Brain, Vol. 126, No. 3, 650-668,
March 2003
© 2003 Guarantors of Brain
doi: 10.1093/brain/awg064
Differential remoteness and emotional tone modulate the neural correlates of autobiographical memory
1 Physiological Psychology, University of Bielefeld, Bielefeld, 2 Institute of Medicine, Research Centre Jülich, Jülich, 3 C. & O. Vogt-Institute of Brain Research, Heinrich Heine University Düsseldorf, Düsseldorf and 4 Department of Neurology, Universitätsklinikum Aachen, Rheinisch-Westfälische-Technische Hochschule Aachen, Aachen, Germany.
Correspondence to: Martina Piefke, Physiological Psychology, University of Bielefeld, PO Box 100131, 33501 Bielefeld, Germany E-mail: martina.piefke{at}uni-bielefeld.de
Received March 22, 2002. Revised September 7, 2002. Second revision October 15, 2002. Accepted October 16, 2002.
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Summary |
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Autobiographical memory relies on complex interactions between episodic memory contents, associated emotions and a sense of self-continuity along the time axis of one’s life history. The neural correlates underlying autobiographical memory are known to primarily comprise areas of prefrontal cortex, medial and lateral temporal cortex, as well as posterior cingulate and retrosplenial cortex. By contrast, the effect of encoding and/or storage parameters such as the emotional tone of the memories retrieved or the length of the time-interval between the initial encoding of information and retrieval remains to be clarified. Using blocked design functional MRI and statistical parametric mapping, we investigated the impact of remoteness (factor 1: recent, remote) and emotional valence (factor 2: positive, negative) on the neural correlates of autobiographical memory retrieval. Changes in neural activity (P < 0.05, corrected) related to autobiographical memory retrieval (irrespective of remoteness and emotional tone) relative to baseline were observed bilaterally in medial and lateral temporal, temporal–occipital, posterior cingulate and frontal cortices. Recent (relative to remote) memories were associated with differentially increased neural activity bilaterally in the retrosplenial cortex and the hippocampal region, whereas remote (relative to recent) memories did not show any statistically significant differential neural activations. Positive (relative to negative) memories bilaterally activated the orbitofrontal cortex, the temporal pole, as well as medial temporal areas, with the activation peak being in the entorhinal region. By contrast, negative (relative to positive) memories differentially increased neural activity in the right middle temporal gyrus only. The data suggest differential functional roles for temporal, prefrontal and retrosplenial regions during autobiographical memory retrieval depending on the remoteness and the emotional valence of the memories retrieved. In particular, our findings support the ‘classic’ model of long-term memory processing, which suggests a time-limited differential involvement of the hippocampus in memory consolidation. Interestingly, the observation of such a time-dependent involvement of the hippocampal region in memory consolidation corresponds to the course of retrograde amnesia observed in demented patients, with the loss of recent memories appearing during early stages of the disease when conspicuous neurofibrillary changes are restricted mainly to the hippocampal and parahippocampal regions. Only during later stages, as the neurofibrillary changes spread out to neocortical association areas, do remote memories also become impaired. We conclude that the brain regions involved in autobiographical memory retrieval are influenced by the triggered memories’ emotional significance and their relationship to the individual time axis.
Keywords: episodic memory; memory consolidation; hippocampus; retrosplenial cortex; entorhinal cortex; fMRI
Abbreviations: AC–PC= anterior–posterior commissure; BOLD = blood oxygenation level-dependent; CN = childhood negative; CP = childhood positive; fMRI = functional MRI; RN = recent negative; ROI = region of interest; RP = recent positive; SPM = statistical parametric mapping
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Introduction |
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Autobiographical memory can best be characterized as a subsystem of episodic memory that implies emotion processing. It also provides a direct link into the awareness of the time course of one’s life history, as it is specifically engaged in the meaningful reconstruction of one’s own past (Tulving, 1983
; Fink et al., 1996; Tulving and Markowitsch, 1998). To do so, the contents of episodic memory need to be integrated with a sense of self-coherence and self-continuity. Furthermore, the recollective experience is, at least in part, related to the evocation of previously experienced emotions. The integration of these diverse processes allows for the creation of subjectively meaningful life experiences. Due to this highly complex interaction of cognitive and emotional processes, the experimental investigation of the neural basis of autobiographical memory remains a challenge to neuroscientists. In humans, functional neuroimaging allows insights into the neural correlates of both memory and emotional states. However, most functional neuroimaging studies concerned with the influence of emotions on the neural mechanisms underlying episodic memory have so far focused on encoding and retrieval processes of non-autobiographical and hence less complex verbal or pictorial material (e.g. Hamann et al., 1999; Dolan et al., 2000; Tabert et al., 2001), where the involved components can be isolated and controlled far more easily than when studying memories of one’s personal past.
Accordingly, only a few functional neuroimaging studies have directly investigated the neural correlates of autobiographical memory. In a PET study, Fink and colleagues compared the neural activations associated with the recollection of autobiographical episodes (personal condition) with those related to recall of biographical episodes of persons unknown to the subjects (impersonal condition) (Fink et al., 1996). Autobiographical memory relative to a low-level (resting) baseline resulted in bilateral activations of the medial and superior temporal gyri, the temporal poles, as well as temporal-mesial, dorsal frontal and posterior cingulate/retrosplenial areas, with a lateralization of neural activity increases to the right hemisphere. The recollection of autobiographical episodes relative to biographical episodes of unknown persons led to additional increases in neural activity, primarily in right prefrontal areas, temporal–mesial and temporal–lateral cortex, insula and posterior cingulate areas, suggesting that a preponderantly right hemispheric network of prefrontal and temporal areas, as well as posterior cingulate/retrosplenial areas is engaged in the retrieval of emotion-laden autobiographical memories. The study did not address the interesting question of whether different qualities or features of autobiographical memories—for example, encoding and/or storage parameters like the emotional tone or the age of the memories retrieved—are represented in separate neural components (Fink et al., 1996). Surprisingly, experimental information regarding these issues remains scarce to date.
Although one can, for example, remember in moderate detail the process of buying a couple of shirts 3 months ago, an experience which is pretty neutral, autobiographical memories are typically associated with emotional contents (Markowitsch, 1998, 2000; Dolan et al., 2000) and both encoding and retrieval processes are known to be influenced by emotional valence (Holmes, 1970; Brewer, 1988; Bower, 1992). As structures of the limbic system are engaged in both memory and emotion processing, the specific functions underlying increased neural activity in these areas and the specific degrees of their involvement in autobiographical memory are of particular interest. In a recent PET study, Dolan and colleagues investigated whether distinct or similar brain regions are involved in retrieving emotional versus neutral pictorial material (Dolan et al., 2000). By varying task requirements (recognition memory versus a judgement task) and target item density, two distinct patterns of neural activation relating to emotional memory retrieval were identified. A right anterior temporal activation was observed that reflected the (tonic) psychological set associated with emotional episodic memory retrieval, while a left amygdala response reflected phasic emotional item-related responses. The data thus support the notion that emotions interact with the neural mechanisms of memory retrieval and suggest that such an interaction depends upon the specific task demands.
