Processing emotional pictures and words: Effects of valence


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Cognitive, Affective, & Behavioral Neuroscience 2006, 6 (2), 110-126
Processing emotional pictures and words: Effects of valence and arousal
ELIZABETH A. KENSINGER and DANIEL L. SCHACTER Boston College, Chestnut Hill, Massachusetts
and Athinoula A. Martinos Center for Biomedical Imaging, Charlestown, Massachusetts
There is considerable debate regarding the extent to which limbic regions respond differentially to items with different valences (positive or negative) or to different stimulus types (pictures or words). In the present event-related fMRI study, 21 participants viewed words and pictures that were neutral, negative, or positive. Negative and positive items were equated on arousal. The participants rated each item for whether it depicted or described something animate or inanimate or something common or uncommon. For both pictures and words, the amygdala, dorsomedial prefrontal cortex (PFC), and ventromedial PFC responded equally to all high-arousal items, regardless of valence. Laterality effects in the amygdala were based on the stimulus type (word  left, picture  bilateral). Valence effects were most apparent when the individuals processed pictures, and the results revealed a lateral/medial distinction within the PFC: The lateral PFC responded differentially to negative items, whereas the medial PFC was more engaged during the processing of positive pictures.

In our daily lives, we experience many events that trigger an emotional response: We receive a compliment, witness a car crash, or watch children playing in a park. One widely accepted framework used to classify these diverse emotional experiences describes emotion in two orthogonal dimensions: Valence is a continuum specifying how negative or positive an event is, whereas arousal refers to the intensity of an event, ranging from very calming to highly exciting or agitating (e.g., Lang, Greenwald, Bradley, & Hamm, 1993; Mehrabian & Russell, 1974; Russell, 1980). There has been much interest in understanding how these different dimensions influence the neural processes recruited during the processing of an emotional event, with particular emphasis on examining how processing in the amygdala and the prefrontal cortex (PFC) is affected by stimulus valence and arousal.
The amygdala often responds preferentially to fear-evoking stimuli, in comparison with stimuli evoking other types of emotions (e.g., happiness, disgust, or anger; Irwin et al., 1996; Morris et al., 1996; Phillips et al., 1997; Whalen et al., 1998; Whalen et al., 2001), and patients with damage to the amygdala often are disproportionately impaired at recognizing or expressing fear (Adolphs, Tranel, Damasio, & Damasio, 1995; Broks et al., 1998; Scott et al., 1997). These findings initially had been interpreted as evidence that the amygdala plays a specific role in the processing of fear-related information, in comparison with other types of information (see Baas, Aleman, & Kahn, 2004; David-
Correspondence concerning this article should be addressed to E. A. Kensinger, Department of Psychology, Boston College, McGuinn Hall 510, 140 Commonwealth Ave., Chestnut Hill, MA 02467 (e-mail: elizabeth [email protected]).

son & Irwin, 1999). In most of the studies demonstrating this preferential amygdala response, however, the fear-related stimuli were more arousing than the other types of stimuli. Therefore, a viable alternative interpretation is that amygdala activity is linked to the arousal of stimuli. In support of this interpretation, recent studies have demonstrated that the amygdala responds to a range of higharousal emotions (e.g., surprise or happiness; Breiter et al., 1996; Kim, Somerville, Johnstone, Alexander, & Whalen, 2003; Whalen et al., 2001). In fact, nearly all studies that have examined amygdala activity to positive and negative stimuli matched in arousal have found that the amygdala responds to both types of stimuli (Garavan, Pendergrass, Ross, Stein, & Risinger, 2001; Hamann, Ely, Grafton, & Kilts, 1999; Hamann, Ely, Hoffman, & Kilts, 2002; Hamann & Mao, 2002). This finding has been replicated using pictorial stimuli (Anders, Lotze, Erb, Grodd, & Girbaumer, 2004; Garavan et al., 2001; Hamann et al., 2002), olfactory stimuli (Anderson et al., 2003; Royet et al., 2000), and gustatory stimuli (Small et al., 2003). Across these modalities, amygdala activity has been found to relate to the intensity, or arousal, of the stimuli, irrespective of valence (but see Kim et al., 2003, for evidence that whereas the dorsal amygdala, the region most commonly revealed by f MRI, may respond on the basis of arousal, ventral subregions may respond in a valencedependent manner).
There is evidence that some regions of the PFC also respond in a valence-independent way. In particular, some regions of the medial PFC have shown greater responses for both positive and negative stimuli than for neutral stimuli (Anders et al., 2004; Dolcos, LaBar, & Cabeza, 2004; Lane, Fink, Chau, & Dolan, 1997; Lane, Reiman, et al., 1997), and in some studies, large regions of the right

Copyright 2006 Psychonomic Society, Inc.

