Scandinavian Journal of Psychology, 2014, 55, 533–537
DOI: 10.1111/sjop.12164
Cognition and Neurosciences Reduced repetition suppression in the occipital visual cortex during repeated negative Chinese personality-trait word processing FUQIANG QIAO,1 LI ZHENG,1 LIN LI,1 LEI ZHU2 and QIANFENG WANG3 1
School of Psychology and Cognitive Science, East China Normal University, Shanghai, China Department of Psychology, Fudan University, Shanghai, China 3 Shanghai Key Laboratory of Magnetic Resonance and Department of Physics, East China Normal University, Shanghai, China 2
Qiao, F., Zheng, L., Li, L., Zhu, L. & Wang, Q. (2014). Reduced repetition suppression in the occipital visual cortex during repeated negative Chinese personality-trait word processing. Scandinavian Journal of Psychology 55, 533–537. Reduced neural activation have been consistently observed during repeated items processing, a phenomenon termed repetition suppression. The present study used functional magnetic resonance imaging (fMRI) to investigate whether and how stimuli of emotional valence affects repetition suppression by adopting Chinese personality-trait words as materials. Seventeen participants were required to read the negative and neutral Chinese personality-trait words silently. And then they were presented with repeated and novel items during scanning. Results showed significant repetition suppression in the inferior occipital gyrus only for neutral personality-trait words, whereas similar repetition suppression in the left inferior temporal gyrus and left middle temporal gyrus was revealed for both the word types. These results indicated common and distinct neural substrates during processing Chinese repeated negative and neutral personality-trait words. Key words: Repetition suppression, negative personality-trait word, fMRI. Lin Li, School of Psychology and Cognitive Science, East China Normal University, North Zhongshan Road 3663, Shanghai, SH 200062 China. Tel: 086-021-62231089; fax: 086-021-62233433; e-mail: [email protected]
INTRODUCTION It has been well-documented that identification and classification of an item would be facilitated after a previous encounter with that item. This phenomenon is termed as “repetition priming,” which is characterized by facilitated reaction time and/or accuracy when processing repeated relative to novel items (Race, Shanker & Wagner, 2009; Wig, Granfton, Demos & Kelly, 2005). At the neural level, the performance enhancement during repeated items processing is associated with reduced neural activations in multiple brain regions (i.e., repetition suppression), including the occipital gyrus, fusiform gyrus, inferior- and middle-temporal gyri and prefrontal areas (e.g., Dobbins, Schnyer, Verfaellie & Schacter, 2004; Gotts, Chow & Martin, 2012; Race, et al., 2009; Schacter, Dobbins & Schnyer, 2004; Schacter, Wig & Stevens, 2007; Wig, Buckner & Schacter, 2009). Emotional stimuli are all around us in everyday life. Recently, using emotional faces as materials, several neuroimaging studies have investigated whether and how repetition priming was affected by negative emotion (Bentley, Vuilleumier, Thiel, Driver & Dolan, 2003; Ishai, Pessoa, Bikle & Ungerleider, 2004; Rotshtein, Malach, Hadar, Graif & Hendler, 2001). For example, Ishai and his colleagues (2004) reported greater suppression in the visual cortex, fusiform gyrus, insula and amygdala for processing fearful faces than for neutral faces repeatedly. However, Suzuki, Goh, Hebrank et al. (2011) did not find any activation difference in above-mentioned brain regions when comparing repetition suppression of angry faces with that of neutral faces. The discrepancy of repetition suppression for angry faces and fearful faces indicated that not all negative stimuli shared the same neural basis during their repetition, © 2014 Scandinavian Psychological Associations and John Wiley & Sons Ltd
even though both of them were basic emotions universally recognized by people in various cultures (Ekman & Friesen, 1971). Besides faces, words are also one of the most important means conveying emotional meaning (Luo, Peng, Jin, Duo, Xiao & Ding, 2004). For example, personality-trait words, existing in all human languages, reflect a person’s relatively enduring styles of thinking, feeling and acting (Dixon, 1977). Unlike emotional face, the emotional information which derives from personalitytrait words is more complicated than mere simple basic emotions and constitutes the basis of social interactions, especially negative information. For example, Pratto and Johu (1991) have demonstrated that people are hard to direct attention away from undesirable personality-trait words, even when they were asked to respond to some other aspect of the words, indicating sustained processing of negative personality-trait words. However, there is increasing evidence that different neural mechanisms may underlie the processing of emotional words and faces (e.g., Citron, 2012; Fr€ uhholz, Jellinghaus & Herrmann, 2011; Julian, Marina, Werner & Annekathrin, 2011; Schacht & Sommer, 2009). Thus it is an interesting issue how people will respond when encountered with the negative personality-trait words repeatedly, which is the aim of the present study. A functional MRI study was conducted to explore repetition priming of negative personality-trait words and its underlying neural mechanism. Specifically, participants were presented with repeated negative and neutral personality-trait words which have been studied three times during a previous training phase and novel negative and neutral personality-trait words presented for the first time while scanning. We focus on the comparisons of repetition priming between negative and neutral personalitytrait words.
534 F. Qiao et al. MATERIAL AND METHOD Participants Seventeen right-handed volunteers recruited from the university community with normal or corrected-to-normal vision (12 females, aged from 19 to 26, Mean = 21.41, SD = 2.15) participated in this experiment. None of the participants had a history of neurological or psychiatric disorders. All of them were paid for their participation and gave informed consent before scanning.
Materials A hundred two-character Chinese personality-trait words were selected from Self-Oriented Characteristics Adjectives (Wang & Cui, 2005) as materials. Half of the words were neutral, the remaining half were negative. The emotional valence of the negative words was significantly different from that of neutral words (t(94.85) = 19.47, p < 0.0001). The negative words and neutral words were randomly divided into two parts (25 words for each part) which were counterbalanced for emotional valence. One part served as repeated items which were studied and then tested, and the other part served as novel items which were tested directly. The resulting four types of words (2 repetition (novel vs. repeated) 9 2 emotion (neutral vs. negative)) were also counterbalanced.