The matter is further complicated by the fact that autobiographical memories are characterized by their specific relationship to the individual time axis. The time-point of the initial encoding of the information, memory consolidation processes and further time-related parameters are all assumed to interact with the neural mechanisms underlying autobiographical memory retrieval. They are thus likely to modulate the neural processes (and the brain regions) involved. Here, a longstanding key debate is concerned with the duration and persistence of hippocampal involvement in memory retrieval. One view attributes a time-limited or time-dependent engagement of the hippocampal system in declarative memory retrieval (Squire, 1992; Teng and Squire, 1999). The other view, by contrast, favours a life-long engagement of the hippocampal system in the recollection of episodic memories (Nadel and Moscovitch, 1997; Ryan et al., 2001).
The current study addresses the issue of whether differential emotional valence and remoteness of memories modulate the functional neuroanatomy of autobiographical memory retrieval. In a functional MRI (fMRI) experiment with 20 volunteers, we measured changes in the regional blood oxygenation level-dependent (BOLD) signals associated with four experimental conditions of interest (recent, remote, positive and negative autobiographical memory retrieval) and a low-level ‘baseline’ applying a factorial blocked design with the factors TIME (recent, remote memories) and EMOTION (positive, negative tone). By means of this design, we assessed both the common and differential neural mechanisms underlying positive/negative and recent/remote autobiographical memories and their interactions.
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Subjects
Twenty healthy, right-handed subjects (10 male, 10 female; mean age ±SD = 26 ± 3 years) with no history of psychiatric or neurological disorder were enrolled and written informed consent was obtained from all subjects prior to participation. The study was approved by the local ethics Committee of the Heinrich-Heine University, Düsseldorf.
Stimuli
For each subject, individual stimuli were acquired by means of a semi-structured autobiographical interview (mean duration = 3.5 h; the interval between the interview and the scanning session was 5–6 weeks). Participants reported 10 positive and 10 negative childhood memories (up to age 10 years) as well as 10 positive and 10 negative memories from their recent past (last 5 years before the interview). Subjects were required to provide detailed contextual information for each remembered episode to allow for the preparation of verbal stimuli describing specific situations of the respective episodes. Six different stimulus sentences were constructed for each autobiographical episode retrieved. Thus, a total of 60 sentences was generated for each of the four memory conditions for each subject: (i) childhood positive (CP); (ii) childhood negative (CN); (iii) recent positive (RP); and (iv) recent negative (RN). This material (i.e. 240 non-identical individual stimulus sentences per subject) was used during the fMRI measurements to trigger the associated autobiographical memories (see Appendices 1 and 2).
Tasks and experimental design
For visual presentation of the verbal stimulus material during the fMRI experiment, a mirror construction was used to reflect the stimulus display. Stimuli were presented in black on a white background. Lying in the MR scanner, subjects viewed the display from a distance of 26 cm (14 cm screen to mirror, 12 cm mirror to subject’s eyes). Presentation and timing of stimuli was accomplished using MEL 4.0 (MEL Professional, Psychology Software Tools, Inc., Pittsburgh, PA, USA). Six individual trials (i.e. stimuli, which each triggered different autobiographical episodes) of one of the four memory conditions were blocked together. Each trial consisted of a stimulus on time of 4.3 s and an interstimulus interval of 1 s. Thus, each block of trials had a duration of 31.8 s. A factorial-blocked design was applied to evoke the neural responses associated with retrieval of different types of emotional tone (negative, positive) and remoteness (recent, remote) of autobiographical memory. Memory conditions were separated from each other by low-level baselines (each lasting 16 s), during which the instructions for the next block of trials were presented. Instructions were as follows: ‘Please remember the events and situations of your personal life history specified in the displayed sentences as vividly and emotionally as possible.’
Per baseline, four (whole brain) volumes [TR (repetition time) = 4 s] were acquired. Per block of trials of each memory condition (CP, CN, RP, RN), eight (whole brain) volumes (TR = 4 s) were acquired. A total of five experimental runs each consisting of nine baselines and eight memory blocks were performed, leading to the acquisition of a total of 500 volumes per subject (100 volume images per run). This scanning paradigm resulted in two repeats per condition per experimental run, leading to 10 repeats per condition per subject. The order of the memory conditions was counterbalanced across runs and individuals. There was no repeat of the individual stimulus sentences, neither within nor across the experimental conditions to avoid any habituation effects.
To control for the subjects’ alertness during a block of trials, we included a subordinate reaction time task into the autobiographical memory task. During the interstimulus interval, subjects viewed either a blank screen for 1 s, or a checkerboard for 500 ms followed by a blank screen for the remaining 500 ms. During each block of trials, 1–4 checkerboards were presented. The number of times a checkerboard was presented was kept identical across all conditions. Subjects were instructed to press a button on a keypad located right of their body with their right index finger as fast as possible upon successful detection of the checkerboard.
Prior to scanning, subjects were familiarized with the experimental set-up and the tasks. Subjects were informed that the reaction time task was subordinate to the autobiographical memory task to prevent them from concentrating on the checkerboard. Moreover, they were required to read the instruction for the next block of trials repeatedly to make sure that the same cognitive task was performed in all baseline conditions.
MRI hardware and technical parameters
Scanning was performed using a 1.5 T whole-body scanner (Siemens Vision, Erlangen, Germany) with EPI (echo-planar imaging) capability. A standard radio frequency head coil was used for transmitting and receiving. Prior to functional neuroimaging, high resolution anatomical images were acquired using a T1-weighted 3D magnetization-prepared, rapid acquisition gradient echo (MP-RAGE) pulse sequence with the following parameters: TE (echo time) = 4.4 ms, TR = 11.4 ms, TI (inversion time) = 300 ms, flip angle = 15°, slice thickness = 1.25 mm, FOV (field of view) = 230 mm, matrix = 200 x 256, 128 sagittal slices. fMRI images were acquired in axial plane with a gradient echo EPI pulse sequence using BOLD contrast. Sequence parameters were as follows: TE = 66 ms, TR = 4 s, flip angle = 90°, slice thickness = 4 mm, inter-slice gap = 0.4 mm, FOV = 200 mm, in plane resolution = 3.125 mm x 3.125 mm, matrix = 64 x 64, 30 transversal slices. These 30 slices covered a subject’s brain from the cerebellar vermis up to the vertex and were oriented along the anterior–posterior commissure (AC–PC) line using a midsagittal scout image. The fMRI paradigm consisted of the five time-series as described above. Each of these time-series was preceded by four dummy images to allow the MRI signal to reach steady state.
Post-scanning debriefing
To assess successful recognition and correct association of each stimulus with the respective personal past episode during the fMRI measurement, each subject was asked immediately after scanning to read all stimulus sentences again. For each of the 240 individual stimuli, subjects retrospectively indicated: (i) whether they recognized the associated context during scanning; (ii) whether it triggered a positive or a negative tone associated with the memory; and (iii) whether it was associated with a recent or a remote memory.
Furthermore, subjects completed a questionnaire on characteristic features of autobiographical memory for each condition separately. On a rating scale ranging from 0 to 5 (0 = not at all, 1 = scarcely, 2 = slightly, 3 = fairly, 4 = intense, 5 = highly intense), subjects retrospectively rated the intensities of the retrieved memories’ characteristics during the scanning session with respect to the following items: picture-likeness, scene-likeness, colouredness, emotionality, re-experience, vividness, richness of details, role of language, olfactory perceptions, temperature, perceptions of touch, acoustical perceptions and gustatory perceptions.