110

EMOTIONAL PICTURES AND WORDS 111

PFC have been implicated in the processing of both positive and negative information (see Bowers, Bauer, Coslett, & Heilman, 1985; Harrington, 1995; Hellige, 1993). The suggestion that the PFC responds in a valence-independent manner, however, has not been universally accepted, and there is ample evidence that many PFC regions respond differentially to positive and negative stimuli.
There have been two prevailing views regarding valencebased effects in the PFC. One is that the left hemisphere (and specifically, the left PFC) plays a disproportionate role in the processing of positive emotions, whereas the right hemisphere (and in particular, the right PFC) is dominant during the processing of negative emotions (see Davidson, 1995; Davidson & Irwin, 1999). Evidence to support this valence-based laterality hypothesis has come mainly from lesion and electrophysiological studies. Patients with left-hemisphere lesions tend to show depressive symptoms, whereas patients with right-hemisphere lesions are more likely to show euphoria (e.g., Lee, Loring, Meader, & Brooks, 1990; Morris et al., 1996; Paradiso, Chemerinski, Yazici, Tartaro, & Robinson, 1999; Paradiso, Johnson, et al., 1999; Starkstein et al., 1989). Measures of electrophysiological activity have corroborated the hemispheric asymmetry based on valence: Individuals with high right frontal baseline activity report more negative affect and less positive affect than do individuals with higher left frontal baseline activity (e.g., George, Ketter, & Post, 1993; Tomarken, Davidson, Wheeler, & Doss, 1992), and event-related potentials are greater in the right hemisphere during the processing of negative stimuli and are greater in the left hemisphere during the processing of positive stimuli (e.g., Aftanas, Varlamov, Pavlov, Makhnev, & Reva, 2001; Wheeler, Davidson, & Tomarken, 1993). The functional neuroimaging literature, in contrast, has pro-

vided only mixed support for this hypothesis. A few f MRI studies have provided evidence of a left/right distinction in the processing of positive and negative pictures (Canli, Desmond, Zhao, Glover, & Gabrieli, 1998; Dolcos et al., 2004) or the generation of positive and negative emotion (Sutton et al., 1997), but others have not (e.g., Lane, Fink, et al., 1997; Schneider et al., 1995; Teasdale et al., 1999).
The second proposal, which has garnered its strongest support from neuroimaging investigations, is that lateral orbital PFC regions respond preferentially to negative stimuli, whereas ventromedial PFC regions respond preferentially to positive stimuli. Evidence supporting this hypothesis has come from studies in which the reward value of stimuli has been manipulated (e.g., by inducing satiety for a particular food): In these studies, as the stimulus became less rewarding, activity in the ventromedial PFC decreased, whereas activity in the orbitolateral PFC increased (Small, Zatorre, Dagher, Evans, & Jones-Gotman, 2001; see also O’Doherty et al., 2000). A similar modulation of the PFC has been found on tasks varying monetary rewards and punishments: The ventromedial PFC has tended to show a greater response for rewards than for punishments, whereas the orbitolateral PFC has shown the opposite pattern of response (O’Doherty, Critchley, Deichmann, & Dolan, 2003; O’Doherty, Kringelbach, Rolls, Hornak, & Andrews, 2001).
In summary, the literature to date has suggested that the amygdala (at least the dorsal amygdala; Kim et al., 2003) may respond in an arousal-based fashion, whereas the PFC may respond in a valence-dependent manner. However, the specific effects of valence on PFC activity remain unclear. Moreover, because nearly all neuroimaging studies investigating the effects of valence and arousal on emotional processing have focused exclusively on the

Animate?

0.5 sec

2.5 sec

+

6–16 sec

Common?

avocado

+ Common?

Figure 1. While in the scanner, the participants viewed positive, negative, and neutral pictures and words, each for 2.5 sec. Each stimulus was preceded by the prompt of “Animate?” or “Common?” indicating the question that the participants should answer regarding the stimulus: Did the stimulus depict or describe something animate, or did the stimulus depict or describe something that would be encountered within a typical month? Interstimulus intervals of 6–16 sec were interspersed between stimuli to provide jitter.

112 KENSINGER AND SCHACTER

amygdala or the PFC (but see Anders et al., 2004, who also examined activity in the insula, thalamus, and anterior parietal cortex), the full network of regions underlying arousal-related versus valence-dependent processing remains underspecified.
The first goal of the present study was to use wholebrain imaging to elucidate the network of regions that respond in an arousal-related manner (i.e., to all high-

arousal stimuli, regardless of valence) versus in a valencerelated manner (i.e., preferentially to positive or negative stimuli). We also wanted to examine whether the arousaland valence-based patterns of activity demonstrated in prior experiments would extend to a paradigm in which participants were asked to judge stimuli for nonemotional factors (whether the stimulus described or depicted something animate/inanimate or something common/uncom-

Table 1 Regions That Showed a Greater Response to Positive Items Than to Neutral Items

Lobe

Region

Hemisphere

Talairach Coordinates of
Peak Voxel (x, y, z)

MNI Coordinates of
Peak Voxel (x, y, z)

Approximate Brodmann Area

Frontal

Superior frontal gyrus Inferior frontal gyrus Medial frontal gyrus

Temporal

Superior temporal gyrus Middle temporal gyrus

Parietal Occipital Cingulate

Inferior temporal gyrus Fusiform gyrus Inferior parietal lobe
Precuneus
Cuneus Lingual gyrus
Cingulate gyrus

Cerebellum

Positive  Neutral (All)

L

9, 54, 22

16, 25, 43

L

30, 14, 16

53, 15, 10

L

9, 36, 29

12, 45, 23

R

12, 54, 24

Bilateral 5, 55, 11

L R L
R
L R R
L
L L R Bilateral

0, 40, 17 45, 17, 13 41, 35, 7 45, 75, 12 60, 6, 15 45, 60, 18 62, 44, 1 63, 18, 17 39, 50, 12 48, 25, 23 50, 56, 39 33, 70, 42 12, 63, 31 15, 90, 5 30, 76, 6 18, 55, 2 3, 37, 10 3, 11, 8 3, 34, 32 3, 19, 34