Procedure Two phases were included in the experiment, one training phase and one test phase. Before scanning, participants studied a word list containing 25 negative and 25 neutral words three times with a 10s rest between two consecutive presentations of the list. Every time these words would be randomly and individually presented at the center of the screen for 2s, with a fixed inter-stimulus interval (ISI) of 0.5s. Participants were required to read the words silently and then press a button (right index) indicating the response time. Participants were scanned during the test phase. Fifty repeated words which have been studied in the training phase and 50 novel words were presented randomly and individually. The duration of trials and participants’ task were the same as those in the training phase. The experimental trials were intermixed with 2s null trials, during which a black fixation cross was presented. All the trials were presented with jittered inter-stimulus intervals from 0.5~1.5s.
fMRI imaging Imaging was carried out on a 3T Siemens scanner at the Functional MRI Lab (East China Normal University, Shanghai). Functional images were acquired using a gradient echo echo-planar imaging (EPI) sequence (TR = 2200 ms, TE = 30 ms, FOV = 220 mm, matrix size = 64 9 64). Thirty five slices paralleled to the AC–PC line (slice thickness = 3 mm, gap = 0.3 mm) were acquired and covered the whole brain. Before the functional run, a high-resolution structural image was acquired using a T1-weighted, multiplanar reconstruction sequence (MPR) (TR = 1900ms, TE = 3.42 ms, 192 slices, slice thickness = 1 mm, FOV = 256 mm, matrix size = 256 9 256).
fMRI data analysis Data preprocessing and statistical analyses were performed with Statistical Parametric Mapping (SPM8, Welcome Department of Cognitive Neurology, London). Preprocessing included discarding the first five functional images to allow scanner equilibrium effects, rigid-body motion correction, spatial normalization into the MNI space (resampled at 2 9 2 9 2 mm3 voxels), and spatial smoothing (using an 8-mm full-width half maximum isotropic Gaussian kernel). © 2014 Scandinavian Psychological Associations and John Wiley & Sons Ltd
Scand J Psychol 55 (2014) Statistical analyses were performed using the general linear model implemented in SPM8. Trials were classified into four conditions according to emotion and repetition: (1) NegN: novel negative words; (2) NegR: repeated negative words; (3) NeuN: novel neutral words; and (4) NeuR: repeated neutral words. Each trial was modeled using a canonical hemodynamic response function and its temporal derivative according to four conditions. Six regressors modeling movement-related variance and one modeling the overall mean were also employed in the design matrix as covariates of no interest. High pass temporal filtering with a cutoff of 128 seconds was also applied in the models. For each subject at the first-level analysis, simple main effects for four types of conditions were computed by applying the “1 0” contrasts. The four first-level individual contrast images were then analyzed at the second group level by using a flexible factorial design which included an additional subject factor. Finally, F-tests for both main effects (repetition and emotion) and the interaction were computed. A voxel-level threshold of p < 0.0005 (uncorrected) and a spatial extent threshold of k > 20 for multiple comparisons were consistently used throughout the paper. To further test how negative personality-trait words affects brain activations associated with effects of repetition suppression, specific activations identified in the main effect of repetition and the interaction were used to define regions of interest (ROIs). Specifically, all the significant voxels within the 6-mm spherical regions centered on the peak or local maximum coordinates of the activated clusters were included in each ROI. Parameter estimates across ROIs were extracted for further statistics.
RESULTS Behavioral results Mean response times (RTs, restricted to responded items whose RTs are within means 2 standard deviations) were calculated for each type of words. Behavioral priming scores for neutral and negative words were calculated as the average differences in RTs between novel and repeated words respectively. One-sample t-tests revealed a trend toward priming effect for neutral words (t(16) = 1.95, p = 0.069), but not for negative words ( p = 0.52).
fMRI results Main effects of repetition and emotion. The F-test of the main effect of repetition revealed significant activations in the left inferior temporal gyrus, left middle temporal gyrus and left caudate nucleus (Table 1). ROI analyses based on the abovementioned activations were conducted and participants’ beta estimates for four types of words were extracted for all of three ROIs. Two repetition (novel vs. repeated) 9 2 emotion (neutral vs. negative) repeated-measures ANOVAs revealed significant main effects of repetition for all of ROIs (Fs > 10.52, p < 0.01). Specifically, left inferior temporal gyrus and left middle temporal gyrus responded more strongly to novel items than to repeated items, whereas left caudate nucleus responded more strongly to repeated items than to novel items (Fig. 1). The F-test of the main effect of emotion revealed a cluster located in the left precentral gyrus (Table 1). Further analysis revealed that this region responded greater to neutral items than to negative items (F(1,16) = 17.62, p < 0.01, Fig. 1).
INTERACTION BETWEEN REPETITION AND EMOTION The F-test of repetition 9 emotion interaction revealed significant activation in left the inferior occipital gyrus (Table 1).
Brain activities during word repetition 535
Scand J Psychol 55 (2014) Table 1. Regions showing main effects and interaction Peak activation Region
X
Y
Z
F Value
Voxels
Main effect of repetition L Inferior Temporal Gyrus L Middle Temporal Gyrus L Caudate Nucleus
–50 –48 –12
–58 –36 8
–14 4 20
37.76 22.82 17.34
343 23 89
Main effect of emotion L Precentral Gyrus
–46
–2
24
30.47
95
Repetition * emotion interaction L Inferior Occipital Gyrus
–30
–88
–10
20.68
62
Notes: Coordinates (mm) are in MNI space. L = left hemisphere; R = right hemisphere. p < 0.0005 (uncorrected), k > 20.
Further ROI analysis was conducted and participants’ beta estimates for four types of words were extracted. Two repetition (novel vs. repeated) 9 2 emotion (neutral vs. negative) repeatedmeasures ANOVAs revealed a significant interaction between repetition and emotion (F(1,16) = 10.94, p < 0.01, Fig. 1). Followup simple effect analyses revealed that significant repetition suppression in the left inferior occipital gyrus was found only for neutral items (F(1,16) = 15.75, p < 0.01), but not for negative items.