Image processing
Image processing and all statistical calculations were performed on Ultra 20 workstations (SUN Microsystems Computers, Palo Alto, CA, USA) using MATLAB (The Mathworks Inc., Natick, MA, USA) and statistical parametric mapping (SPM) software (SPM99; Wellcome Department of Cognitive Neurology, London, UK; http://www.fil.ion.ucl. ac.uk). SPM99 was employed for image preprocessing (image realignment, co-registration, normalization and smoothing) and to create statistical maps of changes in relative regional BOLD responses corresponding to the four memory conditions and the baseline (Friston et al., 1995a, b).
The first four images of each time series were discarded to allow the MRI signal to reach steady state (see above). To correct for head movement between scans, the remaining 100 volume images of each time series were realigned to the first image i.e. to the fifth image of each time series. Following realignment, all image sets were co-registered to the 3D anatomical images acquired prior to functional neuroimaging. For image co-registration, SPM99 and MPItool (Max-Planck Institute for Neurological Research, Cologne, Germany) were used. Thereafter, images were transformed using linear proportions and a non-linear sampling algorithm into standard stereotactic space as defined by Talairach and Tournoux (1988) with the intercommissural AC–PC line being used as the reference plane (Friston et al., 1995a). For this normalization procedure, a representative brain from the Montreal Neurological Institute series provided by SPM99 was employed as the reference template (Evans et al., 1994). Subsequently, all data were expressed in terms of standard stereotactic x, y and z coordinates using the Talairach and Tournoux (1988) stereotactic space convention. The resulting pixel size was 2 x 2 mm with an interplane distance of 2 mm. Following normalization procedures, transformed data were smoothed with a Gaussian kernel of 10 mm (full width half maximum) for the group analysis to compensate for normal variation in individual brain size and shape (as well as gyral and sulcal anatomy across subjects) and to meet the statistical requirements of the theory of Gaussian random fields presupposed by the general linear model employed in SPM99. To restrict analysis to intracranial regions, only voxels with values > 0.8 of the volume mean in all images were selected.
Statistical analyses
Following image pre-processing, statistical analyses of fMRI data were performed. Subject-specific low frequency drifts in signal were modelled and removed using low frequency cosine waves, and proportional scaling normalized the global means. Data analysis was performed by modelling the experimental memory conditions (CP, CN, RP, RN) and the baseline by means of reference waveforms which correspond to boxcar functions convolved with a haemodynamic response function (Friston et al., 1995a). Accordingly, a design matrix that comprised contrasts modelling alternating intervals of ‘activation’ (referring to the four different memory conditions) and ‘baseline’ was defined. Specific effects were assessed by applying appropriate linear contrasts to the parameter estimates of the four experimental memory conditions and the baselines resulting in t-statistics for each voxel. These t-statistics were then transformed to Z-statistics constituting SPM{Z} of differences between both the memory conditions and between the memory conditions and the baseline. SPM{Z}-statistics were interpreted in light of the theory of probabilistic behaviour of Gaussian random fields (Friston et al., 1995b).
For the group analysis, repeated measures were collapsed within subject and within experimental run after having adjusted for both global blood flow by means of proportional scaling, and low frequency drifts by employing a high pass filter of 100 s (see above). This procedure resulted in one scan per condition per subject. Thereafter, experimental conditions were compared between subjects, thereby effecting a random effects model. Voxels had to pass a height threshold of T = 4.88 (corresponding to Z = 4.6; P < 0.05, corrected for multiple comparisons; Friston, 1997) in order to be identified as reflecting statistically significant activation; no extent threshold was applied. These relatively stringent statistical thresholds were employed to reduce the likelihood of type II errors. In addition, small volume corrections (Worsley et al., 1996) were employed to allow for a (hypothesis-driven) region of interest (ROI) approach to the hippocampal region. A priori, x, y and z coordinates for the hippocampus were derived from Talairach and Tournaux’s atlas (Talairach and Tournaux, 1988), which allowed us to centre the ROIs on the hippocampal region: x = +32, y = –14 and z = –18 (right hippocampus) and x = –24, y = –18 and z = –14 (left hippocampus). These coordinates are well within the range of coordinates for activations of the hippocampal region reported in previous studies (e.g. Lane et al., 1997). The extent of the spherical ROIs was set to 10 mm, i.e. Gaussian kernel used for smoothing the group data (see above).
Masking of the relevant contrasts was performed to assess whether or not relative increases in neural activity between conditions reflected activations in the condition of interest or rather deactivations in the other (relative to baseline).
Data were analysed for the overall effect of emotional autobiographical memory retrieval contrasting all memory conditions with the baseline [(CP + CN + RP + RN) > baseline], for the main effects of the factors TIME [recent versus remote (RP + RN) > (CP + CN) and vice-versa] and EMOTION [positive versus negative (CP + RP) > (CN + RN) and vice-versa], and for the interactions between the factors TIME and EMOTION [(CN > CP) > (RN > RP) and (RN > RP) > (CN > CP)].
Localization of activations
Standard stereotactic coordinates of pixels showing local maximum activation were determined within areas of significant relative changes in neural activity associated with the demands of the different memory conditions. These local maxima were anatomically localized by reference to a standard stereotactic atlas (Talairach and Tournoux, 1988). For validation of this method of localization, SPM{Z}-statistics were superimposed on the group mean 3D MRI image, which was calculated following stereotactic transformation of each individual’s 3D MRI image into the same standard stereotactic space of the Montreal Neurological Institute average brain (Friston et al., 1995b) employed as a template by SPM99 (see above).
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Brain activity associated with all memory conditions versus baseline
Significant increases in neural activity (P < 0.05, corrected) related to all memory conditions (irrespective of remoteness and emotional tone) relative to baseline were observed bilaterally in the posterior cingulate/retrosplenial cortex, medial and lateral temporal cortex, temporal–occipital cortex and dorsal–occipital cortex extending into the fusiform gyrus, the parahippocampal and hippocampal regions and, bilaterally, though predominantly left hemispheric in the ventrolateral and dorsolateral prefrontal cortex (see Table 1). There was additional activation of the supplementary motor area, the right cerebellum and the left superior parietal cortex.
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Brain activity associated with differential remoteness of memories: recent versus remote
Recent (relative to remote) memories bilaterally increased neural activity in the retrosplenial cortex (P < 0.05, corrected for multiple comparisons across the whole brain) extending into the posterior cingulate cortex. An additional hypothesis-driven ROI-based analysis of the hippocampal region revealed significant (P < 0.05; small volume corrected) activation of this area bilaterally with the local maxima being in the posterior aspects of the hippocampal regions. The inverse contrast (remote relative to recent) revealed no significant differential increases in neural activity associated with remote memories. Fig. 1A and B display the brain regions with differential increases in neural activity related to recent memories; Table 2A provides the respective stereotactic coordinates and Z-scores.
