Abstract

We used fMRI to investigate the neural processes engaged as individuals down- and up-regulated the emotions associated with negative autobiographical memories (AMs) using cognitive reappraisal strategies. Our analyses examined neural activity during three separate phases, as participants (a) viewed a reappraisal instruction (i.e., Decrease, Increase, Maintain), (b) searched for an AM referenced by a self-generated cue, and (c) elaborated upon the details of the AM being held in mind. Decreasing emotional intensity primarily engaged activity in regions previously implicated in cognitive control (e.g., dorsal and ventral lateral pFC), emotion generation and processing (e.g., amygdala, insula), and visual imagery (e.g., precuneus) as participants searched for and retrieved events. In contrast, increasing emotional intensity engaged similar regions during the instruction phase (i.e., before a memory cue was presented) and again as individuals later elaborated upon the details of the events they had recalled. These findings confirm that reappraisal can modulate neural activity during the recall of personally relevant events, although the time course of this modulation appears to depend on whether individuals are attempting to down- or up-regulate their emotions.

INTRODUCTION

External stimuli in our environments, such as an argument with a loved one or an anxiety-provoking public speaking engagement, often elicit emotional reactions that we desire to regulate (Gross & Thompson, 2007), and indeed much of the extant emotion regulation literature focuses on attempts to change which emotions are experienced or the intensity of emotions evoked in response to external information like images or film clips (see Ochsner & Gross, 2005, 2008, for reviews). However, internally generated cognitions also can produce emotional reactions. For example, recalling a past argument or an anxiety-provoking presentation can reinvoke in the here and now the emotions that were present at the time of an event's occurrence (e.g., Westermann, Kordelia, Stahl, & Hesse, 1996). Just as with external information, we are not merely passive recipients of our internally generated emotional experiences. This study sought to determine the neural correlates of emotion regulation in response to negative autobiographical memories (AMs). Because cognitive reappraisal or the reinterpretation of emotional information in such a way as to decrease or increase its emotional impact is one of the most studied and most effective means for emotion regulation (reviewed by Gross & Thompson, 2007), we focused specifically on how this strategy influences AM.

Although the link between AM recall and emotion regulation is relatively understudied, there is both behavioral and neural evidence that the two processes are interrelated. Individuals report using their AMs in everyday life for regulatory purposes (e.g., recalling a successful exam performance to quell anxiety about an upcoming exam; Bluck, Alea, Habermas, & Rubin, 2005). The reciprocal relation is also true: Regulatory goals can influence which AMs are most likely to be recalled (Josephson, Singer, & Salovey, 1996). In addition, when individuals are instructed to recall a particular event (e.g., high school graduation), regulatory goals can influence which details and appraisals are reported about those AMs (Holland, Tamir, & Kensinger, 2010). The relation between AM and emotion regulation is perhaps most evident in the clinical literature, which illustrates that a failure to effectively regulate emotional responses regarding past negative events (e.g., by ruminating on rather than reappraising negative emotions) is associated with affective disorders like depression (reviewed by Gotlib & Joormann, 2010). Taken together, evidence for the relation between emotion regulation and AM is in line with Conway's (2005) assertion that the constructive nature of AM retrieval leaves it malleable and open to modulation by personally relevant goals.

In addition to their behavioral links, both AM recall and cognitive reappraisal in response to emotional images or film clips engage neural networks with substantial overlap. There are commonalities in pFC activity, likely because of the similar cognitive demands of AM recall and cognitive reappraisal. For example, both tasks rely on dorsolateral pFC (associated with maintaining and manipulating emotional information in working memory during reappraisal [reviewed by Ochsner & Gross, 2008] and manipulating the products of retrieval in working memory during AM recall [reviewed by Cabeza & St. Jacques, 2007]), ventrolateral pFC (associated with selecting appropriate reappraisals during regulation [Denny, Silvers, & Ochsner, 2009] and controlled retrieval processes, including appropriate cue specifications, during the AM access period [Cabeza & St. Jacques, 2007]), and medial pFC (associated with self-referential processing during both regulation [Ochsner & Gross, 2008] and recall [Cabeza & St. Jacques, 2007]). Cognitive reappraisal is further associated with increased activity in dorsal ACC (dACC), a region associated with conflict monitoring (e.g., between competing affective responses; Denny et al., 2009) and correlated with reappraisal success (Ochsner, Bunge, Gross, & Gabrieli, 2002), as well as OFC, thought to support the selection of situationally appropriate emotions (reviewed by Denny et al., 2009).

Both reappraisal and recall processes also engage regions associated with emotional processing, such as the amygdala and the insula. Recalling emotional AMs also has been associated with amygdala and other medial-temporal lobe (MTL) activity (Cabeza & St. Jacques, 2007; Svoboda, McKinnon, & Levine, 2006; Markowitsch et al., 2000), particularly during the initial search for and accessing of events, suggesting that the amygdala may guide the recall of emotionally salient events (Daselaar et al., 2008). Furthermore, amygdala activity during AM recall has been linked to activity in pFC and hippocampus (Greenberg et al., 2005), and the emotional intensity of events is positively correlated with activity in pFC and amygdala (Botzung, Rubin, Miles, Cabeza, & LaBar, 2010), as well as the hippocampus (Addis, Moscovitch, Crawley, & McAndrews, 2004).

