- Email: [email protected]
False recognition of emotional stimuli is lateralised in the brain: An fMRI study
Available online at www.sciencedirect.com
Neurobiology of Learning and Memory 90 (2008) 280–284 www.elsevier.com/locate/ynlme
Brief Report
False recognition of emotional stimuli is lateralised in the brain: An fMRI study A. Marchewka a,*, A. Brechmann b, A. Nowicka a, K. Jednoro´g a, H. Scheich b, A. Grabowska a a
Nencki Institute of Experimental Biology, Department of Neurophysiology, Laboratory of Psychophysiology, 3 Pasteur Street, 02-093 Warsaw, Poland b Leibniz Institute for Neurobiology, Non-Invasive Brain Imaging, Magdeburg, Germany Received 19 November 2007; revised 29 January 2008; accepted 29 January 2008 Available online 7 March 2008
Abstract We have investigated whether the left (LH) and right (RH) hemisphere play a different role in eliciting false recognition (FR) and whether their involvement in this memory illusion depends on the emotional content of stimuli. Negative and neutral pictures (taken from IAPS) were presented in the divided-visual field paradigm. Subjects task was to indicate whether the pictures had already been presented or not during the preceding study phase. FR rate was much higher for the RH than the LH presentations. In line, FR resulted in activations mainly in the right prefrontal cortex (PFC) for either RH or LH presentations. Emotional content of stimuli facilitated the formation of false memories and strengthened the involvement of the right PFC in FR induction. Ó 2008 Elsevier Inc. All rights reserved. Keywords: False recognition; Lateralization; Prefrontal cortex; Emotions; fMRI
Memory distortions and errors are common in everyday life and may lead to a situation when we remember something which in fact did not happen. This phenomenon is widely known as false recognition (FR) or false memory. Experimentally, it is defined as a situation where people mistakenly believe that a newly introduced object, word or different type of stimulus has been encountered in a past experience or event (Roediger & McDermott, 1995). There are a great number of neuroimaging and electrophysiological studies (for review see Schacter & Slotnick, 2004) which show that prefrontal cortex is involved in processes leading to FR. A very recent behavioural study which used laterally presented stimuli (i.e. they were directed to the right hemisphere (RH) or the left one (LH)) has shown that the RH has a strong bias towards FR, i.e. more errors of this type are committed when stimuli are addressed to the RH (Bellamy & Shillcock, 2007). However, to our knowledge, there is no *
Corresponding author. Fax: +48 22 8225342. E-mail address: [email protected] (A. Marchewka).
1074-7427/$ - see front matter Ó 2008 Elsevier Inc. All rights reserved. doi:10.1016/j.nlm.2008.01.012
neuroimaging study that investigated whether such behavioural effects are reflected in asymmetrical brain activation. Our experiment was therefore designed to resolve this issue by using functional magnetic resonance imaging (fMRI). Following Bellamy and Shillcock, we decided to use the divided-visual field paradigm since our previous research clearly indicated that this procedure was very efficient in highlighting hemispheric differences not only on a behavioural but also on a neuronal level (Marchewka & Nowicka, 2007; Nowicka, Marchewka, & Szatkowska, 2006). It is widely known that the emotional content of information can influence memory performance. Negatively charged stimuli are not only better remembered than neutral ones, but FR is also increased for such type of stimuli (McNeely, Dywan, & Segalowitz, 2004; Windmann & Kutas, 2001). Based on these findings, we employed in our study both emotionally negative and neutral stimuli to investigate whether brain activity during FR is influenced by the emotional valence of stimuli. We attempted to advance the understanding of the phenomenon of false memory by combining the divided-visual
A. Marchewka et al. / Neurobiology of Learning and Memory 90 (2008) 280–284
