Skip to main content
NCBI home page
Social Cognitive and Affective Neuroscience logoLink to Social Cognitive and Affective Neuroscience
. 2010 Jun 27;6(4):434–441. doi: 10.1093/scan/nsq058

Sustained happiness? Lack of repetition suppression in right-ventral visual cortex for happy faces

Atsunobu Suzuki 1,✉, Joshua O S Goh 2,3, Andrew Hebrank 3, Bradley P Sutton 2, Lucas Jenkins 4, Blair A Flicker 3, Denise C Park 3
PMCID: PMC3150853  PMID: 20584720

Abstract

Emotional stimuli have been shown to preferentially engage initial attention but their sustained effects on neural processing remain largely unknown. The present study evaluated whether emotional faces engage sustained neural processing by examining the attenuation of neural repetition suppression to repeated emotional faces. Repetition suppression of neural function refers to the general reduction of neural activity when processing a repeated stimulus. Preferential processing of emotional face stimuli, however, should elicit sustained neural processing such that repetition suppression to repeated emotional faces is attenuated relative to faces with no emotional content. We measured the reduction of functional magnetic resonance imaging signals associated with immediate repetition of neutral, angry and happy faces. Whereas neutral faces elicited the greatest suppression in ventral visual cortex, followed by angry faces, repetition suppression was the most attenuated for happy faces. Indeed, happy faces showed almost no repetition suppression in part of the right-inferior occipital and fusiform gyri, which play an important role in face-identity processing. Our findings suggest that happy faces are associated with sustained visual encoding of face identity and thereby assist in the formation of more elaborate representations of the faces, congruent with findings in the behavioral literature.

Keywords: emotion, faces, repetition suppression, sustained processing, ventral visual cortex

INTRODUCTION

Preferential allocation of processing resources to emotional stimuli that signal potential reward or threat has obvious relevance to the survival of an individual. For example, prioritized detection of threatening emotional stimuli has been well studied such that they preferentially capture initial attention (Hansen and Hansen, 1988; Ohman et al., 2001), regardless of task relevance (Vuilleumier et al., 2001) or perceptual awareness (Morris et al., 1998; Whalen et al., 1998). This detection of threatening stimuli also occurs very rapidly probably through the ‘quick-and-dirty’ thalamo-amygdala pathway (LeDoux, 1996). The initial greater processing of emotional stimuli, relative to neutral stimuli, may also involve extended and sustained processing that help to preferentially encode details of the emotional stimuli. Indeed, memory studies showed that happy faces enhanced a conscious recollection of face identity rather than a feeling of familiarity, indicating the formation of fine representations of faces (D’Argembeau et al., 2003; D’Argembeau and van der Linden, 2007). In addition, Fox et al. (2001) demonstrated that participants had difficulty in disengaging attention from angry faces, especially in high-anxious individuals, implying an intrinsic effect of emotion to sustain processing of the emotional stimuli relative to neutral stimuli. However, such sustained processing of emotional stimuli has been rarely studied at the neural level. The present study addressed this issue by measuring repetition suppression of neural function for neutral and emotional faces with functional magnetic resonance imaging (fMRI).

Repetition suppression refers to the reduction of neural activity with repetition of stimuli, which has been replicated using a variety of stimuli and measurement techniques (Grill-Spector et al., 2006). While multiple mechanisms may underlie this phenomenon, one likely function is to reduce demands on the brain from repeated stimuli of limited significance and to allocate more neural resources to novel stimuli of potential significance (Rolls, 2005). Importantly, when a task requires the detection of repetition of identical faces, the repetition of faces becomes task-relevant, resulting in neural responses being relatively maintained and an attenuation of repetition suppression (Henson et al., 2002). Thus, given the intrinsic relevance of emotional faces for an individual’s behavior, emotional faces may also be associated with attenuated repetition suppression, when compared to neutral faces, due to sustained processing.

Direct comparisons of repetition suppression of emotional and neutral faces give mixed results. A number of fMRI studies reported repetition suppression for neutral faces in ventral visual cortex (Winston et al., 2004; Rotshtein et al., 2005) as well as in the amygdala (Glascher et al., 2004). Rotshtein et al. (2001) showed that ‘Thatcherized’ faces that looked highly unusual or odd produced less repetition suppression (more sustained processing) in the middle fusiform compared to normal faces. But it was not clear whether their finding could be generalized to more natural emotional faces. Ishai et al. (2004) addressed this issue by comparing repetition suppression for fearful faces and for neutral faces. Surprisingly, they reported greater suppression for repeated fearful faces than for repeated neutral faces in both the fusiform and amygdala, which they argued resulted from greater initial attention to fearful faces (Vuilleumier et al., 2001). This result in Ishai et al. (2004), however, may have been due to participants performing a match-to-target task. The task required different cognitive operations at the first viewing (encoding of a face) and at subsequent viewings (comparison with the encoded face), which were confounded with repetition and prevented a simple interpretation. In addition, previous studies of face emotion and repetition suppression did not examine emotionally positive faces. This is important because behavioral studies have demonstrated a memory advantage for happy faces, suggesting sustained preferential processing of emotionally positive material (D’Argembeau et al., 2003; D’Argembeau and van der Linden, 2007).