0, 38, 12

3, 60, 28

3, 7, 28

L

9, 56, 15

9, 54, 27 16, 24, 48 30, 15, 18 54, 15, 12 9, 36, 33 12, 45, 27
12, 54, 29
5, 56, 15
0, 42, 18 45, 18, 14 41, 36, 6 45, 78, 9 61, 5, 18 45, 63, 16 63, 45, 4 64, 18, 21 39, 51, 17 48, 27, 24 51, 60, 39 33, 74, 42 12, 66, 30 15, 93, 1 30, 78, 12 18, 57, 6 3, 39, 10 3, 12, 9 3, 37, 33 3, 18, 38
0, 39, 15
3, 63, 27 3, 9, 30 9, 57, 21

9 8 47 44 9 8, 9 10 9, 10 11 38 22 39 21 39 21 20 37
40 7 31 17 18 18/19 32 25 31 24 32 31 24

Positive  Neutral (Pictures)

Frontal

Medial frontal gyrus

Temporal
Parietal Occipital Cingulate

Superior temporal gyrus Middle temporal gyrus Amygdala Parahippocampal gyrus Postcentral gyrus Precuneus Lingual gyrus Cingulate gyrus

L

12, 40, 28

12, 40, 33

9

6, 50, 10

6, 52, 9

10

R

8, 34, 11

8, 36, 11

R

45, 54, 20

45, 56, 19

22

R

45, 64, 11

45, 66, 8

37

R

15, 3, 13

15, 2, 15

R

30, 30, 6

30, 31, 9

27

L

50, 11, 17 51, 12, 18

43

Bilateral 0, 55, 58

0, 60, 60

7

R

18, 87, 4

18, 90, 1

17

L

11, 60, 17 11, 63, 15

31

R

17, 42, 30

17, 45, 30

31

9, 40, 27

9, 43, 27

23

Bilateral 3, 37, 10

3, 39, 10

32

0, 38, 12

0, 39, 15

24

0, 48, 20

0, 50, 19

30

EMOTIONAL PICTURES AND WORDS 113

Lobe Frontal
Temporal Parietal Occipital Cingulate Cerebellum

Table 1 (Continued)

Region

Hemisphere

Talairach Coordinates of
Peak Voxel (x, y, z)

Positive  Neutral (Words)

Superior frontal gyrus
Middle frontal gyrus Inferior frontal gyrus Medial frontal gyrus

L

6, 60, 27

30, 25, 48

39, 14, 50

L

48, 46, 2

45, 16, 27

L

53, 19, 24

32, 14, 13

L

8, 48, 22

6, 62, 16

R

8, 62, 21

Precentral gyrus Superior temporal gyrus Middle temporal gyrus
Inferior temporal gyrus Fusiform gyrus Superior parietal lobe Inferior parietal lobe
Postcentral gyrus Precuneus/angular gyrus Inferior/middle occipital gyrus Cingulate gyrus

R L L
L R L L R R L R Bilateral

60, 16, 40 48, 14, 11 62, 46, 5 53, 29, 1 62, 15, 14 39, 50, 15 30, 67, 50 54, 48, 24 45, 56, 47 48, 15, 40 45, 65, 34 36, 79, 6 3, 36, 23

3, 39, 17

Caudate

0, 33, 32

0, 48, 22

L

14, 56, 20

L

15, 12, 10

MNI Coordinates of
Peak Voxel (x, y, z)
6, 60, 33 30, 23, 53 39, 12, 55 48, 47, 0 45, 15, 30 53, 18, 27 32, 15, 15 8, 48, 26 6, 63, 26 8, 62, 26 61, 19, 43 48, 15, 12 63, 48, 3 53, 30, 1 63, 15, 18 39, 51, 21 30, 72, 51 55, 50, 23 45, 60, 48 48, 18, 43 45, 69, 33 36, 81, 12 3, 36, 27 3, 39, 21 0, 36, 33 0, 50, 21 14, 57, 27 15, 12, 12

Approximate Brodmann Area
9 8 6/8 10 9/46 45 47 9 10 10 6 38 22 21 21/22 37 7 40 7/40 3 39 18/19 32 32 31 23/30

mon). If we think of the requirement for monitoring emotional responses as being on a continuum, prior studies examining valence and arousal effects have been closer to the high-monitoring end of the spectrum than to the lowmonitoring end. Some of the tasks have required explicit regulation of emotion, asking participants to experience the emotion elicited and to make a pleasantness rating (Dolcos et al., 2004). Other studies, although not requiring explicit reporting of the emotional reaction, have nevertheless emphasized that participants should attend to their emotional responses to the stimuli (e.g., “pay attention and experience whatever thoughts or feelings the pictures may elicit in you”; Hamann et al., 2002). A number of studies have suggested that the processes engaged while an emotional experience is monitored or labeled may be distinct from those typically recruited during the processing of emotional information (e.g., Cunningham, Raye, & Johnson, 2004; Hariri, Bookheimer, & Mazziotta, 2000; Lane, Fink, et al., 1997; Lane, Reiman, et al., 1997; Lange et al., 2003; Taylor, Phan, Decker, & Liberzon, 2003; but see Hutcherson et al., 2005, for evidence that monitoring and reporting an emotional response may not have robust effects on behavioral performance or neural activity). Thus, we wanted to examine whether distinct arousaland valence-based responses would still be apparent when participants performed a task that did not require monitoring of an emotional response.