field technique and presentation of emotionally charged stimuli. Since there is strong evidence that processing of negative emotions is lateralised to the RH (Davidson, 1992), we have hypothesised that FR-related activations will be more pronounced in the case of emotionally negative stimuli directed to the RH. Twenty-three healthy, right-handed subjects participated in the study. The data from 7 subjects was excluded from analysis because of the low rate (less than 10%) of FR-type errors (i.e. new items recognised as old ones). The age of the remaining 16 subjects (nine females) ranged from 23 to 30. All subjects gave their written informed consent to the study, which was approved by the Ethical Committee of the University of Magdeburg. Stimuli were displayed using the Presentation software (http//:www.neurobs.com) run on a standard PC computer and back-projected onto a mirror system mounted on the head coil. Eye movements were monitored using a homemade eye tracking system. The set of stimuli consisted of pictures taken from the International Affective Picture System selected following the original scores (Lang, Bradley, & Cuthbert, 2001): emotionally negative with low valence (mean = 2.78, SD = 0.91) and emotionally neutral with high valence (mean = 5.93, SD = 1.04). Stimuli were fully counterbalanced between visual fields and study phases in respect of their valence and luminance. The experiment consisted of two parts: a study phase and a test phase. During the study phase, subjects were presented with emotionally neutral or negative pictures for 400 ms, either in the left (LVF) or right (RVF) visual field. The study phase consisted of 120 trials, presented in pseudo-random order, fully counterbalanced as regards emotional valence and type of visual field. Subjects were told to view pictures without making any response and were not aware that they would later be tested on recognition memory. The test phase was run immediately after the study phase. The total number of stimuli was 240, half of which were new to the subjects. Again, each stimulus was displayed for 400 ms. The inter-stimulus interval (ITI) with a fixation cross lasted 4–6 s. Trials were mixed pseudo-randomly and fully counterbalanced with respect to all experimental conditions (old/new stimulus, emotionally negative/neutral, LVF/RVF). The task of the subjects was to indicate whether the picture was an old or a new one (i.e. whether it had already been presented or not during the study phase) by pressing one of two buttons on a fibre optic response pad using the index finger of the right hand. Magnetic resonance imaging was carried out using a 3 Tesla Trio (Siemens Medical Solution) MRI scanner equipped with an 8-channel phased array coil. Detailed anatomical data of the whole brain was acquired using a multiplanar rapidly acquired gradient echo (MP—RAGE) sequence with 1.0 mm isotropic resolution. For each subject 192 slices were obtained which covered the entire brain. Functional images were acquired using an echo planar
281
imaging (EPI) pulse sequence (FOV 224 mm, matrix 64 64, slice thickness: 3.5 mm, TE: 30 ms, TR 2000 ms, FA: 80°). The functional run in the test phase lasted 22 min 40 s, during which 34 contiguous, oblique-axial images, oriented parallel to the anterior–posterior commissural plane were acquired with a total of 673 brain volumes. Functional MRI data was pre-processed and analysed using SPM5 run on MATLAB software. The data was motion corrected and then spatially normalised (voxel size 2 2 2) using template images implemented in SPM5 (NIH P-20 project), which gives an approximation of the Talairach and Tournoux (1988) atlas space (SPM5 manual 2005). Finally, functional data was smoothed with an 8 mm full-width, half-maximum Gaussian kernel. Pre-processed functional data was first analysed on an individual level with a general linear model using all the experimental conditions involved with the canonical hemodynamic response function (Frackowiak, Friston, Frith, Dolan, & Mazziotta, 1997). Contrast maps from individual subjects were entered into a random-effect group analysis to show significant effects for tested conditions across all subjects. Regions consisting of at least five contiguous voxels that exceeded an uncorrected threshold of P < 0.005 were considered reliable and were reported in this paper. FR-type errors (new stimuli falsely recognised as old ones) and corresponding reaction times were estimated for each subject. The average percentage of FRs across all participants was 25.75% (minimum 13.6%, maximum 41%, SD = 9.3). The number of FRs of new pictures was analysed using repeated measures MANOVA, with emotional valence (neutral/negative) and visual field (RVF/ LVF) as the main factors. Analysis revealed the main effect of valence (F(1, 15) = 53.8, P < 0.001) and an interaction between valence and visual field (F(1, 15) = 5.4, P < 0.05). Emotionally loaded stimuli produced more FRs than emotionally neutral stimuli. The two-way interaction indicated that although generally LVF presentations resulted in a higher number of FRs than RVF presentations (Fig. 1),
Fig. 1. Percentage of false recognition for emotionally neutral and emotionally negative material in the LVF (right hemisphere) and the LVF (left hemisphere). Bars represent SEM. Star indicates significant difference at P < 0.05.