In the present study, we studied repetition suppression for happy (positive), angry (negative) and neutral faces simultaneously in an effort to clarify the role of face emotion in engaging sustained neural processing. The experiment was based on a variant of the repeated-and-single-trials paradigm (Ollinger et al., 2001), allowing us to estimate repetition suppression on an event-related basis. We focused on repetition suppression occurring in a short-time window because extensive repetition would habituate brain responses to any stimuli and thus be likely to obscure emotional modulation (Breiter et al., 1996). Given the possible interference that could occur between directed cognitive operations and repetition suppression (Ishai et al., 2004), we employed a passive-viewing task, which was shown to be an effective method in generating repetition suppression in our previous study (Goh et al., 2004).

Our main interest was whether attenuation of repetition suppression would be observed for emotional faces compared to neutral faces. Less repetition suppression for emotional faces relative to neutral faces was expected in perceptual brain regions involved in face processing, reflecting the formation of more detailed face representations for emotional faces (Henson et al., 2000). Such regions include ventral visual cortex, consisting of the inferior occipital and fusiform gyri (Haxby et al., 2000). The amygdala would also show attenuation of repetition suppression to emotional faces given its modulatory role in face perception and emotional processing (Vuilleumier, 2005). In addition, frontal regions have also been shown to play a role in processing face stimuli (Fairhall and Ishai, 2007). The frontal role in face processing may involve processes such as emotional empathy rather than facial detail (Nakamura et al., 1999; Carr et al., 2003; Winston et al., 2003; Leslie et al., 2004). Thus, it would be interesting to evaluate whether repetition suppression in frontal regions would similarly be modulated by emotion as in ventral visual cortex, or remain consistent across neutral, angry and happy stimuli as long as the same face emotions are repeated.

METHODS

Participants

Nineteen individuals (10 females, ages 19–29 with a mean age of 23.1) gave informed consent to participate in this study, which was approved by the University of Illinois at Urbana-Champaign Institutional Review Board. All the participants were right-handed, had normal or corrected-to-normal vision and reported no history of neurological or psychiatric illness.

Stimuli

Eighty-one digital images of faces were used as stimuli, comprised of neutral, angry and happy faces enacted by 27 posers. The stimuli were selected from four face databases developed by other research groups.1 The stimuli were standardized using MATLAB 7 and Adobe Photoshop CS2 in the following manner: they were cropped into a square shape so that only central features of the face (eyes, eyebrows, nose and mouth) were present, and then converted into gray-scale, with size, mean luminance and contrast equated. The stimuli were used in the fMRI experiment, with each stimulus subtended at visual angles of about 10° × 10°.

Experimental procedure

The fMRI experiment was based on a variant of the repeated-and-single-trials paradigm (Figure 1; Ollinger et al., 2001). In repeated trials, the same stimulus was presented twice consecutively and for 1.5 s each, separated by a 0.5-s fixation interval. In single trials, a single stimulus was presented once for 1.5 s. Between any two trials was a fixation interval of which duration randomly varied among 6.5, 8.5 and 10.5 s, with a mean of ∼7.5 s. Each of the 81 faces was presented once in both repeated and single trials, resulting in a total of 162 trials with six trial-types [(repeated, single) × (neutral, angry, happy)]. Participants were instructed to pay attention to the whole face when it appeared.

Fig. 1.

Fig. 1

Open in a new tab

A schematic time-course of the fMRI experiment.

The fMRI experiment was divided into six runs that lasted for 308 s each. Each run was composed of 27 trials that were preceded and followed by a fixation interval that lasted for 24 and 18 s, respectively. The six trial-types were distributed almost equally across the six runs and were quasi-randomized within a run. In order to minimize long-lag repetition suppression across trials, the same stimulus was never presented in different trials within a run. Repeated and single trials that presented the same stimulus were separated by about 80 trials on average (32–158 trials).

After the fMRI experiment, participants performed a behavioral experiment outside the MRI scanner. They viewed all the 81 faces again, and were asked to rate the intensity of anger and happiness expressed by each face using a 4-point scale (3: ‘very angry/happy’, 2: ‘moderately angry/happy’, 1: ‘a little angry/happy’, 0: ‘not angry/happy at all’). Ratings of the intensity of anger and happiness were made in different trials.