The second goal of the present study was to examine whether the stimulus type (picture or word) would affect the pattern of arousal-related and valence-dependent responses. To our knowledge, no study has compared the arousal- and valence-based processing of two different types of emotional stimuli within the same paradigm (but see Royet et al., 2000, for a comparison of emotionally valenced olfactory, visual, and auditory stimuli). By assessing the neural responses to emotional pictures and words, we could examine the extent to which valencedependent and arousal-based processing overlapped for the two stimulus classes. We were particularly interested in whether the stimulus type would affect the pattern of response in the amygdala: Although there is some evidence, from cross-study comparisons, that the amygdala responds to high-arousal stimuli across a range of modalities and stimulus types (Anderson et al., 2003; Garavan et al., 2001; Hamann et al., 2002; Small et al., 2003), differences in image acquisition methods make it difficult to determine whether it is the same amygdala subregions that respond or whether distinct regions respond on the basis of the type of information being processed. As a corollary of this second goal, we examined whether valence or stimulus type would affect the laterality of amygdala recruitment. Although some research has suggested that the amygdala may respond in a stimulus-specific manner (i.e., the left amygdala responding to words, and the right

114 KENSINGER AND SCHACTER

Table 2 Regions That Showed a Greater Response to Negative Items Than to Neutral Items

Lobe

Region

Hemisphere

Talairach Coordinates of
Peak Voxel (x, y, z)

MNI Coordinates of
Peak Voxel (x, y, z)

Approximate Brodmann Area

Negative  Neutral (All)

Frontal Superior frontal gyrus

Bilateral 3, 62, 22

3, 63, 28

9/10

0, 56, 28

0, 56, 33

9/10

Inferior frontal gyrus

L

L

42, 20, 14 42, 21, 15

47

45, 18, 13

45, 18, 15

45

R

53, 23, 2

54, 24, 3

47

Medial frontal gyrus

Bilateral 3, 43, 14

3, 45, 14

11

0, 54, 10

0, 56, 9

10

Temporal Superior temporal gyrus L

56, 60, 14 56, 62, 12

39

50, 11, 18 50, 12, 21

38

R

62, 46, 10

63, 48, 8

22

44, 43, 18

44, 45, 17

13

Middle temporal gyrus

L

51, 6, 15 51, 7, 16

21

R

50, 60, 16

50, 63, 14

19

53, 69, 20

54, 72, 18

39

56, 5, 15

56, 6, 18

21

Inferior temporal gyrus R

62, 7, 17

63, 6, 21

21

Amygdala

L

21, 6, 17 21, 5, 21

Parietal Precuneus

Bilateral 3, 57, 30

3, 60, 30

7

3, 62, 36

3, 66, 36

7

Inferior parietal lobe

R

56, 42, 24

57, 45, 24

40

Cingulate gyrus

Bilateral 0, 45, 27

0, 48, 27

Frontal Temporal Occipital

Superior frontal gyrus Inferior frontal gyrus
Medial frontal gyrus Superior temporal gyrus Middle temporal gyrus Fusiform gyrus Amygdala
Middle occipital gyrus Cingulate gyrus Thalamus Hypothalamus

Negative  Neutral (Pictures)

Bilateral L
R

3, 54, 27 48, 15, 15 33, 13, 18 53, 23, 2

L L
L R L R L
R R Bilateral
L R

56, 30, 9
3, 43, 12 50, 55, 16 45, 16, 26 38, 75, 25 50, 60, 17 41, 44, 15 39, 53, 7 21, 3, 12 23, 8, 10 20, 4, 17 42, 64, 1 11, 49, 19 2, 20, 6 12, 11, 6 12, 3, 7

3, 54, 32
48, 15, 17 33, 14, 21
53, 24, 3
57, 30, 11
3, 45, 12 50, 57, 14 45, 18, 30 38, 79, 23 51, 63, 15 41, 45, 20 39, 54, 11 21, 3, 14 23, 8, 12 20, 3, 20 42, 66, 3 11, 51, 18 2, 21, 6 12, 12, 6 12, 3, 9

9 44/45
47 47 45 10 39 38 39 19 37 37
37 23/30 24/25

Frontal Temporal Parietal

Superior frontal gyrus Inferior frontal gyrus
Superior temporal gyrus
Middle temporal gyrus Amygdala Precuneus Cingulate gyrus

Negative  Neutral (Words)

L

9, 60, 27

R

0, 57, 27

L
L
R L R L L Bilateral

53, 27, 18 45, 20, 11 44, 37, 14 51, 45, 19 36, 13, 21 35, 14, 23 56, 52, 10 53, 26, 1 26, 0, 20 3, 62, 36 0, 45, 27

9, 60, 33
0, 57, 32
54, 27, 21 45, 21, 12 44, 39, 14 51, 47, 18 36, 14, 24 35, 16, 27 56, 54, 8 54, 27, 3 26, 1, 24 3, 66, 36 0, 48, 27