282
A. Marchewka et al. / Neurobiology of Learning and Memory 90 (2008) 280–284
Table 1 Regions of significant activations (P < 0.005, uncorrected) during false recognition (FR) contrasted with correct recognition (CR) Type of analysis/region
X
Y
Z
T-stat
Voxels
FR > CR, LVF, all pictures R, middle frontal gyrus, BA 6 R, middle frontal gyrus, BA 47 R, inferior frontal gurus, BA 9 R, middle frontal gyrus, BA 47 R, medial frontal gyrus, BA 8 L, middle frontal gyrus, BA 45
36 52 54 26 8 56
10 44 22 24 32 24
62 8 26 8 38 16
4.95 3.92 3.74 3.31 2.91 2.90
91 109 247 200 35 17
FR > CR, LVF, negative pictures R, inferior frontal gurus, BA 47 R, middle frontal gyrus, BA 46 R, superior frontal gyrus, BA 9 R, medial frontal gyrus, BA 8
50 56 6 12
44 24 58 36
10 22 38 34
4.39 4.28 3.94 3.76
57 147 13 16
FR > CR, LVF, neutral pictures R, inferior frontal gurus, BA 47 R, middle frontal gyrus, BA 6
30 36
24 8
18 62
3.87 3.61
17 14
FR > CR, RVF, all pictures R, medial frontal gyrus, BA 9, 8 R, medial frontal gyrus, BA 8 R, middle frontal gyrus, BA 9
10 8 44
36 18 18
34 48 32
3.27 3.24 3.20
33 46 32
FR > CR, RVF, negative pictures R, middle frontal gyrus, BA 9
34
36
34
3.48
14
L, left hemisphere; R, right hemisphere; BA, Brodmann’s area.
this difference was statistically significant (F(1, 15) = 5.9, P < 0.05) only in the case of negative stimuli. Reaction times registered in FR trials were analysed using repeated measures MANOVA with emotional valence and visual field as the main factors. It revealed no statistically significant effects. In the first step of the fMRI data analysis, direct contrasts of false and correct recognitions (CR) of new items (FR > CR) were conducted for the LVF and RVF trials, disregarding the type of pictures. Then, within each visual hemifield, FR > CR contrasts were done separately for negative and neutral stimuli. Table 1 summarises the fMRI results. FR contrasted with CR for all pictures presented in the LVF revealed, as expected, significant activation mainly in the right middle and inferior frontal gyrus with a total number of 682 activated voxels and only 17 activated voxels in the left middle frontal lobe. Separate FR > CR analyses performed for LVF trials subdivided as regards the emotional content of pictures also showed significant activations only in the RH for either negative or neutral stimuli (see Table 1). As regards the RVF presentations, FR > CR contrast for all pictures revealed significant activations, which were again located in the right prefrontal cortex. The size of activated area, however, was much smaller compared to the LVF presentations. Separate analysis for trials with emotionally negative pictures showed activation in the right middle frontal gyrus, while trials with emotionally neutral pictures did not show any significant activation even at a lower statistical threshold (P < 0.05).
In addition, direct comparison of activations for FR of emotionally negative and neutral pictures presented to the LVF showed significant activation (Fig. 2) consisting of 55 voxels in the right prefrontal cortex (BA 9). In the present study, we have investigated whether two hemispheres play a different role in eliciting FR and whether their involvement in this memory illusion depends on the emotional content of stimuli. At a behavioural level we have found that FR occurred significantly more often when emotionally negative pictures were used, compared to emotionally neutral stimuli. In addition, new stimuli were more likely to be recognised as old ones when they were presented to the LVF/RH than when they were presented to the RVF/LH. This is in line with recent behavioural studies (Bellamy & Shillcock, 2007; Westerberg & Marsolek, 2003) which showed that the RH is more susceptible to such memory distortion. Moreover, in the case of emotionally loaded stimuli, the difference between the hemispheres (higher FR rate for stimuli directed to the RH) was more pronounced compared to neutral stimuli. This indicates that the emotionality of new stimuli significantly increases the probability that they will be falsely recognised as old. However, it is possible that a higher emotion-related FR rate may not be a consequence of the emotionality of stimuli per se; it may result from the plausible semantic cohesiveness of emotional items due to shared strong inter-item associations with one another (Maratos & Rugg, 2001; McNeely et al., 2004). Our fMRI findings perfectly corresponded with the behavioural outcome outlined above. FR resulted in activations mainly in the prefrontal areas of the RH. Some fMRI (Schacter, Buckner, Koutstaal, Dale, & Rosen, 1997) and clinical (Rapcsak, Polster, Glisky, & Comer, 