Imaging protocol

Imaging was performed with a 3-T Allegra scanner (Siemens, Erlangen, Germany). In the fMRI experiment, 154 functional images were acquired in each run using a gradient-echo spiral-in/spiral-out sequence, of which the first three images were discarded to allow for T1 equilibrium. Spiral-in/spiral-out images were reconstructed and combined following the weighted combination method described by Glover and Law (2001). The acquisition parameters were as follows: TR = 2000 ms, TE = 25 ms, flip angle = 80°, FOV = 240 mm, resolution = 3.75 × 3.75 × 3 mm (no gap). Each functional image contained 40 oblique axial slices approximately parallel to the AC-PC line, covering the whole brain. High-resolution coplanar T2 anatomical and 3D-MPRAGE anatomical images were also acquired for use in image co-registration and normalization.

fMRI data analyses

Image preprocessing and statistical analyses were conducted using SPM5 (Wellcome Department of Cognitive Neurology, Institute of Neurology, London, UK). Preprocessing of the functional images included slice-time correction, motion correction, co-registration with the anatomical images, spatial normalization to an MNI space (Montreal Neurological Institute, Montreal, Canada) and spatial smoothing with an 8-mm full-width at half-maximum Gaussian kernel.

Each participant’s preprocessed functional images were submitted to a voxel-by-voxel general-linear-model analysis with finite-impulse-response (FIR) predictors. Six sets of FIR predictors were used to separately estimate activations for the first neutral, angry and happy faces and the second neutral, angry and happy faces in repeated trials. The activations for the first neutral, angry and happy faces in repeated trials were assumed to be equal to activations for neutral, angry and happy faces in single trials, respectively. Thus, we modeled the activations to the first faces in repeated trials and the faces in single trials together under the same set of FIR predictors, i.e. as the first face of each emotion condition. Ollinger et al. (2001) presented a theoretical and empirical validation showing that this paradigm correctly estimates activations for the first and second faces, and subsequent studies have demonstrated its successful application (Soon et al., 2003; Kincade et al., 2005).

Each set of FIR predictors consisted of 10 delta functions spanning from 2 to 20 s after stimulus onset. This yielded 10 contrast images for each of the six conditions [(first, second) × (neutral, happy, angry)] per participant. The second to fifth contrast images (4–10 s after stimulus onset) from each condition were entered into a second-level random effect analysis, allowing for the latency of haemodynamic responses. To examine how each emotion condition would engage repetition suppression differently in face-responsive regions at the voxel-by-voxel level, we employed two functionally defined masks to restrict the number of voxels considered. In order to restrict analyses to face-responsive regions, we created a first mask that contained voxels significantly active for the first faces across all face emotions compared to fixation intervals.2 Within this face-responsive regions mask, we performed contrasts to identify voxels showing repetition suppression for each of the emotion conditions. That is, we identified voxels within face-responsive regions that were significantly more active for the first than for the second faces for neutral, angry and happy conditions, separately. In this analysis (i.e. construction of the face-responsive regions mask and identification of voxels showing repetition suppression), the combined voxel intensity and cluster size thresholds of P < 0.001, uncorrected and k > 20 were used in order to reduce the risks of both Type I and II errors in a balanced manner (Forman et al., 1995; Lieberman and Cunningham, 2009). Given that neural responses and repetition suppression to facial stimuli have been robustly observed (Haxby et al., 2000; Grill-Spector et al., 2006; Fairhall and Ishai, 2007), implying large effects, we chose this more stringent threshold.

Then, we defined a second mask as the union of those regions that showed significant repetition suppression for any of the three face emotions. Within this second mask of regions that showed repetition suppression to any face emotion, we performed pair-wise comparisons of differences in suppression between each of the emotion conditions, to identify voxels showing significantly greater suppression for one face emotion than for another face emotion. In addition, to evaluate if there were brain regions that showed a common pattern of repetition suppression across all three emotion conditions, we also identified voxels showing significant suppression irrespective of face emotion using a conjunction analysis within this second mask of regions showing suppression to any emotion. For both the pair-wise comparisons and the conjunction analysis, the threshold of P < 0.005, uncorrected, and k > 10 were used as suggested by Lieberman and Cunningham (2009). We chose this threshold for this second set of analysis because the effects of interest were expected to be small, given that pair-wise comparisons of repetition suppression are tests for ‘differences of differences’ which are associated with large error variances, and that the method of identifying functional regions by specifying conjunctions is conservative (Nichols et al., 2005). Moreover, the use of less stringent thresholds is justifiable given that masking greatly reduced the search space compared to the whole brain (∼2500 voxels; Gutchess et al., 2006).

Finally, in order to illustrate the magnitude of repetition suppression as a function of emotion condition, we also conducted a regions-of-interest (ROIs) analysis. The ROIs were functionally defined as 1-cm spheres around the peak voxels that showed differences in repetition suppression in the pair-wise comparisons between emotion conditions as well as peak voxels that showed common repetition suppression to all emotion conditions in the conjunction analyses above. For each of the ROIs, the effect size of repetition suppression was computed as the standardized difference between activation (averaged parameter estimates within a peristimulus time of 4–10 s) for the first faces and activation for the second faces expressed in ‘SD’ units (Afraz et al., 2006).

