to visual stimuli from the International Affective Pictures System (IAPS) (Lang 1995) or Pictures of Facial Affect by Ekman and Friesen (Ekman et al. 1983) (conceptually identical to the EPS used in the present study) demonstrated such responses, so we assume EPS images carry the same impact.

Conclusion

The results of the present study show that stimulus duration is an important and frequently overlooked factor in studies of emotional processing. In agreement with the explanations offered by Pöppel (1997, 2004), we propose that any stimulus presented for more than 3 s generates secondary associative cognitive processes that divide the attention during emotional but not during neutral stimulation. The rCBF to brain areas devoted to attention is therefore higher during prolonged presentation of a neutral stimulus compared with prolonged presentation of an emotional stimulus. According to the theory of a default mode of brain function (Raichle et al. 2001), IMPC is a primary center of attention. We suggest that the commonly reported activation of the IMPC by emotional stimuli can be a consequence of stimulus duration longer than 3 s rather than of the emotional processing per se. We propose that it is one of the functions of the IMPC to choose among multiple foci of attention and hence to be a switch between default and contingent modes of brain operation.

Supplementary Material

Supplementary material can be found at: http://www.cercor.oxfordjournals.org/.

Conflict of Interest: None declared.

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