1996) studies also pointed to the RH as the hemisphere more prone to such memory errors. Analyses performed for LVF trials gave rise to significant and robust activations, as one might expect, mainly in the contralateral RH. Furthermore, it was again the RH that was activated, though not so extensively, when FR-type errors were committed for pictures presented in the RVF. Thus our results suggest that the prefrontal regions of the RH are specifically involved in FR. In addition, the RH involvement in FR was increased in the case of processing emotionally laden stimuli. While activation related to FR of neutral stimuli was limited to a small number of voxels (for LVF), or even there was no significant activation (for RVF), FRs of negative pictures activated a large neuronal network within the right prefrontal cortex. This is in line with some electrophysiological studies reporting that FR of emotional stimuli, relative to FR of neutral ones, elicited greater sustained ERP positivity in a late slow wave recorded in the RH (McNeely et al., 2004). To investigate further the interaction revealed in behavioural data we performed a separate analysis for FR trials using emotionally negative pictures compared to emotion-
A. Marchewka et al. / Neurobiology of Learning and Memory 90 (2008) 280–284
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Fig. 2. False recognition of emotionally negative stimuli versus correct recognition of emotionally neutral stimuli. Significant group activations are superimposed on a normalised single subject’s T2 image. Only activations consisting of at least five contiguous voxels that exceeded an uncorrected threshold of P < 0.005 are shown.
ally neutral ones presented to the LVF. This yielded significant activation in the right prefrontal cortex (PFC, BA 9), a region that was shown to be involved in tasks requiring close monitoring of item familiarity (Dobbins, Simons, & Schacter, 2004). Thus, this activation might, to some extent, be a by-product of high levels of semantic cohesion of emotionally negative stimuli. Altogether this study provided two interesting findings. Firstly, the emotional content of stimuli facilitated the formation of false memories. Secondly, it was also the emotional load of stimuli that strengthened the involvement of the right PFC in FR generation. One may look at our findings in the light of hemispheric differences for the processing of affectively charged stimuli. The general role of the RH in emotion processing seems to be well documented (Adolphs, Damasio, Tranel, & Damasio, 1996; Christman & Hackworth, 1993; Levy, Heller, Banich, & Burton, 1983). Many studies have suggested, however, that there is a hemispheric bias in the processing of emotional information depending on the valence of the emotion conveyed by that information. The negative valence was said to be processed by the RH and the positive valence by the LH (Davidson, 1992). On the basis of our present results, it is not possible to resolve the issue of whether the stronger involvement of the RH in generating false memories in the case of emotionally negative stimuli was due to the general role of this hemisphere in emotion processing or,
rather, whether it reflected a specific effect of the negative valence of the stimuli. Further studies, using both positive and negative stimuli, are needed to obtain evidence in favour of one or the other hypothesis. Acknowledgments This research was supported by Center for Advance Imaging (BMBF 01GO0505). References Adolphs, R., Damasio, H., Tranel, D., & Damasio, A. R. (1996). Cortical systems for the recognition of emotion in facial expressions. Journal of Neuroscience, 16, 7678–7687. Bellamy, K. J., & Shillcock, R. (2007). A right hemisphere bias towards false memory. Laterality, 12, 154–166. Christman, S. D., & Hackworth, M. D. (1993). Equivalent perceptual asymmetries for free viewing of positive and negative emotional expressions in chimeric faces. Neuropsychologia, 1, 621–624. Davidson, R. (1992). Anterior cerebral asymmetry and the nature of emotion. Brain and Cognition, 20, 125–151. Dobbins, I. G., Simons, J. S., & Schacter, D. L. (2004). fMRI evidence for separable and lateralized prefrontal memory monitoring processes. Journal of Cognitive Neuroscience, 16, 908–920. Frackowiak, R. S. J., Friston, K. J., Frith, C., Dolan, R., & Mazziotta, J. C. (1997). Human brain function. USA: Academic Press. Lang, P. J., Bradley, M. M., & Cuthbert, B. N. (2001). International Affective Picture System (IAPS): Instruction manual and affective ratings. Technical report A-5. Gainesville, FL: The Center for Research Physiology, University of Florida.