RESULTS

Behavioral experiment

Results confirmed the validity of the stimuli as follows. Angry faces attained the largest mean intensity rating of anger (2.28 ± 0.33), which was significantly larger than for neutral (0.77 ± 0.25, t = 21.52, P < 0.001) and happy faces (0.04 ± 0.06, t = 31.25, P < 0.001). Happy faces attained the largest mean intensity rating for happiness (2.48 ± 0.22), which was significantly larger than neutral (0.40 ± 0.23, t = 33.97, P < 0.001) and angry faces (0.03 ± 0.05, t = 49.43, P < 0.001).

fMRI experiment

The contrast of the first faces vs fixation intervals that defined the face-responsive regions, revealed a distributed neural system for face processing (Haxby et al., 2000; Fairhall and Ishai, 2007), including ventral visual cortex, the amygdala and the inferior frontal gyrus (Figure 2). The patterns of repetition suppression for each face emotion within these face-responsive regions were then examined separately for each emotion (Figure 3). Repetition suppression in ventral visual cortex was the most extensive for neutral faces, followed by angry faces, but was not significant for happy faces. In contrast, in the left-inferior frontal gyrus (slice y = 21 in Figure 3), repetition suppression was commonly observed across all three emotion conditions. Repetition suppression in the amygdala did not reach significance for any face emotion, probably due to the low signal-to-noise ratio in this region (LaBar et al., 2001; Zald, 2003). Table 1 provides more detail about repetition suppression for each face emotion.

Fig. 2.

Fig. 2

Open in a new tab

Face-responsive regions. Shown from left to right are coronal sections illustrating activation in ventral visual cortex (indicated by the arrows at y = −57 in an MNI space), the amygdala (y = 0) and the inferior frontal gyrus (y = 21).

Fig. 3.

Fig. 3

Open in a new tab

Repetition suppression for (A) neutral, (B) angry and (C) happy faces in the face-responsive regions. Suppression was observed for repeated neutral and angry faces but not for happy faces in the right-fusiform gyrus (indicated by the arrow at y = −57) and for all faces in the left-inferior frontal gyrus (y = 21). Suppression in the amygdala was not significant for any face (y = 0).

Table 1.

Peak voxels showing repetition suppression for each face emotion in the face-responsive regions

Brain region L/R MNI co-ordinate t
Neutral faces
    Inferior occipital gyrus R [36 −90 −12] 4.99
    Fusiform gyrus R [42 −60 −15] 4.88
    Superior parietal gyrus R [27 −66 51] 3.79
    Precentral gyrus R [54 −3 45] 3.88
    Insula L [−42 3 −3] 3.32
R [42 −3 −12] 3.68
    Temporal pole L [−54 12 −6] 4.67
R [51 18 −15] 3.28
Angry faces
    Calcarine cortex R [12 −87 −3] 3.85
    Cuneus R [9 −93 27] 4.05
    Fusiform gyrus R [42 −57 −18] 3.79
    Cingulate gyrus L [−6 24 36] 3.57
R [9 9 39] 3.56
    Precentral gyrus L [−45 −3 42] 3.51
    Insula R [45 6 −3] 3.72
    Inferior frontal gyrus L [−54 21 0] 4.09
Happy faces
    Middle temporal gyrus L [−57 −27 −12] 3.70
R [63 −39 −6] 4.00
    Cingulate gyrus R [12 18 39] 3.31
    Precentral gyrus R [48 −3 42] 3.50
    Inferior frontal gyrus L [−48 27 −9] 3.87
Open in a new tab

Note: the statistical threshold was P < 0.001 (uncorrected) with >20 contiguous voxels.

Within the union of these regions showing significant repetition suppression for any of the three emotion conditions (‘Methods’ section), suppression was compared pairwise between each of the face emotions. The comparisons revealed that the right-inferior occipital and fusiform gyri showed significantly greater suppression for repeated neutral faces than for repeated happy faces (inferior occipital: peak MNI coordinate = [30 −93 −12], t = 3.39, P < 0.001; fusiform: [36 −57 −21], t = 2.98, P = 0.002). The difference in repetition suppression between neutral and angry faces did not reach significance in any region. Furthermore, no regions showed significantly greater repetition suppression for emotional faces than for neutral faces. In contrast to the right-ventral visual regions that showed differences in repetition suppression due to face emotion, a conjunction analysis revealed that the left-inferior frontal gyrus (peak MNI coordinate = [−51 21 −6], t = 3.17, P = 0.001) and the right-precentral gyrus ([51 −3 42], t = 3.15, P = 0.001) commonly showed repetition suppression across emotion conditions.

The effect sizes of repetition suppression in the ROIs that showed differences as well as commonalities in suppression between emotion conditions (‘Methods’ section) are shown in Figure 4A. In the right-ventral visual regions, neutral faces showed the largest repetition suppression, and, most interestingly, happy faces showed almost no repetition suppression. The lack of repetition suppression for happy faces cannot be attributed to a floor effect because activation for the second neutral faces was well below activation for the second happy faces (Figure 4B). While angry faces appeared to have intermediate responses relative to happy and neural faces, these relative differences were not significant. Consistent with the conjunction analysis, on the other hand, the frontal regions showed equivalent repetition suppression across emotion conditions.