Much of the emotion regulation literature focuses on the control of “hot” emotion processing areas via “cold” cognitive regions in pFC (see Ochsner & Gross, 2005, for a review). However, cognitive reappraisal also modulates posterior activity in regions associated with visuospatial processing and attention, such as the parietal lobe, visual cortex, cuneus, and precuneus (e.g., Goldin, McRae, Ramel, & Gross, 2008; Urry et al., 2006; Phan et al., 2005; Ochsner et al., 2004). Interestingly, activity in similar regions—particularly the visual cortex, precuneus, and posterior cingulate/retrosplenial cortex—are activated by the visual imagery that is a defining feature of AM (e.g., Cabeza & St. Jacques, 2007), and this activity has been positively correlated with behavioral ratings of emotional intensity associated with AMs (Botzung et al., 2010). Although their role in reappraisal is not often elaborated upon, one possibility is that decreasing or increasing mental imagery is a useful strategy for decreasing or increasing emotional intensity, respectively (see Ochsner et al., 2004, for similar discussion).

To date, only a handful of studies have addressed how regions belonging to the AM neural network might be modulated as emotion regulation is occurring during recall. Two studies have focused on a more automatic form of regulation that can occur during mood-incongruent recall, revealing in healthy adults that being instructed to recall a positive AM following a negative mood induction recruited OFC and ACC (Cooney, Joormann, Atlas, Eugène, & Gotlib, 2007), with a similar pattern evident in ACC and lateral pFC in healthy adolescents (Joormann, Cooney, Henry, & Gotlib, 2012). Two other studies have compared the more effortful cognitive reappraisal with rumination during the recall of negative AMs. Ruminating on angry AMs led to enhanced connectivity between inferior frontal gyrus and amygdala (Fabiansson, Denson, Moulds, Grisham, & Schira, 2012), and focusing on sad AMs led to increased activity in ACC and medial pFC (Kross, Davidson, Weber, & Ochsner, 2009). In both studies, self-reported negative affect was lower for reappraisal than rumination conditions. However, reappraisal did not lead to any greater connectivity during the recall of angry AMs (Fabiansson et al., 2012), and it only led to increased activity in a region of left pFC that also was activated during rumination on sad AMs (Kross et al., 2009).

Taken together, the Fabiansson et al. (2012) and Kross et al. (2009) experiments suggest that regulatory strategies can modulate core regions of the AM network, but that rumination may do so to a greater extent than reappraisal (see Kross et al., 2009). However, the designs of these studies leave open a number of questions. One limitation of this work from a memory research standpoint is that participants were asked to apply multiple regulatory strategies to a limited number of AMs (nine in Kross et al., 2009; one in Fabiansson et al., 2012) over the course of a scan. It is unclear what the long-term effects of regulating the emotion related to an AM might be. For example, it is possible that being asked to ruminate upon the negative emotions associated with a memory might influence the details that are later constructed about that event and/or the amount of emotion experienced during recall. If this is indeed the case, then being asked to perform such a strategy first might fundamentally change the experience of later trying to reappraise the emotion associated with that same memory.

A second open question is how the up-regulation of negative emotions might modulate AM recall. Fabiansson et al. (2012) and Kross et al. (2009) focused on the down-regulation of negative emotions, but reappraisal can also be used to increase negative emotions when feeling negative is deemed functional (e.g., recalling negative AMs in preparation for playing an aggressive game; Tamir, Mitchell, & Gross, 2008). Although pFC regions are recruited during both the down- and up-regulation of responses to negative images, the consequence of that activation varies, resulting in a decrease or increase, respectively, of amygdala activity (Ochsner et al., 2004).

To address these first two questions, we modified a cognitive reappraisal task traditionally used with emotional images or film clips for use with AMs. We scanned participants as they decreased, increased, or maintained the emotions associated with negative AMs that had been reported at a prescan session. Each memory cue appeared with only one regulatory instruction to prevent initial reappraisal attempts from influencing subsequent attempts. We predicted that attempts to down- and up-regulate (vs. maintain) negative emotions during AM recall would be associated with cognitive control regions in pFC and dACC that have previously been associated with image-based reappraisal (e.g., Ochsner et al., 2004). We also predicted that activity in several regions would be modulated according to the direction of regulation (e.g., less activity during down-regulation and greater activity during up-regulation), including emotion processing regions (e.g., amygdala, insula, medial pFC), MTL regions shown to be sensitive to emotional intensity (e.g., hippocampus; Botzung et al., 2010), and visual imagery regions (e.g., visual cortex, precuneus).

A third exploratory question that this study addressed concerns the timing of reappraisal during AM recall. The constructive nature of AM recall is relatively lengthy and can be subdivided into at least two phases, including the initial search for and retrieval of AM details as a memory is being accessed (referred to here as the “memory onset” phase), followed by an elaboration phase during which time the searched-for memory is held in mind and its details expounded upon (e.g., Daselaar et al., 2008; Addis, Wong, & Schacter, 2007; Steinvorth, Corkin, & Halgren, 2006). At this point, it is unclear during which phase of AM recall cognitive reappraisal might occur and whether up-regulating and down-regulating emotional responses occur over the same time course. Fabiansson et al. (2012) and Kross et al. (2009) provided regulation instructions only after the AMs had been recalled and were being held in mind; such designs might illustrate how regulation strategies influence the elaboration phase of AM but leave open the question of how having regulatory goals in mind before recall influences the AM retrieval network during the initial memory onset and later memory elaboration phases. In the present experiment, we compared activity during three phases: an instruction phase, when participants were presented only with the reappraisal instructions (i.e., “Decrease,” “Increase,” or “Maintain”) for the subsequent memory cue (see Herwig et al., 2007, for a similar design); a memory onset phase, when the memory cue first was presented; and a memory elaboration phase, demarcated by participants' response that they had an AM in mind (see similar distinctions between memory onset and elaboration in Daselaar et al., 2008; Addis et al., 2007; Steinvorth et al., 2006).