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Levy, J., Heller, W., Banich, M. T., & Burton, L. A. (1983). Asymmetry of perception in free viewing of chimeric faces. Brain and Cognition, 2, 404–419. Maratos, E. J., & Rugg, M. D. (2001). Electrophysiological correlates of the retrieval of emotional and non-emotional context. Journal of Cognitive Neuroscience, 13, 877–891. Marchewka, A., & Nowicka, A. (2007). Repetition priming for emotionally negative and neutral stimuli. Acta Neurobiologiae Experimentalis, 67, 83–92. McNeely, H., Dywan, J., & Segalowitz, S. J. (2004). ERP indices of emotionality and semantic cohesiveness during recognition judgements. Psychophysiology, 41, 117–129. Nowicka, A., Marchewka, A., & Szatkowska, I. (2006). Lateralization of repetition effects in event-related potentials to words in left- and righthanded women. Neuroscience Letters, 393, 150–154. Rapcsak, S. Z., Polster, M. R., Glisky, M. L., & Comer, J. F. (1996). False recognition of unfamiliar faces following right hemisphere damage, neuropsychological and anatomical observations. Cortex, 32, 593–611.
Roediger, H. L., III, & McDermott, K. B. (1995). Creating false memories, remembering words not presented in lists. Journal of Experimental Psychology Learning, Memory and Cognition, 21, 803–814. Schacter, D. L., Buckner, R. L., Koutstaal, W., Dale, A. M., & Rosen, B. R. (1997). Late onset of anterior prefrontal activity during true and false recognition. An event-related fMRI study. NeuroImage, 6, 259–269. Schacter, D. L., & Slotnick, S. D. (2004). The cognitive neuroscience of memory distortion. Neuron, 44, 149–160. Talairach, J., & Tournoux, P. (1988). Co-planar stereotaxic atlas of the human brain. Stuttgart, Germany: Thieme. Westerberg, C. E., & Marsolek, C. J. (2003). Hemispheric asymmetries in memory processes as measured in a false recognition paradigm. Cortex, 39, 627–642. Windmann, S., & Kutas, M. (2001). Electrophysiological correlates of emotion-induced recognition bias. Journal of Cognitive Neuroscience, 13, 577–592.
Neurobiology of Learning and Memory 90 (2008) 280–284 www.elsevier.com/locate/ynlme
Brief Report
False recognition of emotional stimuli is lateralised in the brain: An fMRI study A. Marchewka a,*, A. Brechmann b, A. Nowicka a, K. Jednoro´g a, H. Scheich b, A. Grabowska a a
Nencki Institute of Experimental Biology, Department of Neurophysiology, Laboratory of Psychophysiology, 3 Pasteur Street, 02-093 Warsaw, Poland b Leibniz Institute for Neurobiology, Non-Invasive Brain Imaging, Magdeburg, Germany Received 19 November 2007; revised 29 January 2008; accepted 29 January 2008 Available online 7 March 2008
Abstract We have investigated whether the left (LH) and right (RH) hemisphere play a different role in eliciting false recognition (FR) and whether their involvement in this memory illusion depends on the emotional content of stimuli. Negative and neutral pictures (taken from IAPS) were presented in the divided-visual field paradigm. Subjects task was to indicate whether the pictures had already been presented or not during the preceding study phase. FR rate was much higher for the RH than the LH presentations. In line, FR resulted in activations mainly in the right prefrontal cortex (PFC) for either RH or LH presentations. Emotional content of stimuli facilitated the formation of false memories and strengthened the involvement of the right PFC in FR induction. Ó 2008 Elsevier Inc. All rights reserved. Keywords: False recognition; Lateralization; Prefrontal cortex; Emotions; fMRI
Memory distortions and errors are common in everyday life and may lead to a situation when we remember something which in fact did not happen. This phenomenon is widely known as false recognition (FR) or false memory. Experimentally, it is defined as a situation where people mistakenly believe that a newly introduced object, word or different type of stimulus has been encountered in a past experience or event (Roediger & McDermott, 1995). There are a great number of neuroimaging and electrophysiological studies (for review see Schacter & Slotnick, 2004) which show that prefrontal cortex is involved in processes leading to FR. A very recent behavioural study which used laterally presented stimuli (i.e. they were directed to the right hemisphere (RH) or the left one (LH)) has shown that the RH has a strong bias towards FR, i.e. more errors of this type are committed when stimuli are addressed to the RH (Bellamy & Shillcock, 2007). However, to our knowledge, there is no *
Corresponding author. Fax: +48 22 8225342. E-mail address: [email protected] (A. Marchewka).