Fig. 4.

Fig. 4

Open in a new tab

(A) Effect size of repetition suppression. Namely, the standardized difference between activation (averaged parameter estimates within a peristimulus time of 4–10 s) for the first faces and activation for the second faces expressed in ‘SD’ units (Afraz et al., 2006). Error bars represent standard errors. R IOG, right-inferior occipital gyrus (MNI coordinate = [30 −93 −12]); R FG, right fusiform gyrus ([36 −57 −21]); L IFG, left-inferior frontal gyrus ([−51 21 −6]); R PG, right-precentral gyrus ([51 −3 42]). (B) Activation time-courses in the right inferior occipital and fusiform gyri as a function of repetition (F, first faces; S, second faces) and face emotion (NE, neutral faces; AN, angry faces; HA, happy faces).

DISCUSSION

The present study examined whether emotional faces would attenuate repetition suppression compared to neutral faces due to sustained processing. Our results indicate that this is the case for emotionally positive faces, or happy faces. First, significant repetition suppression was observed in extensive regions of ventral visual cortex for neutral faces but not for happy faces. Second, direct comparison revealed that part of the right inferior occipital and fusiform gyri showed significantly less repetition suppression for happy faces than for neutral faces. Third, in those right-ventral visual regions, happy faces showed almost no repetition suppression. On the other hand, attenuation of suppression was not as evident, or intermediate, for angry faces.

The lack of repetition suppression for happy faces in the right-inferior occipital and fusiform regions is of great interest. These ventral visual regions constitute the so-called ‘core system’ for visual analysis of faces (Haxby et al., 2000), and are shown to play an important role in face-identity processing (Winston et al., 2004; Rotshtein et al., 2005). The lack of repetition suppression in these regions suggests prolonged visual encoding of face identity, which is likely to reflect the formation of new representations of unfamiliar faces (Henson et al., 2000). Consistently, D’Argembeau and colleagues showed that happy faces enhanced recollective memory for face identity (D’Argembeau et al., 2003; D’Argembeau and van der Linden, 2007). Although classical models of face recognition have emphasized independent neural pathways for the processing of face identity and face emotion (Bruce and Young, 1986; Haxby et al., 2000), increasing evidence challenges this dichotomy (Calder and Young, 2005; Tsuchiya et al., 2008). Our results also imply the interaction between the two processes such that the identity of a face may be sustainably processed when the face expresses happy emotion.

Sustained neural processing of emotionally positive stimuli is also indicated by Delgado et al. (2000). Using a gambling task, they demonstrated that reward feedback led to prolonged activation in the ventral striatum and the medial temporal region including the amygdala. In the present study, repetition suppression did not reach significance level in the amygdala probably due to its low signal-to-noise ratio (LaBar et al., 2001; Zald, 2003). However, given the modulatory role of the amygdala in face processing (Vuilleumier, 2005), it is likely that sustained amygdala activation to emotionally positive stimuli maintains the activation in ventral visual cortex, resulting in attenuation of repetition suppression. Although repetition suppression has been theorized as reflecting local neural changes (Grill-Spector et al., 2006), such global modulation of repetition suppression would merit further investigation given interaction among distant brain regions during face processing (Vuilleumier, 2005; Fairhall and Ishai, 2007).

As for angry faces, we did not obtain clear evidence for attenuation of repetition suppression as seen for happy faces. While speculative, this might reflect individual variability in sustained processing of emotionally negative stimuli. Fox et al. (2001) reported that attentional dwelling on angry faces was most reliably observed in high-anxious participants. It would thus be interesting to examine the relationship between repetition suppression for angry faces and trait anxiety.

The present study seems incompatible with Ishai et al. (2004), where they found greater repetition suppression for fearful faces than for neutral faces. Both angry and fearful faces are emotionally negative stimuli. The two faces, however, provide different types of threat information (Adams et al., 2003). Whereas an angry face constitutes a direct threat to the observer, a fearful face conveys that a threat is somewhere in the environment. It may thus be adaptive that fearful faces engage repetition suppression as in Ishai et al. (2004) in order to allocate more neural resources to peripheral stimuli, as indicated by a recent behavioral study (Becker, 2009). Another difference between the two studies is the task imposed. Whereas we employed a passive viewing task, Ishai et al. (2004) used a match-to-target task: each trial began with presentation of a target face, followed by serial presentation of 13 faces, during which participants had to respond to the target face. This procedure resulted in distinct cognitive operations between the first presentation (encoding of the target) and the second to later presentations (comparison with the target), which introduced another factor confounding with repetition and hampered a simple interpretation. In fact, Ishai et al. (2004) observed repetition suppression only at the second and third repetitions; the first repetition was associated with even increased activation in some brain regions including the fusiform gyrus. Their findings are in contrast to a number of reports that repetition suppression occurred even at the first repetition (Soon et al., 2003; Rotshtein et al., 2005).