METHODS

Participants

Twenty-eight young adults (16 women, range = 18–28 years, M = 21.89 years, SD = 3.25 years) participated in this study. Two participants were dropped from subsequent analyses for failing to make button box responses during the scan, one participant was excluded for failing to complete the prescan appointment, one participant was excluded for failing to complete the scan appointment, one participant was excluded for excessive motion, and one participant was excluded because of scanner malfunction. The final sample included 22 participants (13 women; M = 22.27, SD = 3.56) who had no history of psychiatric, neurological, or learning disorders nor any history or current use of psychiatric medication. Informed consent was obtained from all participants in accordance with the Boston College Institutional Review Board.

Prescan Stimulus Collection Session

Approximately 7–14 days before the scan session (M = 6.73 days, SD = 2.00 days, range = 4–13 days), participants completed a stimulus collection session. Each participant generated 90 specific AMs (i.e., events that lasted no longer than a day and were unique to time and place). Sixty of the AMs were required to be negative in valence, and the remaining 30 were neutral. For each event, participants were instructed to create a title that was just a few words but specific enough that if they were to see that title in the scanner they would know which event it was referencing. In addition to the title, participants wrote a brief sentence describing each event and rated the AMs on a 7-point scale for how emotionally intense, negative, positive, and vivid they were. Finally, participants provided their approximate age in years at the time of each event's occurrence. The AM portion of the study took approximately 1.5–2 hr.

Scan Session

AM Stimuli

From the AMs generated during the prescan stimulus collection session, 15 negative events were assigned to each of three emotion regulation conditions (Decrease, Increase, and Maintain), and 15 neutral events were assigned to a Maintain condition. The behavioral characteristics of the events assigned to each condition are presented in Table 1. For each participant, the negative events assigned to each emotion regulation condition were matched on each of the behavioral ratings that participants made (intensity, negativity, positivity, vividness, and age). The neutral and negative events were matched on vividness and age.

Table 1. 

Behavioral Characteristics of Negative and Neutral AMs from the Prescan Session that Were Assigned to the Scan Session Reappraisal or Maintain Conditions


Prescan Behavioral Ratings
Intensity
Negative
Positive
Vividness
Age
Decrease Neg 4.72 (0.75) 5.55 (0.58) 1.27 (0.27) 5.35 (0.77) 4.56 (2.45) 
Increase Neg 4.64 (0.74) 5.54 (0.65) 1.28 (0.33) 5.29 (0.77) 4.52 (2.50) 
Maintain Neg 4.70 (0.74) 5.57 (0.64) 1.28 (0.27) 5.38 (0.80) 4.56 (2.52) 
Maintain Neutral 2.40 (1.05) 1.43 (0.26) 3.92 (1.38) 5.13 (0.85) 3.66 (2.76) 

Prescan Behavioral Ratings
Intensity
Negative
Positive
Vividness
Age
Decrease Neg 4.72 (0.75) 5.55 (0.58) 1.27 (0.27) 5.35 (0.77) 4.56 (2.45) 
Increase Neg 4.64 (0.74) 5.54 (0.65) 1.28 (0.33) 5.29 (0.77) 4.52 (2.50) 
Maintain Neg 4.70 (0.74) 5.57 (0.64) 1.28 (0.27) 5.38 (0.80) 4.56 (2.52) 
Maintain Neutral 2.40 (1.05) 1.43 (0.26) 3.92 (1.38) 5.13 (0.85) 3.66 (2.76) 

Standard deviations are presented in parentheses.

Emotion Regulation Task

Immediately before being scanned, participants received instructions for the emotion regulation task that they performed in the scanner. Participants were instructed that, when they saw either “Decrease” or “Increase” prompts, they should attempt to reinterpret (i.e., cognitively reappraise) the subsequent event cue in such a way as to feel a weaker or stronger emotional reaction than normal to the memory, respectively. Example cognitive reappraisal strategies were given for both decrease and increase instructions. For instance, participants were instructed that if they had a negative event cue about a friend forgetting their birthday, they might decrease their emotional reaction to that memory by focusing on how they still had a great time celebrating their birthday although that friend forgot. If they had to increase their emotional reaction to that event, they might focus on the feelings of sadness or disappointment they had when they realized that friend forgot. For both the maintain negative and maintain neutral conditions, participants were instructed to recall the events without trying to alter their feelings toward them. Participants practiced each possible instruction with two example events that were not used during the scan.

The 60 regulation trials (15 each of Decrease, Increase, Maintain Negative, and Maintain Neutral) were pseudorandomized such that no instruction appeared more than twice in a row; the trials were divided among four functional scanning runs. The overall design for the emotion regulation task is summarized in the left panel of Figure 1. Each trial began with a fixation cross that lasted an average of 3 sec (jittered between 1 and 7 sec). The fixation period was followed by an instruction phase, during which time a regulation prompt (Decrease, Increase, or Maintain) appeared on the screen for an average of 6 sec (jittered between 3 and 9 sec). The onset of this prompt was modeled as the start of the Instruction phase. A memory title created during the prescan session then appeared on the line below the instruction for 12 sec. The onset of this prompt was modeled as the start of the Memory Onset phase. Participants were instructed to make a button press when they felt they had the fully formed event memory in mind. Following the button press, participants were instructed to continue thinking about and elaborating on the details of the memory in accordance with the regulation instructions for that trial for the remainder of the 12 sec. This button press indicated the start of the Memory Elaboration phase. Finally, each trial ended with two 7-point rating scales that asked participants to rate Emotional Intensity and Vividness. Each rating scale appeared for a maximum of 4 sec.

Figure 1. 