1074-7427/$ - see front matter Ó 2008 Elsevier Inc. All rights reserved. doi:10.1016/j.nlm.2008.01.012
neuroimaging study that investigated whether such behavioural effects are reflected in asymmetrical brain activation. Our experiment was therefore designed to resolve this issue by using functional magnetic resonance imaging (fMRI). Following Bellamy and Shillcock, we decided to use the divided-visual field paradigm since our previous research clearly indicated that this procedure was very efficient in highlighting hemispheric differences not only on a behavioural but also on a neuronal level (Marchewka & Nowicka, 2007; Nowicka, Marchewka, & Szatkowska, 2006). It is widely known that the emotional content of information can influence memory performance. Negatively charged stimuli are not only better remembered than neutral ones, but FR is also increased for such type of stimuli (McNeely, Dywan, & Segalowitz, 2004; Windmann & Kutas, 2001). Based on these findings, we employed in our study both emotionally negative and neutral stimuli to investigate whether brain activity during FR is influenced by the emotional valence of stimuli. We attempted to advance the understanding of the phenomenon of false memory by combining the divided-visual
A. Marchewka et al. / Neurobiology of Learning and Memory 90 (2008) 280–284
field technique and presentation of emotionally charged stimuli. Since there is strong evidence that processing of negative emotions is lateralised to the RH (Davidson, 1992), we have hypothesised that FR-related activations will be more pronounced in the case of emotionally negative stimuli directed to the RH. Twenty-three healthy, right-handed subjects participated in the study. The data from 7 subjects was excluded from analysis because of the low rate (less than 10%) of FR-type errors (i.e. new items recognised as old ones). The age of the remaining 16 subjects (nine females) ranged from 23 to 30. All subjects gave their written informed consent to the study, which was approved by the Ethical Committee of the University of Magdeburg. Stimuli were displayed using the Presentation software (http//:www.neurobs.com) run on a standard PC computer and back-projected onto a mirror system mounted on the head coil. Eye movements were monitored using a homemade eye tracking system. The set of stimuli consisted of pictures taken from the International Affective Picture System selected following the original scores (Lang, Bradley, & Cuthbert, 2001): emotionally negative with low valence (mean = 2.78, SD = 0.91) and emotionally neutral with high valence (mean = 5.93, SD = 1.04). Stimuli were fully counterbalanced between visual fields and study phases in respect of their valence and luminance. The experiment consisted of two parts: a study phase and a test phase. During the study phase, subjects were presented with emotionally neutral or negative pictures for 400 ms, either in the left (LVF) or right (RVF) visual field. The study phase consisted of 120 trials, presented in pseudo-random order, fully counterbalanced as regards emotional valence and type of visual field. Subjects were told to view pictures without making any response and were not aware that they would later be tested on recognition memory. The test phase was run immediately after the study phase. The total number of stimuli was 240, half of which were new to the subjects. Again, each stimulus was displayed for 400 ms. The inter-stimulus interval (ITI) with a fixation cross lasted 4–6 s. Trials were mixed pseudo-randomly and fully counterbalanced with respect to all experimental conditions (old/new stimulus, emotionally negative/neutral, LVF/RVF). The task of the subjects was to indicate whether the picture was an old or a new one (i.e. whether it had already been presented or not during the study phase) by pressing one of two buttons on a fibre optic response pad using the index finger of the right hand. Magnetic resonance imaging was carried out using a 3 Tesla Trio (Siemens Medical Solution) MRI scanner equipped with an 8-channel phased array coil. Detailed anatomical data of the whole brain was acquired using a multiplanar rapidly acquired gradient echo (MP—RAGE) sequence with 1.0 mm isotropic resolution. For each subject 192 slices were obtained which covered the entire brain. Functional images were acquired using an echo planar
281