9/10 9/10 46 47 11 22 38 38 39 21/22
7 31

EMOTIONAL PICTURES AND WORDS 115

amygdala responding to pictures; see Markowitsch, 1998), to our knowledge, this hypothesis has not been directly assessed, and there are a number of other hypotheses regarding laterality effects in the amygdala (see Baas et al., 2004; Cahill, 2003; Glascher & Adolphs, 2003; Phelps et al., 2001).
METHOD
Participants The participants were 21 young adults (11 men) between the ages
of 18 and 35 years. All were right-handed native English speakers with no history of psychiatric or neurological disorders. No participant was taking any medication that would affect the central nervous system, and no participant was depressed. Informed consent was obtained from all the participants in a manner approved by the Harvard University and Massachusetts General Hospital Institutional Review Boards.
Materials Stimuli included 360 words (120 positive and arousing, 120 nega-
tive and arousing, and 120 neutral) and 360 pictures (120 positive and arousing, 120 negative and arousing, and 120 neutral). Words were selected from the ANEW database (Bradley & Lang, 1999) and were supplemented with additional neutral words. Pictures were selected from the IAPS database (Lang, Bradley, & Cuthbert, 1997) and were supplemented with additional neutral pictures. The words and pictures were chosen so that positive and negative words, and positive and negative pictures, were equated in arousal and in absolute valence (i.e., distance from neutral valence). In a separate testing session, conducted after completion of the f MRI study, the participants rated the stimuli for valence and arousal. The ratings generally agreed with those from the ANEW and IAPS databases.

Neutral pictures received a mean valence rating of 5.22 (SD  0.64) and a mean arousal rating of 3.45 (SD  0.77), whereas neutral words received a valence rating of 4.89 (SD  0.91) and a mean arousal rating of 3.59 (SD  0.30). Negative pictures received a mean valence rating of 2.76 (SD  0.75) and a mean arousal rating of 5.83 (SD  0.77), whereas negative words received a mean valence rating of 2.89 (SD  1.10) and a mean arousal rating of 5.58 (SD  0.46). Positive pictures received a mean valence rating of 6.99 (SD  0.66) and a mean arousal rating of 5.89 (SD  0.75), whereas positive words received a mean valence rating of 6.67 (SD  0.69) and a mean arousal rating of 5.58 (SD  0.62). In the rare instances in which the participants’ ratings did not agree with the normative data ( 1% of all responses), the items in question were not included in the analyses for that participant.
Positive, negative, and neutral words were matched in frequency, familiarity, imageability, and word length, as determined by normative data in the ANEW database (Bradley & Lang, 1999) and in the MRC psycholinguistic database (Coltheart, 1981). Positive, negative, and neutral pictures were matched for visual complexity (as rated by 5 young adults who did not participate in the MRI study; they were instructed that high scene complexity could be based on “the number of objects, scene details, or colors present in a scene, visual clutter, asymmetry, lack of open spaces, or lack of organization”; see Oliva, Mack, Shrestha, & Peeper, 2004), brightness (as assessed via Adobe Photoshop), and the number of stimuli that included people, animals, or buildings and landscapes. In addition, because the participants were asked to determine whether words and pictures described or depicted something (1) animate or (2) common (see below), the stimuli were selected so that roughly half of the stimuli from each emotion category received a “yes” response to each question.
Procedure The participants were scanned as they viewed 180 words and 180
pictures (60 from each emotional category; see Figure 1). Each word

% Signal Change

0.20 0.15 0.10 0.05
0 –0.05 –0.10 –0.15 –0.20 –0.25

Neg pict

Neu pict

Pos Neg Neu Pos pict word word word

% Signal Change

0.5 0.4 0.3 0.2 0.1
0 –0.1 –0.2 –0.3 –0.4
Neg Neu Pos Neg Neu Pos pict pict pict word word word
Figure 2.Arousal responses (negative  neutral and positive  neutral), collapsing across pictures and words. Both the dorsomedial prefrontal cortex (PFC; circled in pink) and the ventromedial PFC (circled in yellow) showed an arousalrelated response, as did the amygdala (see Figure 4 for time courses in the amygdala).

116 KENSINGER AND SCHACTER

or picture was presented for 2,500 msec. Preceding half of the stimuli was the prompt “Animate?”; the prompt “Common?” preceded the remaining stimuli. The prompt was presented for 500 msec and indicated the question that the participants should answer as they viewed the upcoming stimulus. The participants were instructed to respond “yes” to the “Animate?” prompt if a picture included an animate element or if a word described something animate (either the name of something animate [e.g., a snake] or a word that would generally be used in reference to something animate [e.g., laugh]) and otherwise to respond “no.” The participants were asked to respond “yes” to the “Common?” prompt if the stimulus depicted or described something that they would encounter in a typical month.1 Emotional processing did not differ on the basis of task (judgments of animacy vs. commonality), so all the reported results collapse across the two tasks. Words and pictures from the different emotion categories and prompt conditions were pseudorandomly intermixed, with interstimulus intervals (ISI) ranging from 6 to 16 sec. This design created jitter (Dale, 1999), and in addition, pilot data indicated