DISCUSSION The present study investigated repetition priming of negative and neutral Chinese personality-trait words using an event-related fMRI design. At the behavioral level, only neutral personalitytrait words showed a trend toward repetition priming. At the
neural level, significant repetition suppression in the left inferior temporal gyrus and left middle temporal gyrus was revealed for both the neutral and negative personality-trait words, whereas significant activation decrease in the left inferior occipital gyrus was observed only for neutral (but not negative) personalitytrait words. Reduced occipital visual cortex activations for repeated relative to novel neutral stimuli have been broadly reported (Buckner, Goodman, Burock et al., 1998; Koutstaal, Wagner, Rotte, Maril, Buckner & Schacter, 2001; Simons, Koutstaal, Prince, Wagner & Schacter, 2003) and interpreted to be associated with facilitated processing of perceptual attributes of the target items (Schacter et al. 2007; Wig et al. 2009). In the present study, consistent with prior findings, neutral items showed significant activation decrease in the inferior occipital cortex, indicating facilitated visual encoding of neutral words. In contrast, no repetition effect was found for negative items in the occipital visual cortex. The lack of repetition suppression for repeated negative items in the occipital visual cortex may be associated with sustained visual encoding of repeated negative relative to repeated neutral stimuli. This view is in line with the finding of Rotshtein et al. (2001), which revealed that negative pictures had a processing advantage, and were more immune to neural adaptation relative to neutral pictures in the repetition priming task. Thus it is not surprising to see similar effects of repetition suppression on negative Chinese words and negative pictures. After the initial visual encoding, information travels from the occipital visual cortex to the inferior temporal cortex for further identification and recognition (known as “ventral stream” or “what pathway”) (Goodale & Milner, 1992; Ungerleider & Haxby, 1994). Though inferior temporal cortex in ventral visual processing stream was considered to be involved in perceptual identification of objects (Goodale & Milner, 1992; Ungerleider
Fig. 1. Significant repetition suppression in the left inferior occipital gyrus was found only for neutral items, but not for negative items. Left inferior temporal gyrus (lITG) and left middle temporal gyrus (lMTG) responded more strongly to novel items than to repeated items, whereas left caudate nucleus (lCN) responded more strongly to repeated items than to novel items. Left precentral gyrus (lPCG) was more active for neutral items than negative items. l = left hemisphere, r = right hemisphere. Error bars indicate s.e.m. © 2014 Scandinavian Psychological Associations and John Wiley & Sons Ltd
536 F. Qiao et al. & Haxby, 1994), repetition suppression in this region was revealed independent of stimulus modality, indicating its role in the amodal processing of abstract or conceptual attributes of the item (Buckner, Koutstaal, Schacter & Rosen, 2000). In our data set, similar repetition suppression in the left inferior temporal gyrus was found for neutral and negative personality-trait words. It should be noted that negative information conveyed by negative personality-trait words was different from angry or fearful faces used widely in previous neuroimaging studies on repetition suppression of negative stimuli (Ishai et al., 2004; Suzuki et al., 2011). Anger or fear signals makes people feel threatened and urges them towards an adaptive response (Adams, Gordon, € Baird, Ambady & Kleck, 2003; Ohman, Lundqvist & Esteves, 2001; Pichon, de Gelder & Grezes, 2009), whereas negative personality-trait words, existing in all human languages (Dixon, 1977), do not directly relate to threats or danger in human evolution. Thus when operating semantic or conceptual attributes after the initial visual perception, we may process negative and neutral personality-trait words similarly, especially when the words used in current study were rather familiar to us, suggesting similar conceptual repetition suppression in the left temporal gyrus for both negative and neutral personality-trait words. This assumption was further supported by the activation in the left middle temporal gyrus. The left middle temporal gyrus has been considered to be engaged in semantic representations (Booth, Burman, Meyer, Gitelman, Parrish & Mesulam, 2002) and repetition suppression in this region has been proved to be invariant to manipulations of decision or stimulus type (Wig et al., 2009). Significant activation decreased in the left middle temporal gyrus for negative and neutral personality-trait words observed in the present study may suggest facilitated amodal processing of abstract or semantic features of both the word types. Additionally, compared to novel words, repeated personalitytrait words showed greater activation in the caudate nucleus. Caudate nucleus activation has been argued to be associated with the acquisition of rules and knowledge (Gheysen, Van Opstal, Roggeman, Van Waelvelde & Fias, 2011; Lieberman, Chang, Chiao, Bookheimer & Knowlton, 2004; Rose, Haider, Salari & B€ uchel, 2011). Greater activation in the caudate nucleus for repeated personality-trait words may indicate facilitated processing when encountering with stimuli repeatedly from another perspective.
CONCLUSION The present study investigated the repetition priming of negative and neutral Chinese personality-trait words and the underlying neural basis. At the behavioral level, a trend toward repetition priming effect was only found for neutral but not negative personality-trait words. At the neural level, significant activation decrease in the left inferior occipital gyrus was observed only for neutral (but not negative) personality-trait words, whereas significant repetition suppression in the left inferior temporal gyrus and left middle temporal gyrus was revealed for both neutral and negative personality-trait words, indicating common and distinct neural substrates underlying repetition suppression of negative and neutral Chinese personalitytrait words. © 2014 Scandinavian Psychological Associations and John Wiley & Sons Ltd
Scand J Psychol 55 (2014)
This research was supported by National Natural Science Foundation of China (31271090), Key Project Foundation for Research and Innovation of Shanghai Municipal Education Commission (12ZS046). Fuqiang Qiao and Li Zheng contributed equally to this work.