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Brain activity associated with differential emotional tone of memories: positive versus negative
When compared with negative memories, positive memories differentially increased neural activity in the right orbitofrontal cortex and temporal pole, as well as bilaterally in the medial temporal cortex centred upon the entorhinal region (see Table 2B). The reverse contrast revealed differential increases in neural activity associated with negative (relative to positive) memories in the right middle temporal gyrus only (see Table 2C). Figs 2 and 3 display the brain regions with differential increases in neural activity related to positive and negative memories, respectively.
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As the neural activations in the medial temporal regions may show marked habituation to repeated stimuli, we tested for such habituation effects in the medial temporal activations observed (despite the fact that no stimulus was repeated, yet accounting for the repeated occurrence of episodes to be retrieved). At the single subject level, introduction of time (i.e. repetition of a given memory episode) as a covariate did not reveal any significant changes of neural activity in the entorhinal region or the amygdala complex.
Interactions
The analyses of the interaction terms [(CN > CP) > (RN > RP) and (RN > RP) > (CN > CP)] revealed no statistically significant interactions between the factors TIME and EMOTION.
Reaction times and error rates in the subordinate alertness task during the fMRI experiment
Statistical analysis of the subjects’ reaction times and error rates in the subordinate task did not reveal any significant differences (reaction times, P = 0.347; error rates, P = 0.687) between the four memory conditions suggesting that the overall level of alertness was the same across all memory conditions.
Post-scanning debriefing procedures
Post-scanning recognition of the stimulus sentences and their correct assignment to the respective personal episodes of the subjects’ past was 97.6% across all conditions without statistically significant differences between the four memory conditions (CP = 96.8% ± 5.6; CN = 96.6% ± 5.5; RP = 98.3% ± 4.1; RN = 98.7% ± 3.1), although there was a tendency towards a higher percentage of recognition for recent relative to remote memories.
The results of the questionnaire concerned with characteristic features of autobiographical memory were analysed employing an ANOVA (analysis of variance) with repeated measures on one factor (interaction: factor x group; df = 1). To keep the significance level for multiple comparisons between items at P < 0.05, single comparisons’ 
levels were adjusted according to the Bonferroni inequality. Significantly higher ratings for recent relative to remote memories were obtained for the items picture-likeness (F = 10.7; P = 0.004), emotionality (F = 12.0; P = 0.003), re-experience (F = 17.3; P = 0.001), and richness of details (F = 13.6; P = 0.002). By contrast, no statistically significant differences in the subjects’ ratings were observed for positive versus negative memories.
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Joint effect of all memory conditions
The areas activated by all memory conditions (relative to baseline) correspond to the known networks supporting episodic non-autobiographical and autobiographical memory retrieval, and are in good accordance with most current models of episodic memory (see e.g. Squire, 1992
; Nadel and Moscovitch, 1997; Tulving and Markowitsch, 1998). The areas activated included (bilaterally, but predominantly left hemispheric): the ventrolateral and dorsolateral prefrontal cortex; lateral (neocortical) and medial (mesolimbic) temporal regions, including the hippocampal and parahippocampal regions; the fusiform gyrus extending into the temporal-occipital cortex; and the retrosplenial and posterior cingulate cortices.
The finding of left hemisphere dominance associated with autobiographical memory retrieval was somewhat unexpected, as the data reported by Fink and colleagues implicated a predominantly right-hemispheric network of brain regions in the retrieval of emotionally laden autobiographical memories (Fink et al., 1996). However, recent functional neuroimaging studies concerned with different components of episodic memory encoding and retrieval (for a review see Lee et al., 2003) strongly suggest that laterality effects in the neural activation patterns associated with episodic memory encoding and retrieval depend upon the distinct stimulus characteristics (e.g. type of stimulus materials, modality of stimulus presentation), the complexity of the stimulus material and the information to be retrieved, and the specific task demands rather than clear functional hemispheric specialization. For example, Nolde and colleagues reported that rather simple episodic memory tasks yielded right prefrontal activations (Nolde et al., 1998a, b). In contrast, activations in several distinct areas of the left prefrontal cortex during episodic memory retrieval were related to increasing complexity of retrieved information. Furthermore, Ranganath and colleagues demonstrated that increased neural activity in left prefrontal regions was associated with the retrieval of specific perceptual information (Ranganath et al., 2000). Our subjects retrieved highly complex information, and most likely concentrated on perceptual aspects with high imageability during the retrieval processes as is suggested by the behavioural data (subjects gave highest ratings across memory conditions for the item ‘picture-like memories’). The degree of hemispheric lateralization observed in our current data is thus consistent with recent neuroimaging studies of episodic memory retrieval. Likewise, high imageability of retrieved memories is likely to have caused the extended bilateral activations of the fusiform gyrus and temporal–occipital as well as dorsal–occipital cortex which are known to be activated by visual attention (Fink et al., 1997; Corbetta et al., 1998) and imagery (Howard et al., 1998).
Given the above argument regarding the effects of complexity and perceptual specificity on the neural correlates of episodic memory retrieval, the finding of a primarily right-hemispheric neural network underlying emotional episodic memory retrieval reported by Fink and colleagues is also likely to reflect the specific task demands of that study (Fink et al., 1996); they required their subjects to switch between the retrieval of autobiographical experiences (autobiographical episodic memory = personal) and the biography of a person unknown to them but presented prior to scanning (i.e. impersonal episodic memory). Right-hemispheric activations associated with autobiographical memory when contrasted with the retrieval of an unknown person’s biography could thus have resulted from, for example, taking a self-perspective during remembering personal past episodes (e.g. Keenan et al., 2001; Vogeley et al., 2001). Furthermore, it should be kept in mind that recall of an unknown person’s biography lacks both the typical link into the time course of an individual’s personal life history and the emotional re-experience of one’s own past experiences associated with autobiographical memory. The intricate phenomena of ‘mental time travel’ (Tulving and Markowitsch, 1998) are thus absent when retrieving the biography of a person unknown and may equally well account for or contribute to the right hemispheric preponderance observed by one study (Fink et al., 1996).
Finally, in the current study, stimuli were presented visually so that subjects had to read the written material which might have contributed in part to the observed left-hemispheric activations.
Main effect of the factor TIME
The hippocampal region
The differential increases in neural activity in the hippocampal region bilaterally associated with recent relative to remote memories are of great interest with respect to the ongoing debate on the nature of hippocampal involvement in memory retrieval. To date, numerous investigations of the hippocampal involvement in memory functions have been performed, including studies in rodents (e.g. Aggleton et al., 1986; Sutherland and McDonald, 1990) and non-human primates (e.g. Salmon et al., 1987; Zola-Morgan and Squire, 1990; Gaffan, 1993), neuropsychological assessment of patients with medial temporal lobe damage (e.g. Beatty et al., 1987; Yoneda et al., 1992; De Renzi and Lecchelli, 1993) and functional neuroimaging studies of healthy human subjects (e.g. Haist et al., 2001; Maguire et al., 2001a). From these studies, a general agreement has emerged that the hippocampus is specifically engaged in declarative memory and that hippocampal lesions can result in both anterograde and retrograde amnesia. Interestingly, damage to the hippocampus may disrupt some encoding and retrieval tasks while leaving other forms of learning and memory unaffected (Sutherland et al., 2001).