(Left) Example trial for an AM task in which individuals decreased, increased, or maintained the emotional intensity associated with negative events or maintained the emotional intensity associated with neutral events. Note that the trial types were pseudorandomized such that no instruction appeared more than twice in a row. (Right) Example trial for a sentence baseline task in which participants generated a sentence with the format “X is smaller than Y is smaller than Z” for different groups of three concrete nouns and then elaborated upon the appearance and functions of the objects. Sentence baseline trials were interspersed with the AM task.

Figure 1. 

(Left) Example trial for an AM task in which individuals decreased, increased, or maintained the emotional intensity associated with negative events or maintained the emotional intensity associated with neutral events. Note that the trial types were pseudorandomized such that no instruction appeared more than twice in a row. (Right) Example trial for a sentence baseline task in which participants generated a sentence with the format “X is smaller than Y is smaller than Z” for different groups of three concrete nouns and then elaborated upon the appearance and functions of the objects. Sentence baseline trials were interspersed with the AM task.

Sentence Control Task

Sixteen trials of a sentence control task adapted from Addis, Pan, Vu, Laiser, and Schacter (2009) were divided among the four functional scanning runs and randomly interspersed with the regulation trials. The sentence control task included sets of three concrete, highly imageable and familiar nouns (selected from the Clark and Paivio extended norms; Clark & Paivio, 2004).

The overall design of the sentence control task trials mirrored that of the regulation task and is summarized in the right panel of Figure 1. Each trial began with a fixation cross in the center of the screen for an average of 3 sec (jittered between 1 and 7 sec). The sentence instruction phase, during which time the word “Sentence” appeared on the screen for an average of 6 sec (jittered between 3 and 9 sec), followed. A set of three nouns then appeared on the screen on the line underneath the “Sentence” instruction for 12 sec. Participants were instructed to put the items in physical size order and place them in a sentence with the structure “X is smaller than Y is smaller than Z.” Once participants had subvocalized the sentence, they made a button press that demarcated the end of the onset phase. The sentence onset phase controls for the memory search and integration processes in the memory onset phase. They were then instructed to think about and elaborate on the appearance and functions of the three objects for the remainder of the 12-sec trial; this period between the button press and the end of the trial will be referred to as the elaboration phase. Because the sentence elaboration phase involved visuospatial processing, it controls for the elaboration of visuospatial details during the AM task. The sentence trials ended with two rating scales lasting a maximum of 4 sec each: (a) Detail (1 = low to 7 = high) and (b) Vividness (1 = low to 7 = high).

Postscan Task

Following the scanning portion of the study, after an approximately 0.5-hr delay, participants were given a spreadsheet that included the 60 event titles, one-sentence descriptions, and ages of the AMs they recalled in the scanner. They were asked to make several ratings about each event: (a) how emotionally intense they felt about the event (1 = not at all to 7 = very), (b) how negative they felt about the event (1 = not at all to 7 = very), (c) how positive they felt about the event (1 = not at all to 7 = very), and (d) how vivid their recall of the event was (1 = not at all to 7 = vivid). The AMs were presented in the spreadsheet in the same order that participants saw them while in the scanner, and the task was self-paced.

Scanning Parameters

Images were acquired on a 3-T Siemens Tim Trio MRI scanner using a 32-channel head coil. Stimuli were presented using MacStim presentation software. All words, instructions, and rating scales used in the experiment appeared in white text (Arial 36-point font) on a black background. Stimuli were projected onto a screen located at the back of the magnet bore, and participants viewed the stimuli using a mirror attached to the head coil.

T1-weighted localizer images and a T1-weighted inversion recovery echo-planar image required for autoalignment were collected. Anatomic data were collected with a multiecho multiplanar rapidly acquired gradient-echo (MEMPRAGE) sequence (repetition time = 2200 msec; echo time = 1.64, 3.5, 5.46, 7.22 msec; flip angle = 7°; field of view = 256 × 256 mm; slice thickness = 1 mm, no gap; 1 × 1 × 1 mm resolution). Functional images were collected using a T2*-weighted EPI sequence with the following parameters: repetition time = 3000 msec, echo time = 30 msec, field of view = 216 mm, flip angle = 85°. Forty-seven interleaved coronal-oblique slices aligned perpendicular to the long axis of the hippocampus were collected in a 3 mm3 matrix (slice thickness = 3 mm).

Preprocessing and data analysis were conducted in SPM8 (Wellcome Department of Cognitive Neurology, London). Preprocessing steps were as follows: (1) slice timing correction; (2) motion correction using a six-parameter, rigid body transformation algorithm; (3) normalization to the Montreal Neurological Institute template (resampling at 3 mm isotropic voxels); and (4) spatial smoothing using a 3-mm FWHM isotropic Gaussian kernel.

Imaging Data Analysis

The memory recall phase was divided into two separate events-memory onset and elaboration-based on self-paced RTs to recall each memory. The RTs were random and highly variable (see Table 2), thereby effectively jittering the beginning of the elaboration phase (see Addis et al., 2007; Steinvorth et al., 2006, for similar design and discussion). For each individual, the following events were modeled and analyzed using the general linear model approach on a voxel-by-voxel basis: (a) Decrease Instruction, (b) Increase Instruction, (c) Maintain Negative Instruction, (d) Maintain Neutral Instruction, (e) Sentence Instruction, (f) Decrease Onset, (g) Increase Onset, (h) Maintain Negative Onset, (i) Maintain Neutral Onset, (j) Sentence Onset, (k) Decrease Elaboration, (l) Increase Elaboration, (m) Maintain Negative Elaboration, (n) Maintain Neutral Elaboration, and (o) Sentence Elaboration. Contrasts between the various trial types were computed as described below, and the resulting contrast images were entered into second-level, random-effects analyses that used a statistical threshold of p < .001, uncorrected, and a 5-voxel threshold extent. Because we had a priori hypotheses about how reappraisal instructions would modulate activity in the amygdala (following, e.g., Ochsner et al., 2004), we applied a small volume correction using an anatomically defined mask of the bilateral amygdala from the MARINA toolbox (Walter et al., 2003). Regions of the amygdala resulting from this small volume correction are noted in the relevant tables.