REFERENCES Adams, R. B., Gordon, H. L., Baird, A. A., Ambady, N. & Kleck, R. E. (2003). Effects of gaze on amygdala sensitivity to anger and fear faces. Science, 300, 1536. Bentley, P., Vuilleumier, P., Thiel, C. M., Driver, J. & Dolan, R. J. (2003). Effects of attention and emotion on repetition priming and their modulation by cholinergic enhancement. Journal of Neurophysiology, 90, 1171–1181. Booth, J. R., Burman, D. D., Meyer, J. R., Gitelman, D. R., Parrish, T. B. & Mesulam, M. (2002). Modality independence of word comprehension. Human Brain Mapping, 16, 251–261. Buckner, R. L., Goodman, J., Burock, M., Rotte, M., Koutstaal, W., Schacter, D., et al. (1998). Functional-anatomic correlates of object priming in humans revealed by rapid presentation event-related fMRI. Neuron, 20, 285–296. Buckner, R. L., Koutstaal, W., Schacter, D. L. & Rosen, B. R. (2000). Functional MRI evidence for a role of frontal and inferior temporal cortex in amodal components of priming. Brain, 123, 620–640. Citron, F. M. (2012). Neural correlates of written emotion word processing: A review of recent electrophysiological and hemodynamic neuroimaging studies. Brain and Language, 122, 211–226. Dixon, R. M. W. (1977). Where have all the adjectives gone? Studies in Language, 1, 19–80. Dobbins, I. G., Schnyer, D. M., Verfaellie, M. & Schacter, D. L. (2004). Cortical activity reductions during repetition priming can result from rapid response learning. Nature, 428, 316–319. Ekman, P. & Friesen, W. V. (1971). Constants across cultures in the face and emotion. Journal of Personality and Social Psychology, 17, 124–129. Fr€ uhholz, S., Jellinghaus, A. & Herrmann, M. (2011). Time course of implicit processing and explicit processing of emotional faces and emotional words. Biological Psychology, 87, 265–274. Gheysen, F., Van Opstal, F., Roggeman, C., Van Waelvelde, H. & Fias, W. (2011). The neural basis of implicit perceptual sequence learning. Frontiers in Human Neuroscience, 5, 1–12. Goodale, M. A. & Milner, A. D. (1992). Separate visual pathways for perception and action. Trends in Neurosciences, 15, 20–25. Gotts, S. J., Chow, C. C. & Martin, A. (2012). Repetition priming and repetition suppression: A case for enhanced efficiency through neural synchronization. Cognitive Neuroscience, 3, 227–237. Ishai, A., Pessoa, L., Bikle, P. C. & Ungerleider, L. G. (2004). Repetition suppression of faces is modulated by emotion. Proceedings of the National Academy of Sciences of the United States of America, 101, 9827–9832. Julian, R., Marina, P., Werner, S. & Annekathrin, S. (2011). On the automaticity of emotion processing in words and faces: Event-related brain potentials evidence from a superficial task. Brian and Cognition, 77, 23–32. Koutstaal, W., Wagner, A. D., Rotte, M., Maril, A., Buckner, R. L. & Schacter, D. L. (2001). Perceptual specificity in visual object priming: Functional magnetic resonance imaging evidence for a laterality difference in fusiform cortex. Neuropsychologia, 39, 184–199. Lieberman, M. D., Chang, G. Y., Chiao, J., Bookheimer, S. Y. & Knowlton, B. J. (2004). An event-related fMRI study of artificial grammar learning in a balanced chunk strength design. Journal of Cognitive Neuroscience, 16, 427–438. Luo, Q., Peng, D., Jin, Z., Duo, X., Xiao, L. & Ding, G. (2004). Emotional valence of words modulates the subliminal repetition priming effect in the left fusiform gyrus: An event-related fMRI study. NeuroImage, 21, 414–421.
Scand J Psychol 55 (2014) € Ohman, A., Lundqvist, D. & Esteves, F. (2001). The face in the crowd revisited: A threat advantage with schematic stimuli. Journal of Personality and Social Psychology, 80, 381–396. Pichon, S., de Gelder, B. & Grezes, J. (2009). Two different faces of threat. Comparing the neural systems for recognizing fear and anger in dynamic body expressions. Neuroimage, 47, 1873–1883. Pratto, F. & Johu, O. P. (1991). Automatic vigilance: The attentiongrabbing power of negative social information. Journal of Personality and Social Psychology, 61, 380–391. Race, E. A., Shanker, S. & Wagner, A. D. (2009). Neural priming in human frontal cortex: Multiple forms of learning reduce demands on the prefrontal executive system. Journal of Cognitive Neuroscience, 21(9), 1766–1781. Rose, M., Haider, H., Salari, N. & B€uchel, C. (2011). Functional dissociation of hippocampal mechanism during implicit learning based on the domain of associations. The Journal of Neuroscience, 31, 13739–13745. Rotshtein, P., Malach, R., Hadar, U., Graif, M. & Hendler, T. (2001). Feeling or features: Different sensitivity to emotion in high-order visual cortex and amygdala. Neuron, 32, 747–757. Schacht, A. & Sommer, W. (2009). Emotions in word and face processing: Early and late cortical responses. Brain and cognition, 69, 538–550. Schacter, D. L., Dobbins, I. G. & Schnyer, D. M. (2004). Specificity of priming: A cognitive neuroscience perspective. Nature Reviews Neuroscience, 5, 853–862.
© 2014 Scandinavian Psychological Associations and John Wiley & Sons Ltd
Brain activities during word repetition 537 Schacter, D. L., Wig, G. S. & Stevens, W. D. (2007). Reductions in cortical activity during priming. Current Opinion in Neurobiology, 17, 171–176. Simons, J. S., Koutstaal, W., Prince, S., Wagner, A. D. & Schacter, D. L. (2003). Neural mechanisms of visual object priming: Evidence for perceptual and semantic distinctions in fusiform cortex. Neuroimage, 19, 613–626. Suzuki, A., Goh, J. O. S., Hebrank, A., Sutton, B., Jenkins, L., Flicker, B. & Park, D. C. (2011). Sustained happiness? Lack of repetition suppression in right ventral visual cortex for happy faces. Social, Cognitive and Affective Neuroscience, 6, 434–441. Ungerleider, L. G. & Haxby, J. V. (1994). ‘What’ and ‘where’ in the human brain. Current Opinion in Neurobiology, 4, 157–165. Wang, D & Cui, H. (2005). Explorations of Chinese personality. Beijing, China: Social Sciences Digest Press (in Chinese). Wig, G. S., Buckner, R. L. & Schacter, D. L. (2009). Repetition priming influences distinct brain systems: Evidence from task-evoked data and resting-state correlations. Journal of Neurophysiology, 101, 2632–2648. Wig, G. S., Grafton, S. T., Demos, K. E. & Kelley, W. M. (2005). Reductions in neural activity underlie behavioral components of repetition priming. Nature Neuroscience, 8, 1228–1233. Received 22 February 2014, accepted 27 July 2014
Copyright of Scandinavian Journal of Psychology is the property of Wiley-Blackwell and its content may not be copied or emailed to multiple sites or posted to a listserv without the copyright holder's express written permission. However, users may print, download, or email articles for individual use.