In contrast to the smaller repetition suppression for emotional faces in ventral visual cortex, equivalent suppression regardless of face emotion was observed in part of the left-inferior frontal gyrus and the right-precentral gyrus, which have been shown to play an important role in recognizing face emotion through emotional empathy (Nakamura et al., 1999; Carr et al., 2003; Leslie et al., 2004). Theoretically, detecting changes in facial expression is critical in emotion recognition but not in identity recognition (Bruce and Young, 1986; Haxby et al., 2000). As such, the frontal regions may be more sensitive to detecting whether there are changes in emotional expression in the face stimuli rather than engaging sustained identity processing upon encountering emotional content. Thus, when there is no change in facial expressions across faces, as in our repeated trials, the frontal regions may respond minimally, resulting in repetition suppression for all face emotion conditions. Alternatively, previous studies have shown that frontal activation to face stimuli is the most evident when explicitly judging face emotion (Nakamura et al., 1999; Winston et al., 2003). Then, the possibility is that emotional modulation of repetition suppression would be observed also in frontal regions when an appropriate cognitive task is imposed instead of passive viewing, which remains to be tested in the future research. Nevertheless, our results demonstrate an interesting dissociation between the way frontal and ventral visual regions respond to face repetition within a passive viewing design.

In conclusion, the present study suggests that emotionally positive stimuli maintain sustained neural processing. More specifically, we found that happy faces engaged part of right-ventral visual cortex in a sustained manner evidenced by the lack of repetition suppression. This may be a neural signature of sustained processing of face identity from happy faces, as indicated in the behavioral literature. Future studies would be beneficial to establish a direct link between the neural and behavioral manifestations of such sustained happiness.

Acknowledgments

This work was supported by the National Institute on Aging R01 AGO6265 and R37 AG06265 awarded to D.C.P., and by the Japan Society for the Promotion of Science Research Fellowship for Young Scientists 19-440 awarded to A.S. We thank Susumu Shibui, Ryuta Suzuki, Tomoko Oe, Nobuyuki Watanabe and Norio Koizumi for their help in selecting the stimuli.

Footnotes

1Pictures of Facial Affect, Paul Ekman Group, Oakland, CA, USA; The Karolinska Directed Emotional Faces, Department of Clinical Neuroscience, Karolinska Institutet, Stockholm, Sweden; NimStim Face Stimulus Set, The John D. and Catherine T. MacArthur Foundation Research Network on Early Experience and Brain Development; Facial Information Norm Database, Yamada Laboratory, Department of Psychology, Nihon University, Tokyo, Japan.

2Namely, when making the face-regions mask, we used the contrast of the first faces vs fixation rather than the contrast of the first ‘and’ second faces vs fixation. This was because, due to repetition suppression, the second faces might not activate face-responsive regions and thus because inclusion of the second faces might eliminate normally face-responsive regions.