The ‘classic’ model of long-term memory processing (Squire, 1992; Teng and Squire, 1999) suggests a time-dependent degree of involvement of the hippocampal formation in long-term memory consolidation. This model assumes that memories are transferred to neocortical areas within a certain time-interval and upon storage become independent of the hippocampal formation. To date, a considerable number of lesion studies in animals (e.g. Winocur, 1990; Zola-Morgan and Squire, 1990) as well as neuropsychological studies of patients with damage to the hippocampal region and severe loss of recently acquired information but persisting remote memories (Zola-Morgan et al., 1986; Teyler and Perkins, 1988; Squire, 1992; Rempel-Clower et al., 1996; Anagnostaras et al., 1999; Bak et al., 2001) have corroborated this view. Animal lesion studies of the hippocampus revealed temporally graded retrograde amnesia covering days to months, and studies of amnesic patients with hippocampal damage demonstrated temporal gradients ranging from years to decades. Rempel-Clower and colleagues reported that the length of temporal gradients of enduring retrograde amnesia correlated with the increasing extent of hippocampal damage (Rempel-Clower et al., 1996). In two patients with damage limited to the CA1 field of the hippocampal region, retrograde amnesia covered the last 2 years prior to brain damage only. In the other two patients with more extensive damage to the hippocampal formation, the memory impairment extended back at least 15 years in one patient and as much as 25 years in the other.
By contrast, other lesion studies investigating the degree of hippocampal involvement in memory functions in both animals (Salmon et al., 1987; Bolhuis et al., 1994) and humans (Beatty et al., 1988; Nadel and Moscovitch, 1997; Westmacott et al., 2001) have failed to replicate the above characteristic pattern of a time-dependent memory loss. Rather, flat gradients with equivalent memory loss for all time periods prior to hippocampal damage were reported. The factors determining the absence or presence, as well as the length of temporal gradients in retrograde amnesia resulting from hippocampal lesions, thus remain largely obscure.
In view of the inconsistent findings above, an alternative model for long-term memory consolidation has been proposed: the multiple trace theory (Nadel and Moscovitch, 1997; Ryan et al., 2001). This model assumes a persistent involvement of the hippocampal region in episodic (though not necessarily in semantic) memory retrieval, irrespective of the time point at which the information was acquired. According to the multiple trace theory, each reactivation of a memory leads to the creation of a new memory trace, each of which is assumed to involve an ensemble of hippocampal and neocortical neurons. The proliferation of the memory traces occurring with repeated reactivation of each of the memories is supposed to render older memories less susceptible to disruption from hippocampal damage than recent ones. Depending on the location and the extent of medial temporal damage, distinct types of retrograde amnesia may then result.
Two recent functional neuroimaging studies support the multiple trace theory (Maguire et al., 2001a; Ryan et al., 2001). Using event-related fMRI, Maguire and colleagues parametrically varied the remoteness of autobiographical and public event memories (Maguire et al., 2001a). Stimulus sentences were presented auditorily, and subjects indicated by pressing a key whether each statement was true or false. Neural activity in the ventrolateral prefrontal cortex (bilaterally, but predominantly right-hemispheric) decreased parametrically with increasing remoteness of autobiographical memories. No parametric effect related to memory age was observed in the hippocampal regions. However, specific aspects of the experimental design are likely to have prevented the possibility of a differential hippocampal involvement in recent and remote autobiographical memory retrieval from being observed in that study. For example, the decision task employed may have prompted subjects to focus on the decision component rather than the vivid recollection of personal past episodes (Maguire et al., 2001a). It is conceivable that one knows whether or not a statement depicts a personal past episode without engaging at depth in the retrieval of the details of the respective episode. Ryan and colleagues also demonstrated the absence of differential hippocampal activations in recent and remote autobiographical memory retrieval (Ryan et al., 2001). In this study, no distracting task was employed during the retrieval condition that might have prevented subjects from concentrating on the recollection of autobiographical experiences.
By contrast, two other fMRI studies employing topographical (Niki and Luo, 2002) and semantic (Haist et al., 2001) memories have provided evidence for a differential involvement of the hippocampal region in recent and remote memory retrieval. Using blocked fMRI, Haist and colleagues investigated the neural correlates of recent and remote memories by applying a famous faces test, thus primarily measuring semantic memory. They reported memories for faces from the 1990s only with increased neural activity in the hippocampal region bilaterally (relative to memories for faces from more remote decades). Furthermore, right entorhinal cortex activations showed a linear decrease from recent to remote decades suggesting that this brain area is more enduringly involved in long-term memory retrieval than the hippocampal formation (Haist et al., 2001).
In good accordance with the findings above, Niki and Luo (2002) provided evidence for a time-limited engagement of hippocampal and parahippocampal regions in topographical autobiographical memory. Memories for places the subjects had visited within the last 2 years prior to the investigation were associated with hippocampal and parahippocampal activations, while memories for places visited > 7 years before did not yield any medial temporal activations.
It should be noted that subject numbers were small in all these fMRI experiments on recent and remote memory retrieval—six in Maguire et al. (2001a), seven in Ryan et al. (2001), eight in Haist et al. (2001) and nine in Niki and Luo (2002). One should thus be cautious in interpreting the data reported in these reports. Furthermore, none of the studies employed statistical models allowing for inferences to the general population. Our current data (based on n = 20, using a random effects model which allows inferences to the general population) strongly support the view of a time-dependent differential involvement of the hippocampal region in long-term episodic memory retrieval. The BOLD signal plots of the hippocampal regions (Fig. 1) activated in our study clearly demonstrate that recent (relative to remote) memories (irrespective of emotional content) led to increased neural activity in the hippocampal formation.
Interestingly, this differential involvement of the hippocampal complex in recent versus remote memories is paralleled by the sequential development of memory loss in Alzheimer’s disease. The loss of recent memories appears during Braak stages III–IV, when conspicuous neurofibrillary changes are restricted mainly to the hippocampal and parahippocampal regions (Braak et al., 1996). Only during later stages (Braak stages V–VI), as the neurofibrillary changes spread out to the association areas of the neocortex, do the remote memories also become impaired. These pathological and neuropsychological findings thus support the suggested predominant role of the hippocampal formation in the retrieval of recent relative to remote memories demonstrated directly in the current study.
It should be kept in mind, however, that in the present study recent and remote autobiographical memories did not only differ with respect to the factor TIME but also with regard to picture-likeness, emotionality and the richness of details of memories, as well as to the degree subjects re-experienced their autobiographical past events. Although we consider it unlikely, differences in imageability or emotional load of the stimulus material could, at least in principle, account for the observed differential neural activity. However, no differential activations were observed in striate/extrastriate areas or the amygdala complex to support such an argument. Our findings thus provide direct support for a time-dependent degree of involvement of the hippocampal region in autobiographical memories.