DOI: 10.1111/sjop.12164
Cognition and Neurosciences Reduced repetition suppression in the occipital visual cortex during repeated negative Chinese personality-trait word processing FUQIANG QIAO,1 LI ZHENG,1 LIN LI,1 LEI ZHU2 and QIANFENG WANG3 1
School of Psychology and Cognitive Science, East China Normal University, Shanghai, China Department of Psychology, Fudan University, Shanghai, China 3 Shanghai Key Laboratory of Magnetic Resonance and Department of Physics, East China Normal University, Shanghai, China 2
Qiao, F., Zheng, L., Li, L., Zhu, L. & Wang, Q. (2014). Reduced repetition suppression in the occipital visual cortex during repeated negative Chinese personality-trait word processing. Scandinavian Journal of Psychology 55, 533–537. Reduced neural activation have been consistently observed during repeated items processing, a phenomenon termed repetition suppression. The present study used functional magnetic resonance imaging (fMRI) to investigate whether and how stimuli of emotional valence affects repetition suppression by adopting Chinese personality-trait words as materials. Seventeen participants were required to read the negative and neutral Chinese personality-trait words silently. And then they were presented with repeated and novel items during scanning. Results showed significant repetition suppression in the inferior occipital gyrus only for neutral personality-trait words, whereas similar repetition suppression in the left inferior temporal gyrus and left middle temporal gyrus was revealed for both the word types. These results indicated common and distinct neural substrates during processing Chinese repeated negative and neutral personality-trait words. Key words: Repetition suppression, negative personality-trait word, fMRI. Lin Li, School of Psychology and Cognitive Science, East China Normal University, North Zhongshan Road 3663, Shanghai, SH 200062 China. Tel: 086-021-62231089; fax: 086-021-62233433; e-mail: [email protected]
INTRODUCTION It has been well-documented that identification and classification of an item would be facilitated after a previous encounter with that item. This phenomenon is termed as “repetition priming,” which is characterized by facilitated reaction time and/or accuracy when processing repeated relative to novel items (Race, Shanker & Wagner, 2009; Wig, Granfton, Demos & Kelly, 2005). At the neural level, the performance enhancement during repeated items processing is associated with reduced neural activations in multiple brain regions (i.e., repetition suppression), including the occipital gyrus, fusiform gyrus, inferior- and middle-temporal gyri and prefrontal areas (e.g., Dobbins, Schnyer, Verfaellie & Schacter, 2004; Gotts, Chow & Martin, 2012; Race, et al., 2009; Schacter, Dobbins & Schnyer, 2004; Schacter, Wig & Stevens, 2007; Wig, Buckner & Schacter, 2009). Emotional stimuli are all around us in everyday life. Recently, using emotional faces as materials, several neuroimaging studies have investigated whether and how repetition priming was affected by negative emotion (Bentley, Vuilleumier, Thiel, Driver & Dolan, 2003; Ishai, Pessoa, Bikle & Ungerleider, 2004; Rotshtein, Malach, Hadar, Graif & Hendler, 2001). For example, Ishai and his colleagues (2004) reported greater suppression in the visual cortex, fusiform gyrus, insula and amygdala for processing fearful faces than for neutral faces repeatedly. However, Suzuki, Goh, Hebrank et al. (2011) did not find any activation difference in above-mentioned brain regions when comparing repetition suppression of angry faces with that of neutral faces. The discrepancy of repetition suppression for angry faces and fearful faces indicated that not all negative stimuli shared the same neural basis during their repetition, © 2014 Scandinavian Psychological Associations and John Wiley & Sons Ltd
even though both of them were basic emotions universally recognized by people in various cultures (Ekman & Friesen, 1971). Besides faces, words are also one of the most important means conveying emotional meaning (Luo, Peng, Jin, Duo, Xiao & Ding, 2004). For example, personality-trait words, existing in all human languages, reflect a person’s relatively enduring styles of thinking, feeling and acting (Dixon, 1977). Unlike emotional face, the emotional information which derives from personalitytrait words is more complicated than mere simple basic emotions and constitutes the basis of social interactions, especially negative information. For example, Pratto and Johu (1991) have demonstrated that people are hard to direct attention away from undesirable personality-trait words, even when they were asked to respond to some other aspect of the words, indicating sustained processing of negative personality-trait words. However, there is increasing evidence that different neural mechanisms may underlie the processing of emotional words and faces (e.g., Citron, 2012; Fr€ uhholz, Jellinghaus & Herrmann, 2011; Julian, Marina, Werner & Annekathrin, 2011; Schacht & Sommer, 2009). Thus it is an interesting issue how people will respond when encountered with the negative personality-trait words repeatedly, which is the aim of the present study. A functional MRI study was conducted to explore repetition priming of negative personality-trait words and its underlying neural mechanism. Specifically, participants were presented with repeated negative and neutral personality-trait words which have been studied three times during a previous training phase and novel negative and neutral personality-trait words presented for the first time while scanning. We focus on the comparisons of repetition priming between negative and neutral personalitytrait words.
534 F. Qiao et al. MATERIAL AND METHOD Participants Seventeen right-handed volunteers recruited from the university community with normal or corrected-to-normal vision (12 females, aged from 19 to 26, Mean = 21.41, SD = 2.15) participated in this experiment. None of the participants had a history of neurological or psychiatric disorders. All of them were paid for their participation and gave informed consent before scanning.
Materials A hundred two-character Chinese personality-trait words were selected from Self-Oriented Characteristics Adjectives (Wang & Cui, 2005) as materials. Half of the words were neutral, the remaining half were negative. The emotional valence of the negative words was significantly different from that of neutral words (t(94.85) = 19.47, p < 0.0001). The negative words and neutral words were randomly divided into two parts (25 words for each part) which were counterbalanced for emotional valence. One part served as repeated items which were studied and then tested, and the other part served as novel items which were tested directly. The resulting four types of words (2 repetition (novel vs. repeated) 9 2 emotion (neutral vs. negative)) were also counterbalanced.