Table 2. 

Behavioral Characteristics of Negative and Neutral AMs that Participants Were Instructed to Decrease, Increase, or Maintain during the Scan Session

Trial Type
Scan Behavioral Ratings
RT (sec)
Intensity
Vividness
Decrease Neg 3.63 (1.46) 3.69 (0.92) 4.75 (0.81) 
Increase Neg 3.44 (1.43) 5.19 (0.58) 5.34 (0.73) 
Maintain Neg 3.46 (1.47) 4.65 (0.79) 4.96 (0.75) 
Maintain Neutral 3.04 (1.13) 2.79 (1.09) 4.74 (0.77) 
Trial Type
Scan Behavioral Ratings
RT (sec)
Intensity
Vividness
Decrease Neg 3.63 (1.46) 3.69 (0.92) 4.75 (0.81) 
Increase Neg 3.44 (1.43) 5.19 (0.58) 5.34 (0.73) 
Maintain Neg 3.46 (1.47) 4.65 (0.79) 4.96 (0.75) 
Maintain Neutral 3.04 (1.13) 2.79 (1.09) 4.74 (0.77) 

Standard deviations are presented in parentheses.

RESULTS

Scan Behavioral Results

The behavioral results from the scan session are summarized in Table 2.

RT

A within-subject ANOVA examining the effect of emotion regulation instruction on RT to access an AM revealed a main effect of instruction, F(3, 63) = 7.98, p < .001, partial η2 = .28, with significantly faster RT for the maintain neutral condition than any of the negative AM regulation conditions, ps < .01, as well as a trend for longer RTs in the decrease condition than AMs in the increase condition, p < .10. Because these RT differences would mean different mean lengths of the onset phase depending on condition, we included RT as a parametric regressor for the onset phase on a trial-by-trial basis in the first-level analysis for each participant.

Memory Qualities

As expected, there was a main effect of Instruction on emotional intensity, F(3, 63) = 56.80, p < .001, partial η2 = .73 (Figure 2). Post hoc pairwise comparisons confirmed that neutral AMs were rated as lower in intensity than any of the negative AM conditions, ps < .001, and intensity for negative AMs was lowest in the decrease condition, higher in the maintain condition, and highest in the increase condition, all ps < .001.

Figure 2. 

Average emotional intensity ratings (on a 1–7 scale) for negative and neutral AMs before the scan (i.e., when no regulation instructions were given), during the scan (when regulation instructions were given), and approximately 0.5 hr after the scan (in the absence of any regulation instructions).

Figure 2. 

Average emotional intensity ratings (on a 1–7 scale) for negative and neutral AMs before the scan (i.e., when no regulation instructions were given), during the scan (when regulation instructions were given), and approximately 0.5 hr after the scan (in the absence of any regulation instructions).

Consistent with predictions, regulation instruction also influenced vividness ratings, F(3, 63) = 7.61, p < .001, partial η2 = .27. Post hoc pairwise comparisons confirmed that negative events in the increase condition were rated as more vivid than any other memories (ps < .006); negative events in the maintain condition were rated as significantly more vivid than those in the decrease condition (p = .003) and trended toward being more vivid than neutral events (p < .10). The vividness of negative memories in the decrease condition was equivalent to that of neutral memories (p = .97).

Imaging Results

Identifying the AM Retrieval Network

We first compared the neural activity during the neutral maintain condition to the activity during the sentence control task to establish that regions previously associated with AM recall were present in our task (see Figure 3). Consistent with prior research on the AM retrieval network (see Cabeza & St. Jacques, 2007; Svoboda et al., 2006, for reviews), the onset phase of AM (i.e., in the time between the appearance of the memory cue and the button press indicating that a fully formed memory was in mind; see Figure 3, middle) was associated with activity in several left-lateralized regions of ventrolateral (BA 44 and BA 47) pFC regions, left lateral temporal lobe regions (BA 21/BA 22), left posterior cingulate (BA 30), bilateral occipital lobe (BA 18), and bilateral cuneus (BA 17/BA 18). During memory elaboration (see Figure 3, bottom), activation was present in right-lateralized regions of ventrolateral pFC (BA 47) and frontal pole (BA 10), as well as throughout the medial pFC (BA 8, BA 9, and BA 10). Activity was also evident throughout the bilateral temporal (BA 21 and BA 22) and parietal (BA 5 and BA 40) lobes and in left posterior cingulate (BA 23/BA 31), left fusiform gyrus, and left precuneus (BA 31).

Figure 3. 

Neural activity for the maintain neutral > sentence and maintain negative > maintain neutral contrasts during the instruction, onset, and elaboration phases. Right-most column shows saggital cutaways for each phase. Activity is significant at p < .001 and a 5-voxel threshold extent.

Figure 3. 

Neural activity for the maintain neutral > sentence and maintain negative > maintain neutral contrasts during the instruction, onset, and elaboration phases. Right-most column shows saggital cutaways for each phase. Activity is significant at p < .001 and a 5-voxel threshold extent.

Retrieving Negative versus Neutral AMs

Replicating previous findings demonstrating greater right-lateralized activity during emotional AM recall (see Cabeza & St. Jacques, 2007, for a review), at memory onset, negative AM retrieval recruited more right ventrolateral pFC (BA 44) and bilateral frontal pole (BA 10), as well as right lateral temporal regions (BA 37/BA 19, BA 39, BA 41, and BA 42/BA 22) and bilateral precuneus (BA 7) than did neutral AM retrieval (see Figure 3, middle).