Obviously, the factor TIME cannot simply be viewed as some kind of formal temporal criterion. Rather, one needs to account for its differential effects on the dimensions of imageability, emotionality, re-experience and details of memories (see behavioural data). Hence, the differences observed between recent and remote memories along any of these dimensions may have contributed to the differential activation patterns associated with the retrieval of recent relative to remote memories. Autobiographical memories typically differ from each other along these dimensions. It will thus barely be possible to match autobiographical memories perfectly for the respective factors. However, Haist and colleagues have also shown a time-dependent differential hippocampal involvement in long-term memory using a famous faces test (Haist et al., 2001), which is less susceptible to the above confounds. Although the famous faces test draws on semantic rather than episodic memory processes, it is reasonable to assume that the differential involvement of the hippocampal formation in recent versus remote memories reflects a more general time-dependent hippocampal role in memory consolidation.
A second putative confound common to all experiments contrasting recent and remote autobiographical memories also needs to be considered. By necessity, retrieval of memories is accompanied by simultaneous re-encoding processes, which are at present poorly understood (Buckner et al., 2001). Since in our study both remote and recent autobiographical memories had to be retrieved (and hence re-encoded) during the interview 5–6 weeks prior to the scanning session, we cannot exclude the possibility that childhood memories were refreshed, leading to alterations (in the sense of an interaction) in neural activation patterns associated with retrieval of these memories during scanning. Activation patterns of recent and remote memories might thus have become similar to each other. For example, in a study of fear memory consolidation in rats, Nader and colleagues demonstrated that consolidated fear memories return to a labile state when they are reactivated—with the reactivation being induced 1 or 14 days after conditioning (Nader et al., 2000). For reconsolidation, this labile state required de novo protein synthesis (see also Land et al., 2000). These findings may be taken as evidence that consolidated memories become similar to unconsolidated ones by reactivation, i.e. by each instance of retrieval and re-encoding. It should be noted, however, that the study by Nader and colleagues (Nader et al., 2000) bears on time intervals that are entirely different from those referred to in the current study. Thus, in the case of autobiographical memories of events that happened > 20 years ago retrieval and re-encoding processes must not necessarily yield biochemical reactivation mechanisms such as reported by Nader et al. (2000). Also, autobiographical memories are retrieved and re-encoded throughout one’s whole life. The behavioural importance of the interview prior to scanning with an interval of 5–6 weeks should thus not be overestimated. Moreover, if the hippocampal activation resulted from re-encoding rather than retrieval, the induced BOLD signal changes in this region should have been fairly similar during all four memory conditions.
The observed bilateral activation of the posterior aspects of the hippocampal region is also in good accordance with recent evidence for a functional segregation within the human hippocampal formation. This suggests a rostral–caudal functional division within the hippocampal region, with encoding demands (predominantly) activating the anterior part of the hippocampal region and retrieval demands (predominantly) activating the posterior aspect of the hippocampal region (Lepage et al., 1998; Dolan and Fletcher, 1999). A similar segregation has also been observed with stimulus novelty leading to activation of the anterior part of the hippocampal region and stimulus familiarity activating the posterior part of the hippocampal region (Strange et al., 1999).
The retrosplenial cortex
Retrieval of recent autobiographical memories was also associated with increased neural activity in the retrosplenial cortex (bilaterally) extending into parts of the posterior cingulate cortex. Activation of a comparable region associated with autobiographical memory has been observed previously (Fink et al., 1996; Maguire et al., 2001b). Furthermore, activation of this area has recently been reported in fMRI studies on person familiarity (Shah et al., 2001) and a case of lexical synaesthesia for familiar names (Weiss et al., 2001). In the former study, increased neural activity in the retrosplenial cortex was related to the processing of personally familiar faces or voices (when compared with unfamiliar faces or voices). In the latter study, a comparable cortical region became activated when the subject experienced synaesthesia for personally familiar names only. Based on our behavioural data, recent autobiographical memories were more emotionally laden and familiar to our subjects than childhood memories. Taken together, our current findings and previous data suggest that the activation of the retrosplenial cortex associated with recent relative to remote memories may result from retrieval of personally familiar information in a more general sense. An alternative account for the activation of the retrosplenial cortex is provided by a number of functional neuroimaging studies on emotion processing, which revealed increased neural activity in the retrosplenial cortex associated with responses to the presentation of emotional relative to neutral stimulus material (Maddock, 1999). Since our debriefing results (see above) provided higher ratings for the item ‘emotionality’ for recent (relative to remote) autobiographical memories, our data could also be interpreted as reflecting a retrosplenial involvement in emotion processing.
Anatomically, as well as behaviourally, an expanded network relates retrosplenial and hippocampal structures to memory processing. Anatomically, the retrosplenial cortex lies adjacent to the retrocommissural hippocampus, a small tissue stripe extending around the posterior end of the corpus callosum. It is connected with the entorhinal, the parahippocampal and the perirhinal cortex. The retrosplenial cortex is thus closely associated with the hippocampal formation and other structures of the medial temporal lobe subserving memory functions and emotion processing (Insausti et al., 1987). There are several behavioural studies that demonstrate severe and lasting amnesia following selective retrosplenial damage (Bowers et al., 1988; Gainotti et al., 1998; Heilman et al., 1990). The retrosplenial cortex and its multiple anatomical connections could thus provide a basis for the interplay among emotion and cognitive components that autobiographical memories are typically composed of.
Interestingly, retrieval of remote (relative to recent) memories did not yield any statistically significant differential activations, suggesting that memories which become independent of the hippocampus might be stored in the same cortical regions as those still relying on an hippocampal involvement.
Main effect of the factor EMOTION
The observed bilateral increases in neural activity in the medial basal temporal cortex (with the local maximum being in the entorhinal region associated with positive relative to negative emotional tone of the episodes retrieved) complement other functional neuroimaging studies that have implicated amygdala and adjacent areas in memory and emotion (e.g. Schneider et al., 1995; Breiter et al., 1996; Ketter et al., 1996; Morris et al., 1996; Lane et al., 1997; Garavan et al., 2001). The entorhinal region, as well as its neighbouring medial temporobasal areas, is strongly interconnected with the retrosplenial cortex; all have been implicated in learning, memory and emotional behaviour (e.g. Wyss and Van Groen, 1992). The medial temporobasal areas, including the entorhinal region, are thus likely to hold a key position within the neural networks mediating the interplay among memory and emotion.
Despite the general consensus of a medial temporal involvement in emotion processing, the data show great variance with regard to both the precise structures involved and putative hemispheric asymmetries. For example, while some studies imply the left amygdala in negative emotion processing (e.g. Schneider et al., 1995; Breiter et al., 1996; Ketter et al., 1996; Morris et al., 1996), others have reported the opposite functional lateralization (Canli et al., 1998; Zalla et al., 2000). Since in the present study we observed bilateral entorhinal and adjacent mesio-limbic activations associated with the recollection of positive personal memories, we cannot address the specific issue of lateralization of amygdala functions. However, together with the above findings, our data suggest that the issue of lateralization of medial temporal functions may be highly context-dependent, as is the case with hemispheric asymmetries associated with episodic memory processing (see above).