Procedure Two phases were included in the experiment, one training phase and one test phase. Before scanning, participants studied a word list containing 25 negative and 25 neutral words three times with a 10s rest between two consecutive presentations of the list. Every time these words would be randomly and individually presented at the center of the screen for 2s, with a fixed inter-stimulus interval (ISI) of 0.5s. Participants were required to read the words silently and then press a button (right index) indicating the response time. Participants were scanned during the test phase. Fifty repeated words which have been studied in the training phase and 50 novel words were presented randomly and individually. The duration of trials and participants’ task were the same as those in the training phase. The experimental trials were intermixed with 2s null trials, during which a black fixation cross was presented. All the trials were presented with jittered inter-stimulus intervals from 0.5~1.5s.
fMRI imaging Imaging was carried out on a 3T Siemens scanner at the Functional MRI Lab (East China Normal University, Shanghai). Functional images were acquired using a gradient echo echo-planar imaging (EPI) sequence (TR = 2200 ms, TE = 30 ms, FOV = 220 mm, matrix size = 64 9 64). Thirty five slices paralleled to the AC–PC line (slice thickness = 3 mm, gap = 0.3 mm) were acquired and covered the whole brain. Before the functional run, a high-resolution structural image was acquired using a T1-weighted, multiplanar reconstruction sequence (MPR) (TR = 1900ms, TE = 3.42 ms, 192 slices, slice thickness = 1 mm, FOV = 256 mm, matrix size = 256 9 256).
fMRI data analysis Data preprocessing and statistical analyses were performed with Statistical Parametric Mapping (SPM8, Welcome Department of Cognitive Neurology, London). Preprocessing included discarding the first five functional images to allow scanner equilibrium effects, rigid-body motion correction, spatial normalization into the MNI space (resampled at 2 9 2 9 2 mm3 voxels), and spatial smoothing (using an 8-mm full-width half maximum isotropic Gaussian kernel). © 2014 Scandinavian Psychological Associations and John Wiley & Sons Ltd
Scand J Psychol 55 (2014) Statistical analyses were performed using the general linear model implemented in SPM8. Trials were classified into four conditions according to emotion and repetition: (1) NegN: novel negative words; (2) NegR: repeated negative words; (3) NeuN: novel neutral words; and (4) NeuR: repeated neutral words. Each trial was modeled using a canonical hemodynamic response function and its temporal derivative according to four conditions. Six regressors modeling movement-related variance and one modeling the overall mean were also employed in the design matrix as covariates of no interest. High pass temporal filtering with a cutoff of 128 seconds was also applied in the models. For each subject at the first-level analysis, simple main effects for four types of conditions were computed by applying the “1 0” contrasts. The four first-level individual contrast images were then analyzed at the second group level by using a flexible factorial design which included an additional subject factor. Finally, F-tests for both main effects (repetition and emotion) and the interaction were computed. A voxel-level threshold of p < 0.0005 (uncorrected) and a spatial extent threshold of k > 20 for multiple comparisons were consistently used throughout the paper. To further test how negative personality-trait words affects brain activations associated with effects of repetition suppression, specific activations identified in the main effect of repetition and the interaction were used to define regions of interest (ROIs). Specifically, all the significant voxels within the 6-mm spherical regions centered on the peak or local maximum coordinates of the activated clusters were included in each ROI. Parameter estimates across ROIs were extracted for further statistics.
RESULTS Behavioral results Mean response times (RTs, restricted to responded items whose RTs are within means 2 standard deviations) were calculated for each type of words. Behavioral priming scores for neutral and negative words were calculated as the average differences in RTs between novel and repeated words respectively. One-sample t-tests revealed a trend toward priming effect for neutral words (t(16) = 1.95, p = 0.069), but not for negative words ( p = 0.52).
fMRI results Main effects of repetition and emotion. The F-test of the main effect of repetition revealed significant activations in the left inferior temporal gyrus, left middle temporal gyrus and left caudate nucleus (Table 1). ROI analyses based on the abovementioned activations were conducted and participants’ beta estimates for four types of words were extracted for all of three ROIs. Two repetition (novel vs. repeated) 9 2 emotion (neutral vs. negative) repeated-measures ANOVAs revealed significant main effects of repetition for all of ROIs (Fs > 10.52, p < 0.01). Specifically, left inferior temporal gyrus and left middle temporal gyrus responded more strongly to novel items than to repeated items, whereas left caudate nucleus responded more strongly to repeated items than to novel items (Fig. 1). The F-test of the main effect of emotion revealed a cluster located in the left precentral gyrus (Table 1). Further analysis revealed that this region responded greater to neutral items than to negative items (F(1,16) = 17.62, p < 0.01, Fig. 1).
INTERACTION BETWEEN REPETITION AND EMOTION The F-test of repetition 9 emotion interaction revealed significant activation in left the inferior occipital gyrus (Table 1).
Brain activities during word repetition 535
Scand J Psychol 55 (2014) Table 1. Regions showing main effects and interaction Peak activation Region
X
Y
Z
F Value
Voxels
Main effect of repetition L Inferior Temporal Gyrus L Middle Temporal Gyrus L Caudate Nucleus
–50 –48 –12
–58 –36 8
–14 4 20
37.76 22.82 17.34
343 23 89
Main effect of emotion L Precentral Gyrus
–46
–2
24
30.47
95
Repetition * emotion interaction L Inferior Occipital Gyrus
–30
–88
–10
20.68
62
Notes: Coordinates (mm) are in MNI space. L = left hemisphere; R = right hemisphere. p < 0.0005 (uncorrected), k > 20.
Further ROI analysis was conducted and participants’ beta estimates for four types of words were extracted. Two repetition (novel vs. repeated) 9 2 emotion (neutral vs. negative) repeatedmeasures ANOVAs revealed a significant interaction between repetition and emotion (F(1,16) = 10.94, p < 0.01, Fig. 1). Followup simple effect analyses revealed that significant repetition suppression in the left inferior occipital gyrus was found only for neutral items (F(1,16) = 15.75, p < 0.01), but not for negative items.