that this ISI was sufficient to allow the emotional response to one item to dissipate before presentation of the next item.
Image Acquisition and Data Analysis Images were acquired on a 1.5 Tesla Siemens Sonata MRI scan-
ner. Stimuli were back-projected onto a screen in the scanner bore, and the participants viewed the words through an angled mirror attached to the head coil. Detailed anatomic images were acquired using a multiplanar rapidly acquired gradient echo (MP-RAGE) sequence. Functional images were acquired using a T2*-weighted echo planar imaging sequence (TR  3,000 msec, TE  40 msec, FOV  200 mm, flip angle  90°). Twenty-nine axial-oblique slices (3.12-mm thickness, 0.6-mm skip between slices), aligned in a plane along the axis connecting the anterior commisure and the posterior commisure, were acquired in an interleaved fashion.
All preprocessing and data analysis were conducted within SPM99 (Wellcome Department of Cognitive Neurology). Standard preprocessing was performed on the functional data, including slice-

Table 3 Regions That Showed an Arousal-Related Response: Greater Activity for Positive Items Than for
Neutral Items and for Negative Items Than for Neutral Items

Lobe

Region

Hemisphere

Talairach Coordinates of
Peak Voxel (x, y, z)

MNI Coordinates of
Peak Voxel (x, y, z)

Approximate Brodmann Area

Frontal Temporal
Occipital Cingulate

Negative  Neutral and Positive  Neutral (All)

Superior frontal gyrus

L

9, 54, 22

9, 54, 27

R

3, 54, 28

3, 54, 33

Inferior frontal gyrus

L

30, 14, 16 30, 15, 18

54, 15, 10

54, 15, 12

Medial frontal gyrus

Bilateral 0, 60, 16

0, 61, 20

Superior temporal gyrus Middle temporal gyrus Fusiform gyrus Amygdala
Middle occipital gyrus Cingulate gyrus Putamen

L R L R L L R
R Bilateral
L

0, 40, 17 45, 17, 13 56, 43, 10 48, 70, 12 63, 6, 15 39, 53, 15 15, 4, 18 28, 1, 17 15, 1, 17 48, 73, 6 3, 60, 28 0, 45, 22 21, 1, 11

0, 42, 18 45, 18, 14 57, 45, 9 48, 73, 9 63, 5, 18 39, 54, 21 15, 3, 21 28, 0, 20 15, 0, 20 48, 75, 3 3, 63, 27 0, 47, 21 21, 0, 12

9 9 47 44 10 11 38 21/22 39 21 37
37 31 23/30

Frontal Temporal
Parietal Occipital

Negative  Neutral and Positive  Neutral (Pictures)

Medial frontal gyrus
Superior temporal gyrus Middle temporal gyrus
Fusiform gyrus Amygdala
Parahippocampal gyrus
Precuneus Middle occipital gyrus Cingulate gyrus

Bilateral
R R
R R
R
Bilateral R R Bilateral

6, 51, 28
3, 52, 10 45, 54, 20 45, 64, 11 60, 45, 2 53, 6, 10 48, 7, 22 15, 3, 15 25, 1, 17 30, 30, 6 24, 36, 11 6, 45, 50 48, 72, 6 12, 49, 14 0, 39, 30
0, 39, 12
3, 37, 9 3, 4, 30

6, 51, 33
3, 54, 9 45, 56, 19 45, 66, 9 61, 46, 0 54, 6, 12 48, 6, 27 15, 2, 18 25, 0, 20 30, 30, 9 24, 37, 15 6, 49, 52 48, 74, 3 12, 51, 13 0, 42, 30
0, 40, 15
3, 39, 8 3, 3, 33

9 10, 11
22 37 22 21, 38 20
27 35 7 19 23, 30 31 24, 32 32 24

EMOTIONAL PICTURES AND WORDS 117

Table 3 (Continued)

Lobe

Region

Hemisphere

Talairach Coordinates of
Peak Voxel (x, y, z)

MNI Coordinates of
Peak Voxel (x, y, z)

Approximate Brodmann Area

Negative  Neutral and Positive  Neutral (Words)

Frontal

Superior frontal gyrus Middle frontal gyrus
Inferior frontal gyrus

Medial frontal gyrus Temporal Superior temporal gyrus

Middle temporal gyrus

Parietal
Occipital Cingulate

Amygdala Superior parietal lobe Inferior parietal lobe Precuneus Inferior/middle occipital gyrus Cingulate gyrus

Cerebellum

L L
L
Bilateral
L
R L R L L L L R Bilateral

6, 60, 27 39, 22, 49 48, 40, 10 39, 14, 50 45, 19, 27 54, 19, 24 48, 18, 5 45, 20, 11 56, 18, 10 0, 40, 17 3, 43, 37 6, 65, 16 48, 14, 11 42, 10, 31 50, 2, 10 39, 43, 13 60, 50, 8 60, 30, 1 53, 27, 1 25, 4, 17 39, 64, 48 42, 65, 47 3, 60, 39 48, 78, 1 0, 45, 30 0, 49, 21 3, 19, 31 3, 2, 28 6, 56, 15

6, 60, 33 39, 20, 54 48, 42, 10 39, 12, 55 45, 19, 30 54, 18, 27 48, 18, 6 45, 21, 12 56, 18, 12 0, 42, 18 3, 42, 43 6, 66, 21 48, 15, 12 42, 12, 36 51, 3, 12 39, 45, 12 60, 42, 7 60, 31, 0 53, 28, 3 25, 3, 20 39, 68, 49 42, 69, 47 3, 64, 39 48, 80, 6 0, 48, 30 0, 51, 20 3, 21, 33 3, 4, 30 6, 57, 21