Interestingly, our data are in line with recent investigations of emotion processing in patients with Alzheimer’s disease. There is a general agreement that already early stages of Alzheimer’s disease are associated with impairments of emotion processing (e.g. Abrisqueta-Gomez et al., 2002; Hargrave et al., 2002) and interpersonal behaviour (Shimokawa et al., 2001). The finding that the entorhinal cortex and adjacent limbic areas are specifically affected by brain pathology in early Alzheimer’s disease (e.g. Braak et al., 1996; see above) is in good accordance with the observation of these behavioural deficits. Interestingly, one recent study (Padovan et al., 2002) reported positive (relative to negative) information to be more vulnerable to the disease, suggesting that these medial temporal regions might be particularly engaged in the processing of positive emotions. Our data directly support the above hypothesis, as the entorhinal region and its adjacent limbic structures were relatively more involved in retrieving positive than negative memories. In addition, our data suggest that the bilateral activations of the entorhinal region and adjacent meso-limbic areas, in conjunction with activation of the orbitofrontal cortex, may reflect key components of the functional neuroanatomy underlying the retrieval of positively valenced autobiographical memories. There is already some evidence that medial temporobasal areas, including the entorhinal region and the amygdala, are specifically engaged in the processing of positively valenced emotion (Garavan et al., 2001; Hamann and Mao, 2002; Padovan et al., 2002), despite some conflicting results suggesting that these areas are more involved in negative emotion (e.g. Whalen et al., 1998; Morris et al., 2001). Our data showing bilateral entorhinal and neighbouring mesiotemporal activations in response to positive valenced autobiographical stimulus material complement another recent fMRI study investigating amygdala involvement in the processing of positively and negatively valenced emotions (Garavan et al., 2001). In this study, the arousal level of the stimuli (high versus low) modulated the amygdala responses to negative stimuli. By contrast, no such effect was observed for positively valenced stimuli, where even a low arousal level for positive stimulus material was sufficient to produce a significant amygdala response. In the present study, emotional valence and arousal level associated with each type of autobiographical memory (recent, remote, positive, negative) were not distinguished systematically, and therefore we cannot address this issue systematically. It should be noted, however, that the limbic activations related to the recall of positive personal memories are unlikely to reflect differences of emotional intensity, or the degree of re-experiencing across conditions as there were no significant differences revealed by the post-scanning debriefing of the subjects.
Activation of the orbitofrontal cortex has been shown in the appraisal of reward (Rogers et al., 1999), the control and correction of behaviour related to reward and punishment (Rolls, 2000), and the retrieval of sad and happy life events (George et al., 1995). Interestingly, the orbitofrontal cortex has also been implicated in the retrieval of items from positive relative to negative emotional context (Maratos et al., 2001), which is in good accordance with our suggestion that this region may be preferentially engaged in the retrieval of autobiographical memories associated with positively valenced emotional context. The reverse finding, namely significantly less activation in the medial orbitofrontal cortex, has been found in patients with posttraumatic stress disorder who in a symptom-provocation experiment had to re-experience traumatic memories (Lanius et al., 2001).
Our data also suggest that the right middle temporal gyrus is implicated in the processing of negative emotions. This finding is supported by a study that reported activation of this area in response to the presentation of negative facial expressions (Iidaka et al., 2001). The additional activations observed in that study (left inferior frontal gyrus and left precentral gyrus) may have resulted from task demands other than those implicated in our study.
No significant interactions between time and emotion were observed. This is likely to reflect the fact that the subjects’ ratings for the items picture-likeness, emotionality, re-experience and richness of details was higher for recent memories than remote ones (see behavioural data). The data thus suggest that the main effect of time includes changes in emotional valence, as discussed above.
Conclusions
In conclusion, our data provide clear evidence that both differential remoteness from the date of information encoding and differential emotional valence modulate the neural activations in key regions within the networks known to support episodic autobiographical memory retrieval (Fink et al., 1996; Maguire et al., 2001b). Our current study shows a differential involvement of both the hippocampal and the retrosplenial region during the retrieval of recent versus remote memories. By contrast, the orbitofrontal cortex as well as the entorhinal region and adjacent medial temporobasal areas were observed to be differentially more active in positive than in negative autobiographical memory retrieval. Importantly, our data demonstrate a time-dependent differential involvement of the hippocampal region in autobiographical long-term memory processing. This is consistent with the view that the hippocampal formation functions as a distributor during memory consolidation (Teyler and Perkins, 1988), but becomes largely obsolete once the information has been firmly integrated in (primarily) neocortical networks (Damasio, 1990; McClelland, 1994; Mesulam, 2000; Squire and Knowlton, 2000).
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Acknowledgements |
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We wish to thank the Institute of Medicine, Jülich, fMRI staff for their expert technical assistance. H.J.M., K.Z. and G.R.F. are supported by the Deutsche Forschungsgemeinschaft (DFG).
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Appendix 1 |
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TopSummaryIntroductionMaterial and methodsResultsDiscussionAppendix 1Example of the stimulus...Appendix 2Example of the stimulus...References |
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Example of the stimulus materials employed: Subject 211 (Run 1) original German version |
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TopSummaryIntroductionMaterial and methodsResultsDiscussionAppendix 1Example of the stimulus...Appendix 2Example of the stimulus...References |
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For anonymization of stimulus sentences, names of family members, friends, locations etc. mentioned by the subject have been replaced by fictitious names.
Positive remote memories
Freude am ersten Schultag: Meine Patentante gibt mir ganz viele Süssigkeiten.
Grosser Bagger im Kindergarten: Wir graben uns unter der Schuppenwand durch.
Monika hat Beeren von den Eiben gegessen: Sie sagt, das sind doch kleine Apfel.
Lego Baukasten zu Weihnachten: Nan grossen Buggy von Mama und Papa gekriegt.
Mit Michael im CVJM Zeltlager: Das spannendste ist doch diese Nachtwanderung.
Am Feldrand ein keines Feuer machen: Wir braten uns da Kartoffeln und Apfel.
Negative remote memories
Mit Martin zu spät zu Hause sein: Papa verkloppt Martin mit dem Handfeger.
Besuch zu Susannes Geburtstag: Ich brenne so ein kleines Loch in ihr neues Zelt.
Der Schlitten schlägt mir in die Hüfte: Ich habe eine lange und tiefe Wunde.
Vater hat Chinaböller gekauft: Der eine explodiert 10 cm von meiner Hand weg.
Im Krankenhaus schon am Schlafen: Da wird mir nachts ne neue Kanüle gelegt.
Frau Richter will unseren Ball haben: Sie steht da jetzt mit dem Küchenmesser.
Positive recent memories
Ich habe den Führerschein bestanden: Sogar im 2. Gang anfahren hat geklappt.
Nach dem Abi auf Mallorca: Mit 11 Freunden Urlaub in einem so schönen Hotel.
Auf Mallorca mit dem Fussballverein: Wir gehen heute mal in den Ballermann 6.
Meine Schwester Sonja ruft mich an: Der Ronald schenkt mir jetzt sein altes Auto.
Auszug von zu Hause: Als ich Sonntag komme, sind Herbert und Eduard schon da.
In Felsberg auf der Schiessbahn: Ich schiesse zum 1. Mal mit scharfer Munition.
Negative recent memories
Fahrradunfall auf dem Schulweg: Mein gebrochener Finger muss operiert werden.
Michaels Selbstmordversuch: Er ist von der Brücke der Autobahn gesprungen.
Martin kriegt die Abizulassung nicht: Sein Freund Wolfgang hat ihn beeinflusst.