DISCUSSION The present study investigated repetition priming of negative and neutral Chinese personality-trait words using an event-related fMRI design. At the behavioral level, only neutral personalitytrait words showed a trend toward repetition priming. At the
neural level, significant repetition suppression in the left inferior temporal gyrus and left middle temporal gyrus was revealed for both the neutral and negative personality-trait words, whereas significant activation decrease in the left inferior occipital gyrus was observed only for neutral (but not negative) personalitytrait words. Reduced occipital visual cortex activations for repeated relative to novel neutral stimuli have been broadly reported (Buckner, Goodman, Burock et al., 1998; Koutstaal, Wagner, Rotte, Maril, Buckner & Schacter, 2001; Simons, Koutstaal, Prince, Wagner & Schacter, 2003) and interpreted to be associated with facilitated processing of perceptual attributes of the target items (Schacter et al. 2007; Wig et al. 2009). In the present study, consistent with prior findings, neutral items showed significant activation decrease in the inferior occipital cortex, indicating facilitated visual encoding of neutral words. In contrast, no repetition effect was found for negative items in the occipital visual cortex. The lack of repetition suppression for repeated negative items in the occipital visual cortex may be associated with sustained visual encoding of repeated negative relative to repeated neutral stimuli. This view is in line with the finding of Rotshtein et al. (2001), which revealed that negative pictures had a processing advantage, and were more immune to neural adaptation relative to neutral pictures in the repetition priming task. Thus it is not surprising to see similar effects of repetition suppression on negative Chinese words and negative pictures. After the initial visual encoding, information travels from the occipital visual cortex to the inferior temporal cortex for further identification and recognition (known as “ventral stream” or “what pathway”) (Goodale & Milner, 1992; Ungerleider & Haxby, 1994). Though inferior temporal cortex in ventral visual processing stream was considered to be involved in perceptual identification of objects (Goodale & Milner, 1992; Ungerleider
Fig. 1. Significant repetition suppression in the left inferior occipital gyrus was found only for neutral items, but not for negative items. Left inferior temporal gyrus (lITG) and left middle temporal gyrus (lMTG) responded more strongly to novel items than to repeated items, whereas left caudate nucleus (lCN) responded more strongly to repeated items than to novel items. Left precentral gyrus (lPCG) was more active for neutral items than negative items. l = left hemisphere, r = right hemisphere. Error bars indicate s.e.m. © 2014 Scandinavian Psychological Associations and John Wiley & Sons Ltd
536 F. Qiao et al. & Haxby, 1994), repetition suppression in this region was revealed independent of stimulus modality, indicating its role in the amodal processing of abstract or conceptual attributes of the item (Buckner, Koutstaal, Schacter & Rosen, 2000). In our data set, similar repetition suppression in the left inferior temporal gyrus was found for neutral and negative personality-trait words. It should be noted that negative information conveyed by negative personality-trait words was different from angry or fearful faces used widely in previous neuroimaging studies on repetition suppression of negative stimuli (Ishai et al., 2004; Suzuki et al., 2011). Anger or fear signals makes people feel threatened and urges them towards an adaptive response (Adams, Gordon, € Baird, Ambady & Kleck, 2003; Ohman, Lundqvist & Esteves, 2001; Pichon, de Gelder & Grezes, 2009), whereas negative personality-trait words, existing in all human languages (Dixon, 1977), do not directly relate to threats or danger in human evolution. Thus when operating semantic or conceptual attributes after the initial visual perception, we may process negative and neutral personality-trait words similarly, especially when the words used in current study were rather familiar to us, suggesting similar conceptual repetition suppression in the left temporal gyrus for both negative and neutral personality-trait words. This assumption was further supported by the activation in the left middle temporal gyrus. The left middle temporal gyrus has been considered to be engaged in semantic representations (Booth, Burman, Meyer, Gitelman, Parrish & Mesulam, 2002) and repetition suppression in this region has been proved to be invariant to manipulations of decision or stimulus type (Wig et al., 2009). Significant activation decreased in the left middle temporal gyrus for negative and neutral personality-trait words observed in the present study may suggest facilitated amodal processing of abstract or semantic features of both the word types. Additionally, compared to novel words, repeated personalitytrait words showed greater activation in the caudate nucleus. Caudate nucleus activation has been argued to be associated with the acquisition of rules and knowledge (Gheysen, Van Opstal, Roggeman, Van Waelvelde & Fias, 2011; Lieberman, Chang, Chiao, Bookheimer & Knowlton, 2004; Rose, Haider, Salari & B€ uchel, 2011). Greater activation in the caudate nucleus for repeated personality-trait words may indicate facilitated processing when encountering with stimuli repeatedly from another perspective.
CONCLUSION The present study investigated the repetition priming of negative and neutral Chinese personality-trait words and the underlying neural basis. At the behavioral level, a trend toward repetition priming effect was only found for neutral but not negative personality-trait words. At the neural level, significant activation decrease in the left inferior occipital gyrus was observed only for neutral (but not negative) personality-trait words, whereas significant repetition suppression in the left inferior temporal gyrus and left middle temporal gyrus was revealed for both neutral and negative personality-trait words, indicating common and distinct neural substrates underlying repetition suppression of negative and neutral Chinese personalitytrait words. © 2014 Scandinavian Psychological Associations and John Wiley & Sons Ltd
Scand J Psychol 55 (2014)
This research was supported by National Natural Science Foundation of China (31271090), Key Project Foundation for Research and Innovation of Shanghai Municipal Education Commission (12ZS046). Fuqiang Qiao and Li Zheng contributed equally to this work.