Unlike the onset phase, which recruited primarily right-lateralized activity during negative AM recall, elaborating upon negative AMs disproportionately engaged mostly left-lateralized regions (see Figure 3, bottom), including in dorsal (BA 45/ BA 46) and ventral (BA 47) lateral pFC and lateral temporal lobe areas. Negative AM elaboration also engaged medial pFC (BA 6) and a number of visuospatial processing regions (e.g., bilateral cuneus [BA 17, BA 18, and BA 31], left fusiform [BA 37] and right lingual [BA 18] gyri, bilateral inferior [BA 18 and BA 19] and left middle [BA 19 and BA 37] occipital gyri).

Emotion Regulation during AM Recall

Having generally replicated prior findings with regard to the AM retrieval network and its modulation by emotion (reviewed by Cabeza & St. Jacques, 2007; Svoboda et al., 2006), we next analyzed the neural activity present as individuals down- and up-regulated (vs. maintained) the negative emotions associated with their AMs. For each phase, we will first report the results for the decrease and increase conditions compared with the maintain condition and then report the results for the direct comparisons between the decrease and increase trials.

Regulation during Recall: Instruction Phase

Reappraising versus Maintaining Emotions

We explored whether there was any anticipatory activity evident as individuals prepared to increase or decrease negative AMs versus to maintain negative AMs or vice versa. The overall pattern revealed that being instructed to reappraise negative emotions engaged more regions than being instructed to maintain emotions, with the increase condition revealing the most extensive activity. More specifically, during the decrease (vs. maintain) instruction condition, regions of left dorsolateral pFC (BA 47) and right anterior cingulate (BA 24) previously implicated in the reappraisal of negative images (Ochsner et al., 2004) were activated, as was right medial pFC (BA 6), and bilateral temporal (BA 22/BA 21) and occipital (BA 19/BA 18) cortices (see Figure 4A). Although a conjunction analysis between the decrease > maintain and increase > maintain contrasts during the Instruction phase did not reveal any statistically significant overlap in clusters of activations, right anterior cingulate (BA 32/BA 24), bilateral temporal (BA 42/BA 22/BA 39/BA 41), and right occipital (BA 31/BA 18/BA 19) lobe activity was also present in the increase (vs. maintain) instruction contrast. This contrast also revealed more extensive activity in regions throughout pFC (see Figure 4B). Areas of right dorsolateral pFC (BA 9), left medial pFC (BA 8), and bilateral frontal pole (BA 10) were all engaged more by the increase than maintain instruction. Few regions were more active during the maintain instruction phase; only a single cluster of left posterior cingulate (BA 31) and two clusters of left caudate nucleus were engaged to a greater extent in the maintain instruction than the decrease instruction phase, and only a region of left cerebellum was engaged to a greater extent than in the increase instruction phase.

Figure 4. 

(A) Neural activity for the decrease and maintain trials during the negative AM instruction phase. (B) Neural activity for the increase and maintain trials during the negative AM instruction phase. (C) Neural activity for the decrease and increase trials during the negative AM instruction phase. Plotted activity is significant at p < .001 and a 5-voxel threshold extent.

Figure 4. 

(A) Neural activity for the decrease and maintain trials during the negative AM instruction phase. (B) Neural activity for the increase and maintain trials during the negative AM instruction phase. (C) Neural activity for the decrease and increase trials during the negative AM instruction phase. Plotted activity is significant at p < .001 and a 5-voxel threshold extent.

Decreasing versus Increasing Emotions

A direct contrast of the decrease and increase instruction phases confirmed that activity was more widespread during increase than decrease instructions (see Figure 4C; Table 3). Most striking were a number of regions in pFC, including left ventrolateral (BA 47), dorsolateral (BA 9), and orbito-frontal (BA 11) areas and right-lateralized frontal pole (BA 10). Regions previously associated with emotion processing and regulation, such as right insula (BA 13) and bilateral anterior cingulate gyrus (BA 32/BA 24, BA 23, and BA 25) were also engaged more during the “Increase” than “Decrease” instructions, as were posterior areas important for visuospatial processing and representation (right cuneus [BA 31], left precuneus [BA 31/BA 7], left posterior cingulate gyrus [BA 31/BA 24/BA 23] and inferior parietal lobe [BA 40]).

Table 3. 

Group Activations for the Increase > Decrease Instruction Contrast

Lobe/Region
BA
Hemisphere
Talairach
t
k
x
y
z
Frontal 
Inferior frontal gyrus 47 −32 23 −15 4.68 
47 −26 27 −6 4.60 
47 −30 33 −8 4.20 
Middle frontal gyrus 10 34 60 −10 4.51 31 
Medial frontal gyrus 10 61 14 3.77 
Superior frontal gyrus 11 −24 50 −11 4.35 13 
−12 46 31 3.95 
18 52 32 4.20 
 
Parietal 
Inferior parietal lobe 40 −28 −45 28 4.86 
Precuneus 31/7 −20 −47 36 5.06 10 
 
Occipital 
Cuneus 31 26 −73 4.66 
 
Limbic 
Insula 13 32 20 16 4.17 
Cingulate gyrus 31 −24 −33 40 5.93 13 
24/23 −20 −20 27 5.38 14 
32/24 −24 25 25 4.22 
24/23 22 27 4.92 
25 −5 4.51 
32 35 −7 4.44 
 