Ronald trennt sich von Sonja: Er zieht jetzt mit so einer 24 jährigen zusammen.
Was, Sie geben Widerworte: Der Stufz Kreidemann verpasst mir da Extrawachen.
Bin sauer auf Herbert: Er fragt nicht, ob wir die Hausarbeit zusammen schreiben.
Negative recent memories
Pech mit Mama und Papas Auto: An der Tanke fahre ich an den parkenden Bulli.
Hütchenspiel auf Mallorca: Wie konnte ich dem das Geld in die Hand drücken.
Herr Feldmann im Bio Leistungskurs: Ich habe mich jetzt doch 17 Mal gemeldet.
Gerhard Baumgarten hat sich umgebracht: Zwei Schüsse in seinen Kopf versetzt.
OP wegen gebrochenem Finger: Die pressen mit dem Gummiband Blut aus dem Arm.
Michael hat versucht, sich umzubringen: Er liegt dort 6 Stunden unter der Brücke.
Positive recent memories
Oberleutnant Brand ist unser Zugführer: Der ist ja echt ziemlich locker drauf.
Zwei Wochen Urlaub in Südspanien: Ostermontag feiert das Dorf da auf der Wiese.
Das Hurricane Festival in Bachstein: Zwei Tage feiern, poben und crowd surfing.
Nach unserm Kinoabend bei Ingrid: Sabine und ich bleiben dort beide über Nacht.
Führerschein beim ersten Mal bestanden: Und dazu hab ich das auch selbst bezahlt.
All-inclusive Reise nach dem Abitur: Auf Mallorca erstklassig essen und trinken.
Negative remote memories
Wasser ins Fenster der Nachbarn gespritzt: Die fordern von Papa Bestrafung.
In der Mathegruppe neben Peter: Er bespritzt mich nun mit der Tintenpatrone.
Beim Spielen mit Ali aneinander geraten: Ich habe Angst vor seinen Leuten.
Prügelei mit Jannis im Kindergarten: Er gewinnt obwohl ich ja viel älter bin.
Papa verkloppt Martin: Ich verstecke mich im Bad und schliesse mich hier ein.
Ein kleines Loch im Zelt von Susanne: Hoffentlich sagt die das jetzt nicht Papa.
Positive remote memories
Mein Geburtstag in Dänemark: Morgens allein mit Mama durch die Gegend ziehn.
Religionsunterricht bei Frau Zimmermann: Trotz meines Verhaltens ne 2 gekriegt.
Im Zeugnis eine 1 in Mathe: Die Lehrerin sagt, dass ich sogar besser als eins bin.
Zur Sportgruppe in den Osterferien: Ich mache nun meine ganzen Laufabzeichen.
In der Klasse am ersten Schultag: Wir bekommen die Aufgabe, jetzt etwas zu malen.
Der grosse Bagger im Schuppen: Peter und ich graben uns nun einfach ein Loch.
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Appendix 2 |
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TopSummaryIntroductionMaterial and methodsResultsDiscussionAppendix 1Example of the stimulus...Appendix 2Example of the stimulus...References |
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Example of the stimulus materials employed: Subject 211 (Run 1) English translation* |
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TopSummaryIntroductionMaterial and methodsResultsDiscussionAppendix 1Example of the stimulus...Appendix 2Example of the stimulus...References |
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For anonymization of stimulus sentences, names of family members, friends, locations etc. mentioned by the subject have been replaced by fictitious names.
Positive remote memories
Pleasure at my first day at school: My godmother gives me so many sweets.
The big excavator in the Kindergarten: We dig a hole underneath the wall of the shed.
Monika has eaten berries of the yew trees: She says that these are like little apples.
LEGO set at Christmas: I’ve got big lorry from mum and dad.
Together with Michael in the YMCA camp: The walking-tour by night is most exciting.
Enkindling a fire at the edge of the field: We roast potatoes and apples for us there.
Negative remote memories
Together with Martin late at home: Father beats Martin with the swab.
Visiting Susanne on her birthday: I burn such a small hole in her new tent.
The sledge bumps into my haunch: I now have a long and severe wound.
Father has bought firecrackers: One of them explodes 10 cm away from my hand.
I was already asleep in the hospital: By night they are applying a new canula.
Mrs. Richter wants to have our ball: She is now standing there with that knife.
Positive recent memories
I have got my driving licence: Even starting up at second gear has worked out easily.
In Majorca after school leaving examination: Vacation with 11 friends in this beautiful hotel.
With the football club in Majorca: Today let’s go into the Ballermann 6.
My sister Sonja calls me on the telephone: Ronald gives his old car to me as a present.
Moving out of my parents’ house: As I arrive on Sunday Herbert and Eduard are already there.
In Felsberg on the shooting field: For the first time I am shooting with sharp ammunition.
Negative recent memories
Accident with my bike on the way to school: Surgery because my finger is broken.
Michael’s suicide attempt: He jumps off the bridge of the motorway.
Martin gets no admission to the Abitur: His friend Wolfgang has influenced him badly.
Ronald parts with Sonja: He now lives together with a women of age 24.
Oh, you are in opposition: Army Officer Kreidemann says I have to keep additional watch.
I’m annoyed with Herbert: He does not ask whether we can write that homework together.
Negative recent memories
Bad luck with mum and dad’s car: At the petrol station I crash into the parking van.
Gambling game in Majorca: How could I ever give the money to that person?
Mr Feldmann in the biology course: I have tried 17 times to contribute to the lesson.
Gerhard Baumgarten has committed suicide: He shot himself two times in his head.
Surgery because of my broken finger: With an elastic band they pressed blood out of my arm.
Michael has attempted suicide: He lies under that bridge for six hours.
Positive recent memories
Lieutenant Brand is our chief guard: He is a good fellow and behaves really informally.
Vacation in the south of Spain for two weeks: The village celebrates Easter in that meadow.
The Hurricane Festival in Bachstein: Celebrating, dancing and crowd surfing for two days.
After visiting the cinema we go to Ingrid: Sabine and I both are staying there overnight.
I’ve got the driving licence at my first attempt: And additionally, I have paid that myself.
All-inclusive journey after the Abitur: First class eating and drinking in Majorca.
Negative remote memories
I have spattered water into the window of our neighbours’ house: They want dad to punish me.
Sitting next to Peter in the math course: He bespatters me with ink.
Clashing with Ali during the play: I am afraid of his people.
Brawl with Jannis in the Kindergarten: He is the winner although I am much older than he.
Father beats Martin: I hide here in the bathroom and lock the door.
A small hole in Susanne’s new tent: I hope that she will not tell this to dad now.
Positive remote memories
My birthday in Denmark: In the morning I stroll around with mum only.
The religion course of Mrs Zimmermann: Despite my behaviour I’ve got the note 2.
Note 1 in maths in the certificate: The teacher says that I am even better than 1.
During the vacation around Easter in the sports group: I pass all my examinations in running.
On my first day at school in the class: We are now asked to paint something.
The big excavator in the shed: Peter and I simply dig a hole to get in there.
*Note that the stimulus sentences all had approximately the same length in the original German version (see Appendix 1). As the English language is associated with distinct semantics, syntax and grammar structures, this could not be replicated in the English translation.
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References |
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