REFERENCES

  1. Adams RB, Gordon HL, Baird AA, Ambady N, Kleck RE. Effects of gaze on amygdala sensitivity to anger and fear faces. Science. 2003;300:1536. doi: 10.1126/science.1082244. [DOI] [PubMed] [Google Scholar]
  2. Afraz SR, Kiani R, Esteky H. Microstimulation of inferotemporal cortex influences face categorization. Nature. 2006;442:692–5. doi: 10.1038/nature04982. [DOI] [PubMed] [Google Scholar]
  3. Becker MW. Panic search: fear produces efficient visual search for nonthreatening objects. Psychological Science. 2009;20:435–7. doi: 10.1111/j.1467-9280.2009.02303.x. [DOI] [PubMed] [Google Scholar]
  4. Breiter HC, Etcoff NL, Whalen PJ, et al. Response and habituation of the human amygdala during visual processing of facial expression. Neuron. 1996;17:875–87. doi: 10.1016/s0896-6273(00)80219-6. [DOI] [PubMed] [Google Scholar]
  5. Bruce V, Young A. Understanding face recognition. British Journal of Psychology. 1986;77:305–27. doi: 10.1111/j.2044-8295.1986.tb02199.x. [DOI] [PubMed] [Google Scholar]
  6. Calder AJ, Young AW. Understanding the recognition of facial identity and facial expression. Nature Reviews Neuroscience. 2005;6:641–51. doi: 10.1038/nrn1724. [DOI] [PubMed] [Google Scholar]
  7. Carr L, Iacoboni M, Dubeaut MC, Mazziotta JC, Lenzi GL. Neural mechanisms of empathy in humans: a relay from neural systems for imitation to limbic areas. Proceedings of the National Academy of Sciences of the United States of America. 2003;100:5497–502. doi: 10.1073/pnas.0935845100. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. D’Argembeau A, van der Linden M. Facial expressions of emotion influence memory for facial identity in an automatic way. Emotion. 2007;7:507–15. doi: 10.1037/1528-3542.7.3.507. [DOI] [PubMed] [Google Scholar]
  9. D’Argembeau A, van der Linden M, Comblain C, Etienne AM. The effects of happy and angry expressions on identity and expression memory for unfamiliar faces. Cognition & Emotion. 2003;17:609–22. doi: 10.1080/02699930302303. [DOI] [PubMed] [Google Scholar]
  10. Delgado MR, Nystrom LE, Fissell C, Noll DC, Fiez JA. Tracking the hemodynamic responses to reward and punishment in the striatum. Journal of Neurophysiology. 2000;84:3072–7. doi: 10.1152/jn.2000.84.6.3072. [DOI] [PubMed] [Google Scholar]
  11. Fairhall SL, Ishai A. Effective connectivity within the distributed cortical network for face perception. Cerebral Cortex. 2007;17:2400–6. doi: 10.1093/cercor/bhl148. [DOI] [PubMed] [Google Scholar]
  12. Forman SD, Cohen JD, Fitzgerald M, Eddy WF, Mintun MA, Noll DC. Improved assessment of significant activation in functional magnetic-resonance-imaging (fMRI): use of a cluster-size threshold. Magnetic Resonance in Medicine. 1995;33:636–47. doi: 10.1002/mrm.1910330508. [DOI] [PubMed] [Google Scholar]
  13. Fox E, Russo R, Bowles R, Dutton K. Do threatening stimuli draw or hold visual attention in subclinical anxiety? Journal of Experimental Psychology: General. 2001;130:681–700. [PMC free article] [PubMed] [Google Scholar]
  14. Glascher J, Tucher O, Weiller C, Buchel C. Elevated responses to constant facial emotions in different faces in the human amygdala: an fMRI study of facial identity and expression. BMC Neuroscience. 2004;5:45. doi: 10.1186/1471-2202-5-45. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Glover GH, Law CS. Spiral-in/out BOLD fMRI for increased SNR and reduced susceptibility artifacts. Magnetic Resonance in Medicine. 2001;46:515–22. doi: 10.1002/mrm.1222. [DOI] [PubMed] [Google Scholar]
  16. Goh JOS, Siong SC, Park D, Gutchess A, Hebrank A, Chee MWL. Cortical areas involved in object, background, and object background processing revealed with functional magnetic resonance adaptation. Journal of Neuroscience. 2004;24:10223–8. doi: 10.1523/JNEUROSCI.3373-04.2004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Grill-Spector K, Henson R, Martin A. Repetition and the brain: neural models of stimulus-specific effects. Trends in Cognitive Sciences. 2006;10:14–23. doi: 10.1016/j.tics.2005.11.006. [DOI] [PubMed] [Google Scholar]
  18. Gutchess AH, Welsh RC, Boduroglu A, Park DC. Cultural differences in neural function associated with object processing. Cognitive, Affective, & Behavioral Neuroscience. 2006;6:102–9. doi: 10.3758/cabn.6.2.102. [DOI] [PubMed] [Google Scholar]
  19. Hansen CH, Hansen RD. Finding the face in the crowd: an anger superiority effect. Journal of Personality and Social Psychology. 1988;54:917–24. doi: 10.1037//0022-3514.54.6.917. [DOI] [PubMed] [Google Scholar]
  20. Haxby JV, Hoffman EA, Gobbini MI. The distributed human neural system for face perception. Trends in Cognitive Sciences. 2000;4:223–33. doi: 10.1016/s1364-6613(00)01482-0. [DOI] [PubMed] [Google Scholar]
  21. Henson R, Shallice T, Dolan R. Neuroimaging evidence for dissociable forms of repetition priming. Science. 2000;287:1269–72. doi: 10.1126/science.287.5456.1269. [DOI] [PubMed] [Google Scholar]
  22. Henson RNA, Shallice T, Gorno-Tempini ML, Dolan RJ. Face repetition effects in implicit and explicit memory tests as measured by fMRI. Cerebral Cortex. 2002;12:178–86. doi: 10.1093/cercor/12.2.178. [DOI] [PubMed] [Google Scholar]