Other 
Basal ganglia  22 −7 22 4.68 
 −28 16 4.13 
 −24 22 15 3.76 
Lobe/Region
BA
Hemisphere
Talairach
t
k
x
y
z
Frontal 
Inferior frontal gyrus 47 −32 23 −15 4.68 
47 −26 27 −6 4.60 
47 −30 33 −8 4.20 
Middle frontal gyrus 10 34 60 −10 4.51 31 
Medial frontal gyrus 10 61 14 3.77 
Superior frontal gyrus 11 −24 50 −11 4.35 13 
−12 46 31 3.95 
18 52 32 4.20 
 
Parietal 
Inferior parietal lobe 40 −28 −45 28 4.86 
Precuneus 31/7 −20 −47 36 5.06 10 
 
Occipital 
Cuneus 31 26 −73 4.66 
 
Limbic 
Insula 13 32 20 16 4.17 
Cingulate gyrus 31 −24 −33 40 5.93 13 
24/23 −20 −20 27 5.38 14 
32/24 −24 25 25 4.22 
24/23 22 27 4.92 
25 −5 4.51 
32 35 −7 4.44 
 
Other 
Basal ganglia  22 −7 22 4.68 
 −28 16 4.13 
 −24 22 15 3.76 

By contrast, when examining the decrease > increase contrast, no regions survived our statistical threshold of p < .001 and a 5-voxel cluster extent (but see Table 4 for regions that arose at a reduced threshold of p < .005).

Table 4. 

Group Activations for the Decrease > Increase Instruction Contrast

Lobe/Region
BA
Hemisphere
Talairach
t
k
x
y
z
Medial Temporal 
Parahippocampal gyrus  −16 −41 −3 3.84 
Hippocampus  −28 −22 −11 2.95 
 
Other Temporal 
Fusiform gyrus  −30 −36 −12 3.84 
 
Limbic 
Cingulate gyrus 30 −20 −54 14 3.26 
 
Occipital 
Middle occipital gyrus 37/19 38 −74 −8 3.31 
 
Other 
Cerebellum  16 −59 −7 3.70 
Lobe/Region
BA
Hemisphere
Talairach
t
k
x
y
z
Medial Temporal 
Parahippocampal gyrus  −16 −41 −3 3.84 
Hippocampus  −28 −22 −11 2.95 
 
Other Temporal 
Fusiform gyrus  −30 −36 −12 3.84 
 
Limbic 
Cingulate gyrus 30 −20 −54 14 3.26 
 
Occipital 
Middle occipital gyrus 37/19 38 −74 −8 3.31 
 
Other 
Cerebellum  16 −59 −7 3.70 

Note that activity in reported regions was significant only at a more liberal threshold of p < .005 and a 5-voxel cluster extent.

Regions reported are significant at p < .005, k ≥ 5 voxels.

Regulation during Recall: Onset Phase

Reappraising versus Maintaining Negative Emotions

There was a relative paucity of regions showing statistically greater activity for the increase than maintain conditions during the onset phase, with only a small cluster of BG revealed (see Figure 5B). By contrast and in line with our expectations based on the results of image-based reappraisal studies (e.g., Ochsner et al., 2004), when comparing activity in the decrease and maintain conditions (Figure 5A), regions of the bilateral dorsal (BA 46) and ventral (BA 11, BA 44, and BA 47) pFC and of the left frontal pole (BA 10) were engaged more by the decrease condition, as were bilateral regions of temporal cortex (BA 21, BA 22, BA 38, and BA 39), left hippocampus, and bilateral posterior cingulate cortex (BA 30 and BA 23). Contrary to expectations, emotion processing regions (left medial pFC [BA 6] and left insula [BA 13]) and visuospatial (left cuneus [BA 18 and BA 30], right precuneus [BA 31], right angular [BA 39], and bilateral occipital [BA 18 and BA 19] gyri), previously associated with enhanced emotional intensity during cognitive reappraisal (e.g., Ochsner et al., 2004) and AM (Botzung et al., 2010) tasks, were more active as individuals accessed negative events that they were instructed to down-regulate versus maintain.

Figure 5. 

(A) Neural activity for the decrease and maintain trials during negative AM onset. Saggital slice shows a region of left hippocampus (Tal: x = −26, y = −35, z = 0) that was more active during the decrease than maintain trials. (B) Neural activity for the increase and maintain trials during negative AM onset. Saggital slice shows a region of right amygdala (Tal: x = 30, y = −3, z = −17) as well as two regions of right hippocampus (Tal: x = 28, y = −14, z = −14; Tal: x = 30, y = −29, z = −7) that were more active during the maintain than increase trials. (C) Neural activity for the decrease and increase trials during negative AM onset. Saggital slice shows a region of right amygdala (Tal: x = 30, y = 1, z = −17) as well as two regions of right hippocampus (Tal: x = 26, y = −33, z = −8; Tal: x = 32, y = −16, z = −14) that were more active during the decrease than increase trials. Activity is significant at p < .001 and a 5-voxel threshold extent.

Figure 5. 

(A) Neural activity for the decrease and maintain trials during negative AM onset. Saggital slice shows a region of left hippocampus (Tal: x = −26, y = −35, z = 0) that was more active during the decrease than maintain trials. (B) Neural activity for the increase and maintain trials during negative AM onset. Saggital slice shows a region of right amygdala (Tal: x = 30, y = −3, z = −17) as well as two regions of right hippocampus (Tal: x = 28, y = −14, z = −14; Tal: x = 30, y = −29, z = −7) that were more active during the maintain than increase trials. (C) Neural activity for the decrease and increase trials during negative AM onset. Saggital slice shows a region of right amygdala (Tal: x = 30, y = 1, z = −17) as well as two regions of right hippocampus (Tal: x = 26, y = −33, z = −8; Tal: x = 32, y = −16, z = −14) that were more active during the decrease than increase trials. Activity is significant at p < .001 and a 5-voxel threshold extent.