9, 10 6, 8 11
6 9/46 45, 9 45, 47 47 44 11
6 10 38 38 21 22 22/39 21/22 21/22
7 7/40
7 18, 19
31 23/30
23 24

Note—Underlined regions were revealed when the individual contrast analyses were set to a threshold of p .05 and a 20-voxel extent. All other regions were present when the individual contrast analyses entered into the conjunction analysis were analyzed at a threshold of p .01 and a 10-voxel extent.

timing correction, rigid body motion correction, normalization to the Montreal Neurological Institute template (resampling at 3 mm cubic voxels), and spatial smoothing (using an 8-mm full-width half maximum isotropic Gaussian kernel).
For each participant, and on a voxel-by-voxel basis, an event-related analysis was first conducted in which all instances of a particular event type were modeled through convolution with a canonical hemodynamic response function. Effects for each event type were estimated using a subject-specific, fixed-effects model. These data were then entered into a second-order, random effects analysis. Contrast analyses were performed to examine effects of valence (positive vs. negative); one-sample t tests were used to examine the consistency of activity at each voxel (using between-participants variability to estimate variance). An individual voxel threshold of p .01 with a cluster threshold of 19 contiguous voxels was used to yield results corrected for multiple comparisons to p .05 (see Slotnick, Moo, Segal, & Hart, 2003). Conjunction analyses, using the masking function in SPM99, examined the regions shared between two contrasts. The results for these conjunction analyses are presented in two ways: with the individual contrasts included in the contrast analysis analyzed at a threshold of p .01 and with a voxel extent of 10 voxels (so that the conjoint probability of the conjunction analysis, using Fisher’s estimate [Fisher, 1950; Lazar, Luna, Sweeney, & Eddy, 2002], was p .001) and with the contrasts analyzed at a more lenient threshold ( p .05) but with a larger voxel extent (20 voxels).2
All activations are presented in neurological coordinates (i.e., activity on the right hemisphere is presented on the right side of the brain images). Voxel coordinates are reported in Talairach coordinates (Talai-

rach & Tournoux, 1988) and in Montreal Neurological Institute (MNI) coordinates (Collins et al., 1998) and reflect the most significant voxel within the cluster of activation. Event-related time courses were extracted from active clusters by creating regions-of-interest (ROIs) as 8-mm spheres, using the ROI toolbox implemented in SPM99.
RESULTS
Analyses were conducted to identify the regions that responded to all high-arousal stimuli, regardless of valence, versus in a valence-dependent manner. These analyses were conducted separately for all the stimuli (collapsing across pictures and words), for pictures only, and for words only. Thus, we could examine the extent to which stimulus type affected the pattern of responses.
Arousal Responses We first collapsed across pictures and words to exam-
ine the regions in which activity was enhanced for positive, in comparison with neutral, stimuli and for negative, in comparison with neutral, stimuli (i.e., positive  neutral and negative  neutral; see Tables 1 and 2 for regions identified in each of these separate contrasts).3 The regions revealed by this conjunction analysis were those that responded to all high-arousal items, regardless

118 KENSINGER AND SCHACTER

of valence (see Figure 2; yellow indicates regions identified when individual contrasts were analyzed at p .01 with a 10-voxel extent; green indicates regions identified when individual contrasts were analyzed at p .05 with a 20-voxel extent). Consistent with prior findings (Dolcos et al., 2004; Hamann et al., 2002), activity in the dorsomedial PFC (Figure 2, region outlined in pink; Talairach coordinates 3, 54, 28; BA 9/10) and in the amygdala bilaterally (Figure 2, region outlined in blue; Talairach coordinates 15, 4, 18; 15, 1, 17) showed this arousalrelated pattern of response. In addition, a second region of the medial PFC, in a very ventral portion (Figure 2, region outlined in yellow; Talairach coordinates 0, 40, 17; BA 11) also showed this arousal-based activity, as did a large portion of the anterior temporal lobe, a region spanning the temporo-occipital junction, and a portion of the left dorsolateral PFC (see Table 3).
We then examined whether these arousal responses were consistent when analyses were conducted separately for pictures and words. When the conjunction analysis was conducted only for pictures, the results looked very similar to those discussed for all stimuli (Figure 3, panel A): Activity in the same two medial PFC regions (outlined in pink and yellow; Talairach coordinates 6, 51, 28 [BA 9] and 3, 52, 10, [BA 10 and 11]) and in the amygdala bilaterally (outlined in blue; Talairach coordinates 15, 3, 15; 25, 1, 17) corresponded with arousal-related activity, as did activity in the anterior temporal lobe and in a region spanning the temporo-parietal junction (see Table 3). For the pictures, however, the activity in the latter two regions was strongest in the right hemisphere (as depicted in Figure 3).
When arousal-related activity for the words was analyzed (Figure 3, panel B), the same two regions of the medial PFC (outlined in pink and yellow; Talairach coordinates 6, 60, 27 [BA 9 and 10] and 0, 40, 17 [BA 11]) were identified. Amygdala activity also corresponded with arousal-related activity, but the activation was lateralized to the left (outlined in blue; Talairach coordinates 25, 4, 17). In addition, although there was activity in the anterior temporal lobe and in the temporo-occipital junction, this activity was stronger in the left hemisphere than in the right hemisphere [a pattern of laterality opposite to that demonstrated when only pictures were analyzed, as depicted in Figure 3 and as confirmed by a significant interaction between stimulus type and laterality on the arousal-related signal change throughout the lateral temporal lobe; F(1,19)  8.13, p .01]. Thus, the general arousal-based patterns of activation (in two regions of the medial PFC and in the amygdala) were comparable for both pictures and words (see Table 3).