imaging (EPI) pulse sequence (FOV 224 mm, matrix 64 64, slice thickness: 3.5 mm, TE: 30 ms, TR 2000 ms, FA: 80°). The functional run in the test phase lasted 22 min 40 s, during which 34 contiguous, oblique-axial images, oriented parallel to the anterior–posterior commissural plane were acquired with a total of 673 brain volumes. Functional MRI data was pre-processed and analysed using SPM5 run on MATLAB software. The data was motion corrected and then spatially normalised (voxel size 2 2 2) using template images implemented in SPM5 (NIH P-20 project), which gives an approximation of the Talairach and Tournoux (1988) atlas space (SPM5 manual 2005). Finally, functional data was smoothed with an 8 mm full-width, half-maximum Gaussian kernel. Pre-processed functional data was first analysed on an individual level with a general linear model using all the experimental conditions involved with the canonical hemodynamic response function (Frackowiak, Friston, Frith, Dolan, & Mazziotta, 1997). Contrast maps from individual subjects were entered into a random-effect group analysis to show significant effects for tested conditions across all subjects. Regions consisting of at least five contiguous voxels that exceeded an uncorrected threshold of P < 0.005 were considered reliable and were reported in this paper. FR-type errors (new stimuli falsely recognised as old ones) and corresponding reaction times were estimated for each subject. The average percentage of FRs across all participants was 25.75% (minimum 13.6%, maximum 41%, SD = 9.3). The number of FRs of new pictures was analysed using repeated measures MANOVA, with emotional valence (neutral/negative) and visual field (RVF/ LVF) as the main factors. Analysis revealed the main effect of valence (F(1, 15) = 53.8, P < 0.001) and an interaction between valence and visual field (F(1, 15) = 5.4, P < 0.05). Emotionally loaded stimuli produced more FRs than emotionally neutral stimuli. The two-way interaction indicated that although generally LVF presentations resulted in a higher number of FRs than RVF presentations (Fig. 1),
Fig. 1. Percentage of false recognition for emotionally neutral and emotionally negative material in the LVF (right hemisphere) and the LVF (left hemisphere). Bars represent SEM. Star indicates significant difference at P < 0.05.
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A. Marchewka et al. / Neurobiology of Learning and Memory 90 (2008) 280–284
Table 1 Regions of significant activations (P < 0.005, uncorrected) during false recognition (FR) contrasted with correct recognition (CR) Type of analysis/region
X
Y
Z
T-stat
Voxels
FR > CR, LVF, all pictures R, middle frontal gyrus, BA 6 R, middle frontal gyrus, BA 47 R, inferior frontal gurus, BA 9 R, middle frontal gyrus, BA 47 R, medial frontal gyrus, BA 8 L, middle frontal gyrus, BA 45
36 52 54 26 8 56
10 44 22 24 32 24
62 8 26 8 38 16
4.95 3.92 3.74 3.31 2.91 2.90
91 109 247 200 35 17
FR > CR, LVF, negative pictures R, inferior frontal gurus, BA 47 R, middle frontal gyrus, BA 46 R, superior frontal gyrus, BA 9 R, medial frontal gyrus, BA 8
50 56 6 12
44 24 58 36
10 22 38 34
4.39 4.28 3.94 3.76
57 147 13 16
FR > CR, LVF, neutral pictures R, inferior frontal gurus, BA 47 R, middle frontal gyrus, BA 6
30 36
24 8
18 62
3.87 3.61
17 14
FR > CR, RVF, all pictures R, medial frontal gyrus, BA 9, 8 R, medial frontal gyrus, BA 8 R, middle frontal gyrus, BA 9
10 8 44
36 18 18
34 48 32
3.27 3.24 3.20
33 46 32
FR > CR, RVF, negative pictures R, middle frontal gyrus, BA 9
34
36
34
3.48
14
L, left hemisphere; R, right hemisphere; BA, Brodmann’s area.
this difference was statistically significant (F(1, 15) = 5.9, P < 0.05) only in the case of negative stimuli. Reaction times registered in FR trials were analysed using repeated measures MANOVA with emotional valence and visual field as the main factors. It revealed no statistically significant effects. In the first step of the fMRI data analysis, direct contrasts of false and correct recognitions (CR) of new items (FR > CR) were conducted for the LVF and RVF trials, disregarding the type of pictures. Then, within each visual hemifield, FR > CR contrasts were done separately for negative and neutral stimuli. Table 1 summarises the fMRI results. FR contrasted with CR for all pictures presented in the LVF revealed, as expected, significant activation mainly in the right middle and inferior frontal gyrus with a total number of 682 activated voxels and only 17 activated voxels in the left middle frontal lobe. Separate FR > CR analyses performed for LVF trials subdivided as regards the emotional content of pictures also showed significant activations only in the RH for either negative or neutral stimuli (see Table 1). As regards the RVF presentations, FR > CR contrast for all pictures revealed significant activations, which were again located in the right prefrontal cortex. The size of activated area, however, was much smaller compared to the LVF presentations. Separate analysis for trials with emotionally negative pictures showed activation in the right middle frontal gyrus, while trials with emotionally neutral pictures did not show any significant activation even at a lower statistical threshold (P < 0.05).