  23. Ishai A, Pessoa L, Bikle PC, Ungerleider LG. Repetition suppression of faces is modulated by emotion. Proceedings of the National Academy of Sciences of the United States of America. 2004;101:9827–32. doi: 10.1073/pnas.0403559101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Kincade JM, Abrams RA, Astafiev SV, Shulman GL, Corbetta M. An event-related functional magnetic resonance imaging study of voluntary and stimulus-driven orienting of attention. Journal of Neuroscience. 2005;25:4593–604. doi: 10.1523/JNEUROSCI.0236-05.2005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. LaBar KS, Gitelman DR, Mesulam MM, Parrish TB. Impact of signal-to-noise on functional MRI of the human amygdala. Neuroreport. 2001;12:3461–4. doi: 10.1097/00001756-200111160-00017. [DOI] [PubMed] [Google Scholar]
  26. LeDoux J. The Emotional Brain: The Mysterious Underpinnings of Emotional Life. New York: Simon & Schuster Inc; 1996. [Google Scholar]
  27. Leslie KR, Johnson-Frey SH, Grafton ST. Functional imaging of face and hand imitation: towards a motor theory of empathy. Neuroimage. 2004;21:601–7. doi: 10.1016/j.neuroimage.2003.09.038. [DOI] [PubMed] [Google Scholar]
  28. Lieberman MD, Cunningham WA. Type I and Type II error concerns in fMRI research: re-balancing the scale. Social Cognitive and Affective Neuroscience. 2009;4:423–8. doi: 10.1093/scan/nsp052. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Morris JS, Ohman A, Dolan RJ. Conscious and unconscious emotional learning in the human amygdala. Nature. 1998;393:467–70. doi: 10.1038/30976. [DOI] [PubMed] [Google Scholar]
  30. Nakamura K, Kawashima R, Ito K, et al. Activation of the right inferior frontal cortex during assessment of facial emotion. Journal of Neurophysiology. 1999;82:1610–4. doi: 10.1152/jn.1999.82.3.1610. [DOI] [PubMed] [Google Scholar]
  31. Nichols T, Brett M, Andersson J, Wager T, Poline JB. Valid conjunction inference with the minimum statistic. Neuroimage. 2005;25:653–60. doi: 10.1016/j.neuroimage.2004.12.005. [DOI] [PubMed] [Google Scholar]
  32. Ohman A, Lundqvist D, Esteves F. The face in the crowd revisited: a threat advantage with schematic stimuli. Journal of Personality and Social Psychology. 2001;80:381–96. doi: 10.1037/0022-3514.80.3.381. [DOI] [PubMed] [Google Scholar]
  33. Ollinger JM, Shulman GL, Corbetta M. Separating processes within a trial in event-related functional MRI: I The method. Neuroimage. 2001;13:210–7. doi: 10.1006/nimg.2000.0710. [DOI] [PubMed] [Google Scholar]
  34. Rolls ET. Emotion Explained. New York: Oxford University Press; 2005. [Google Scholar]
  35. Rotshtein P, Henson RNA, Treves A, Driver J, Dolan RJ. Morphing Marilyn into Maggie dissociates physical and identity face representations in the brain. Nature Neuroscience. 2005;8:107–13. doi: 10.1038/nn1370. [DOI] [PubMed] [Google Scholar]
  36. Rotshtein P, Malach R, Hadar U, Graif M, Hendler T. Feeling or features: different sensitivity to emotion in high-order visual cortex and amygdala. Neuron. 2001;32:747–57. doi: 10.1016/s0896-6273(01)00513-x. [DOI] [PubMed] [Google Scholar]
  37. Soon CS, Venkatraman V, Chee MWL. Stimulus repetition and hemodynamic response refractoriness in event-related fMRI. Human Brain Mapping. 2003;20:1–12. doi: 10.1002/hbm.10122. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Tsuchiya N, Kawasaki H, Oya H, Howard MA, Adolphs R. Decoding face information in time, frequency and space from direct intracranial recordings of the human brain. PLoS One. 2008;3:e3892. doi: 10.1371/journal.pone.0003892. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Vuilleumier P. How brains beware: neural mechanisms of emotional attention. Trends in Cognitive Sciences. 2005;9:585–94. doi: 10.1016/j.tics.2005.10.011. [DOI] [PubMed] [Google Scholar]
  40. Vuilleumier P, Armony JL, Driver J, Dolan RJ. Effects of attention and emotion on face processing in the human brain: an event-related fMRI study. Neuron. 2001;30:829–41. doi: 10.1016/s0896-6273(01)00328-2. [DOI] [PubMed] [Google Scholar]
  41. Whalen PJ, Rauch SL, Etcoff NL, McInerney SC, Lee MB, Jenike MA. Masked presentations of emotional facial expressions modulate amygdala activity without explicit knowledge. Journal of Neuroscience. 1998;18:411–8. doi: 10.1523/JNEUROSCI.18-01-00411.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Winston JS, Henson RNA, Fine-Goulden MR, Dolan RJ. fMRI-adaptation reveals dissociable neural representations of identity and expression in face perception. Journal of Neurophysiology. 2004;92:1830–9. doi: 10.1152/jn.00155.2004. [DOI] [PubMed] [Google Scholar]
  43. Winston JS, O’Doherty J, Dolan RJ. Common and distinct neural responses during direct and incidental processing of multiple facial emotions. NeuroImage. 2003;20:84–97. doi: 10.1016/s1053-8119(03)00303-3. [DOI] [PubMed] [Google Scholar]
  44. Zald DH. The human amygdala and the emotional evaluation of sensory stimuli. Brain Research Reviews. 2003;41:88–123. doi: 10.1016/s0165-0173(02)00248-5. [DOI] [PubMed] [Google Scholar]

Articles from Social Cognitive and Affective Neuroscience are provided here courtesy of Oxford University Press

RESOURCES