ing to stronger right-lateralized activity and words leading to stronger left-lateralized activity. To further explore the factors that contributed to the laterality effects in the amygdala, we defined regions in the left and right amygdala functionally, from an analysis contrasting activity for positive and negative stimuli with activity for neutral stimuli (i.e., positive pictures  positive words  negative pictures  negative words  neutral pictures  neutral words).4 This analysis was, therefore, unbiased with regard to whether the activity in the amygdala was influenced by stimulus type (picture or word) or stimulus valence (positive or negative). For both of the amygdalar regions, we extracted the peak signal change (i.e., the maximum signal change, from baseline, along the time course).
As is shown in Figure 4, the left amygdala showed arousal-related activity for both pictures and words,
A
B

Laterality of Amygdala Activation The results described above indicated that although the
general patterns of arousal-related activity were comparable for pictures and for words, laterality effects throughout the temporal lobe, including those in the amygdala, may arise from stimulus-specific effects, with pictures lead-

Figure 3. Arousal responses (negative  neutral and positive  neutral) for (A) pictures and (B) words. For both stimulus types, arousal-related activity occurred in the dorsomedial prefrontal cortex (PFC; outlined in pink), in the ventromedial PFC (outlined in yellow), and in the amygdala (outlined in blue).

EMOTIONAL PICTURES AND WORDS 119

% Signal Change % Signal Change

0.4 0.3 0.2 0.1
0 –0.1 –0.2 –0.3

Neg pict

Left Amygdala

Neu pict

Pos Neg Neu Pos pict word word word

0.4 0.3 0.2 0.1
0 –0.1 –0.2 –0.3

Neg pict

Right Amygdala
Neu Pos Neg Neu Pos pict pict word word word

Figure 4. The left amygdala (in yellow) showed an arousal-related response for both pictures and words, whereas the right amygdala (in red) showed an above baseline response only for pictures.

whereas the right amygdala showed an above baseline response only for pictures. This laterality effect was confirmed by a repeated measures ANOVA conducted on the peak signal change in the regions of the right and left amygdala. We considered laterality (left or right), emotion type (positive, negative, or neutral), and stimulus type (picture or word) as within-subjects factors and sex (male or female) as a between-subjects factor. This analysis indicated a main effect of emotion type [positive and negative  neutral; F(2,18)  4.85, p .05; partial h2  .36] and an interaction between stimulus type and laterality [the left amygdala responded equally to pictures and words; the right amygdala responded more strongly to pictures; F(1,19)  4.11, p .05; partial h2  .18]. No other factors interacted with laterality, suggesting that in this task design, stimulus type was the predominant characteristic that led to laterality effects in the amygdala.
Valence Responses To examine the regions that showed a differential response
based on valence, we contrasted activity for high-arousal positive items with activity for high-arousal negative items (and vice versa). Because positive and negative items were matched in arousal, activation differences should be related to differences in valence. We first performed this analysis by collapsing across pictures and words. Within the PFC, the ventrolateral PFC responded more strongly to negative items than to positive items (red regions of Figure 5; Talairach coordinates 45, 15, 16 [BA 44] and 35, 6, 25 [BA 44/6]), whereas a region of the medial PFC (Figure 5, in

green) responded more to positive items than to negative items (Talairach coordinates 9, 27, 10 [BA 24/32/8 5]). In addition to these distinctions within the PFC, positive stimuli elicited greater activity than did negative stimuli in a large region spanning the precuneus and inferior parietal lobe, in the right superior temporal gyrus, in the inferior/ middle temporal gyrus bilaterally, and in the fusiform/lingual gyrus bilaterally (Figure 5; Table 5).
When valence effects were examined for pictures, the same general patterns of activity were revealed in the PFC (Figure 6, panel A): The bilateral ventrolateral PFC responded differentially to negative pictures, in comparison with positive pictures (BA 44/45/47), whereas activity in the medial PFC (BA 10) showed a preferential response to positive pictures, in comparison with negative pictures. Valence effects also were revealed outside of the PFC (see Tables 4 and 5). Activity was greater during processing of negative pictures than during processing of positive pictures in the superior temporal gyrus bilaterally, the left middle temporal gyrus, and the left anterior temporal lobe. The converse effect (processing of positive  negative) held in all of the regions described above for all the stimuli and was additionally revealed in the left lingual gyrus, the right cuneus, and a region spanning the left postcentral and precentral gyri.
When valence effects were examined for verbal stimuli, the effects were much less extensive than had been noted with pictures (Figure 6, panel B). Within the PFC, only a single left lateral PFC region (BA 44) showed greater activity for negative words than for positive words, and no

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Processing emotional pictures and words: Effects of valence