REFERENCES Adams, R. B., Gordon, H. L., Baird, A. A., Ambady, N. & Kleck, R. E. (2003). Effects of gaze on amygdala sensitivity to anger and fear faces. Science, 300, 1536. Bentley, P., Vuilleumier, P., Thiel, C. M., Driver, J. & Dolan, R. J. (2003). Effects of attention and emotion on repetition priming and their modulation by cholinergic enhancement. Journal of Neurophysiology, 90, 1171–1181. Booth, J. R., Burman, D. D., Meyer, J. R., Gitelman, D. R., Parrish, T. B. & Mesulam, M. (2002). Modality independence of word comprehension. Human Brain Mapping, 16, 251–261. Buckner, R. L., Goodman, J., Burock, M., Rotte, M., Koutstaal, W., Schacter, D., et al. (1998). Functional-anatomic correlates of object priming in humans revealed by rapid presentation event-related fMRI. Neuron, 20, 285–296. Buckner, R. L., Koutstaal, W., Schacter, D. L. & Rosen, B. R. (2000). Functional MRI evidence for a role of frontal and inferior temporal cortex in amodal components of priming. Brain, 123, 620–640. Citron, F. M. (2012). Neural correlates of written emotion word processing: A review of recent electrophysiological and hemodynamic neuroimaging studies. Brain and Language, 122, 211–226. Dixon, R. M. W. (1977). Where have all the adjectives gone? Studies in Language, 1, 19–80. Dobbins, I. G., Schnyer, D. M., Verfaellie, M. & Schacter, D. L. (2004). Cortical activity reductions during repetition priming can result from rapid response learning. Nature, 428, 316–319. Ekman, P. & Friesen, W. V. (1971). Constants across cultures in the face and emotion. Journal of Personality and Social Psychology, 17, 124–129. Fr€ uhholz, S., Jellinghaus, A. & Herrmann, M. (2011). Time course of implicit processing and explicit processing of emotional faces and emotional words. Biological Psychology, 87, 265–274. Gheysen, F., Van Opstal, F., Roggeman, C., Van Waelvelde, H. & Fias, W. (2011). The neural basis of implicit perceptual sequence learning. Frontiers in Human Neuroscience, 5, 1–12. Goodale, M. A. & Milner, A. D. (1992). Separate visual pathways for perception and action. Trends in Neurosciences, 15, 20–25. Gotts, S. J., Chow, C. C. & Martin, A. (2012). Repetition priming and repetition suppression: A case for enhanced efficiency through neural synchronization. Cognitive Neuroscience, 3, 227–237. Ishai, A., Pessoa, L., Bikle, P. C. & Ungerleider, L. G. (2004). Repetition suppression of faces is modulated by emotion. Proceedings of the National Academy of Sciences of the United States of America, 101, 9827–9832. Julian, R., Marina, P., Werner, S. & Annekathrin, S. (2011). On the automaticity of emotion processing in words and faces: Event-related brain potentials evidence from a superficial task. Brian and Cognition, 77, 23–32. Koutstaal, W., Wagner, A. D., Rotte, M., Maril, A., Buckner, R. L. & Schacter, D. L. (2001). Perceptual specificity in visual object priming: Functional magnetic resonance imaging evidence for a laterality difference in fusiform cortex. Neuropsychologia, 39, 184–199. Lieberman, M. D., Chang, G. Y., Chiao, J., Bookheimer, S. Y. & Knowlton, B. J. (2004). An event-related fMRI study of artificial grammar learning in a balanced chunk strength design. Journal of Cognitive Neuroscience, 16, 427–438. Luo, Q., Peng, D., Jin, Z., Duo, X., Xiao, L. & Ding, G. (2004). Emotional valence of words modulates the subliminal repetition priming effect in the left fusiform gyrus: An event-related fMRI study. NeuroImage, 21, 414–421.
Scand J Psychol 55 (2014) € Ohman, A., Lundqvist, D. & Esteves, F. (2001). The face in the crowd revisited: A threat advantage with schematic stimuli. Journal of Personality and Social Psychology, 80, 381–396. Pichon, S., de Gelder, B. & Grezes, J. (2009). Two different faces of threat. Comparing the neural systems for recognizing fear and anger in dynamic body expressions. Neuroimage, 47, 1873–1883. Pratto, F. & Johu, O. P. (1991). Automatic vigilance: The attentiongrabbing power of negative social information. Journal of Personality and Social Psychology, 61, 380–391. Race, E. A., Shanker, S. & Wagner, A. D. (2009). Neural priming in human frontal cortex: Multiple forms of learning reduce demands on the prefrontal executive system. Journal of Cognitive Neuroscience, 21(9), 1766–1781. Rose, M., Haider, H., Salari, N. & B€uchel, C. (2011). Functional dissociation of hippocampal mechanism during implicit learning based on the domain of associations. The Journal of Neuroscience, 31, 13739–13745. Rotshtein, P., Malach, R., Hadar, U., Graif, M. & Hendler, T. (2001). Feeling or features: Different sensitivity to emotion in high-order visual cortex and amygdala. Neuron, 32, 747–757. Schacht, A. & Sommer, W. (2009). Emotions in word and face processing: Early and late cortical responses. Brain and cognition, 69, 538–550. Schacter, D. L., Dobbins, I. G. & Schnyer, D. M. (2004). Specificity of priming: A cognitive neuroscience perspective. Nature Reviews Neuroscience, 5, 853–862.
© 2014 Scandinavian Psychological Associations and John Wiley & Sons Ltd
Brain activities during word repetition 537 Schacter, D. L., Wig, G. S. & Stevens, W. D. (2007). Reductions in cortical activity during priming. Current Opinion in Neurobiology, 17, 171–176. Simons, J. S., Koutstaal, W., Prince, S., Wagner, A. D. & Schacter, D. L. (2003). Neural mechanisms of visual object priming: Evidence for perceptual and semantic distinctions in fusiform cortex. Neuroimage, 19, 613–626. Suzuki, A., Goh, J. O. S., Hebrank, A., Sutton, B., Jenkins, L., Flicker, B. & Park, D. C. (2011). Sustained happiness? Lack of repetition suppression in right ventral visual cortex for happy faces. Social, Cognitive and Affective Neuroscience, 6, 434–441. Ungerleider, L. G. & Haxby, J. V. (1994). ‘What’ and ‘where’ in the human brain. Current Opinion in Neurobiology, 4, 157–165. Wang, D & Cui, H. (2005). Explorations of Chinese personality. Beijing, China: Social Sciences Digest Press (in Chinese). Wig, G. S., Buckner, R. L. & Schacter, D. L. (2009). Repetition priming influences distinct brain systems: Evidence from task-evoked data and resting-state correlations. Journal of Neurophysiology, 101, 2632–2648. Wig, G. S., Grafton, S. T., Demos, K. E. & Kelley, W. M. (2005). Reductions in neural activity underlie behavioral components of repetition priming. Nature Neuroscience, 8, 1228–1233. Received 22 February 2014, accepted 27 July 2014
Copyright of Scandinavian Journal of Psychology is the property of Wiley-Blackwell and its content may not be copied or emailed to multiple sites or posted to a listserv without the copyright holder's express written permission. However, users may print, download, or email articles for individual use.