In addition, direct comparison of activations for FR of emotionally negative and neutral pictures presented to the LVF showed significant activation (Fig. 2) consisting of 55 voxels in the right prefrontal cortex (BA 9). In the present study, we have investigated whether two hemispheres play a different role in eliciting FR and whether their involvement in this memory illusion depends on the emotional content of stimuli. At a behavioural level we have found that FR occurred significantly more often when emotionally negative pictures were used, compared to emotionally neutral stimuli. In addition, new stimuli were more likely to be recognised as old ones when they were presented to the LVF/RH than when they were presented to the RVF/LH. This is in line with recent behavioural studies (Bellamy & Shillcock, 2007; Westerberg & Marsolek, 2003) which showed that the RH is more susceptible to such memory distortion. Moreover, in the case of emotionally loaded stimuli, the difference between the hemispheres (higher FR rate for stimuli directed to the RH) was more pronounced compared to neutral stimuli. This indicates that the emotionality of new stimuli significantly increases the probability that they will be falsely recognised as old. However, it is possible that a higher emotion-related FR rate may not be a consequence of the emotionality of stimuli per se; it may result from the plausible semantic cohesiveness of emotional items due to shared strong inter-item associations with one another (Maratos & Rugg, 2001; McNeely et al., 2004). Our fMRI findings perfectly corresponded with the behavioural outcome outlined above. FR resulted in activations mainly in the prefrontal areas of the RH. Some fMRI (Schacter, Buckner, Koutstaal, Dale, & Rosen, 1997) and clinical (Rapcsak, Polster, Glisky, & Comer, 1996) studies also pointed to the RH as the hemisphere more prone to such memory errors. Analyses performed for LVF trials gave rise to significant and robust activations, as one might expect, mainly in the contralateral RH. Furthermore, it was again the RH that was activated, though not so extensively, when FR-type errors were committed for pictures presented in the RVF. Thus our results suggest that the prefrontal regions of the RH are specifically involved in FR. In addition, the RH involvement in FR was increased in the case of processing emotionally laden stimuli. While activation related to FR of neutral stimuli was limited to a small number of voxels (for LVF), or even there was no significant activation (for RVF), FRs of negative pictures activated a large neuronal network within the right prefrontal cortex. This is in line with some electrophysiological studies reporting that FR of emotional stimuli, relative to FR of neutral ones, elicited greater sustained ERP positivity in a late slow wave recorded in the RH (McNeely et al., 2004). To investigate further the interaction revealed in behavioural data we performed a separate analysis for FR trials using emotionally negative pictures compared to emotion-
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Fig. 2. False recognition of emotionally negative stimuli versus correct recognition of emotionally neutral stimuli. Significant group activations are superimposed on a normalised single subject’s T2 image. Only activations consisting of at least five contiguous voxels that exceeded an uncorrected threshold of P < 0.005 are shown.
ally neutral ones presented to the LVF. This yielded significant activation in the right prefrontal cortex (PFC, BA 9), a region that was shown to be involved in tasks requiring close monitoring of item familiarity (Dobbins, Simons, & Schacter, 2004). Thus, this activation might, to some extent, be a by-product of high levels of semantic cohesion of emotionally negative stimuli. Altogether this study provided two interesting findings. Firstly, the emotional content of stimuli facilitated the formation of false memories. Secondly, it was also the emotional load of stimuli that strengthened the involvement of the right PFC in FR generation. One may look at our findings in the light of hemispheric differences for the processing of affectively charged stimuli. The general role of the RH in emotion processing seems to be well documented (Adolphs, Damasio, Tranel, & Damasio, 1996; Christman & Hackworth, 1993; Levy, Heller, Banich, & Burton, 1983). Many studies have suggested, however, that there is a hemispheric bias in the processing of emotional information depending on the valence of the emotion conveyed by that information. The negative valence was said to be processed by the RH and the positive valence by the LH (Davidson, 1992). On the basis of our present results, it is not possible to resolve the issue of whether the stronger involvement of the RH in generating false memories in the case of emotionally negative stimuli was due to the general role of this hemisphere in emotion processing or,
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