There was very little enhancement of activity when maintaining rather than decreasing negative AMs during the onset period (Figure 5A). Only a small cluster in the left frontal pole (BA 10) as well as two clusters in the left caudate nucleus were more active during the maintain negative than decrease onset conditions. By contrast and contrary to our expectations, there was greater activity evident for the maintain negative > increase contrast in a number of regions during the onset phase (Figure 5B), including throughout bilateral pFC (dorsal [BA 9 and BA 46], ventral [BA 47], and orbito-frontal [BA 11] regions), bilateral posterior cingulate gyrus (BA 23, BA 30, and BA 31), and right-lateralized medial (hippocampus, parahippocampal and fusiform gyri, amygdale), and bilateral temporal lobes (BA 21, BA 22, BA 38, and BA 39). In addition to greater amygdala activity, the maintain negative condition also engaged other emotion processing regions bilaterally, including insula (BA 13), and medial pFC (BA 6 and BA 10) to a greater extent than the increase negative condition during the memory onset phase. Finally, a number of posterior regions were also revealed in this contrast, including sensory processing regions in both the occipital (bilateral precuneus [BA 7, BA 19, and BA 31], left lingual gyrus [BA 19], bilateral occipital gyri [BA 18 and BA 19]) and inferior (left BA 40) and superior parietal (bilateral BA 7) lobes.

Decreasing versus Increasing Negative Emotions

A direct contrast of the decrease and increase conditions during the onset phase confirmed that the decrease condition engaged more activity (Table 5; Figure 5C); this whole-brain contrast of decrease > increase revealed reappraisal and retrieval-related regions throughout pFC (right dorsal [BA 6, BA 9, and BA 46] and bilateral ventral lateral [BA 11/BA 47] pFC and left frontal pole [BA 10]) and retrieval-related regions in bilateral posterior cingulate gyrus (BA 24 and BA 31), primarily right-lateralized medial (hippocampus, fusiform, and parahippocampal gyri) and bilateral temporal (BA 21, BA 22, and BA 39) lobes. Contrary to our hypotheses (but in line with the above-reported results contrasting the reappraisal and maintain negative onset conditions), the decrease condition was also associated with greater activity in primarily left-lateralized emotional processing regions (medial pFC [BA 6, BA 9, and BA 11] and amygdale) during the onset phase. Accessing memories in the decrease (vs. increase) condition was further associated with increased activity in visual processing regions (right precuneus [BA 7 and BA 31], bilateral cuneus [BA 18 and BA 23], and bilateral occipital gyri [BA 18 and BA 19]). On the other hand, activity revealed by the increase > decrease contrast was limited to relatively small clusters in left insula (BA 13) and right anterior (BA 24) and left posterior (BA 23) cingulate gyrus (Table 6).

Table 5. 

Group Activations for the Decrease > Increase Onset Contrast

Lobe/Region
BA
Hemisphere
Talairach
t
k
Present in Condition × Phase Interaction
x
y
z
Frontal 
Inferior frontal gyrus 47 42 34 −12 6.34 535 10 mm 
13 32 11 −11 5.08 7 mm 
46 50 26 15 4.97 92 2 mm 
45 51 27 4.88  
Medial frontal gyrus −2 16 47 6.41 623 8 mm 
−6 46 34 4.61 22  
−8 42 18 4.47 19  
11 −6 52 −13 5.47 106 4 mm 
10 53 10 4.03  
Middle frontal gyrus 6/9 −46 39 4.21  
Superior frontal gyrus 10 −8 61 19 5.68 118 3 mm 
52 29 4.92 25  
Precentral gyrus 44 −46 10 7.91 1698 6 mm 
 
Medial Temporal 
Hippocampus  32 −16 −14 6.62 30 3 mm 
 26 −33 −8 6.09 46 6 mm 
Parahippocampal gyrus  −22 −37 −7 9.92 3448  
30/19 22 −39 −3 4.68 10  
30 18 −45 3.97  
 
Other Temporal 
Superior temporal gyrus 22 −48 −25 9.23 1307  
Middle temporal gyrus 39 −50 −67 27 4.96 94  
21 55 −6 −13 6.16 314 8 mm 
21 65 −41 4.71 20  
22 46 −35 4.67 56 8 mm 
21/22 61 −48 10 4.41 21  
Fusiform gyrus 37 42 −51 −8 4.10  
 
Parietal 
Superior parietal lobe 28 −61 53 3.92  
Precuneus 28 −52 49 3.76  
31 14 −65 20 4.15 11  
31 10 −71 22 3.74  
 
Occipital 
Inferior occipital gyrus 18 36 −80 −6 7.40 1311  
Middle occipital gyrus 19 −26 −73 20 4.16  
Superior occipital gyrus 19 −32 −70 31 5.61 23  
19 32 −68 29 4.80 96 6 mm 
Cuneus 23 −6 −71 13 4.64 63  
18 −12 −83 13 3.80  
18 10 −73 17 3.89 11  
 
Limbic 
Amygdala  −30 −4 −12 6.18 2a  
 −28 −17 4.70 4a  
 −18 −6 −13 4.26 3a  
 30 −17 5.16 7a  
 30 −17 5.16  
Cingulate gyrus 31 −2 −29 38 7.00 92 9 mm 
24 −4 −4 28 3.97  
24 27 6.71 71  
31 −35 29 4.77 36  
 
Other 
Basal ganglia  −6 −2 5.13  
 −18 −6 −6 5.10 17  
Cerebellum  −4 −60 −36 4.69  
 −26 −68 −39 4.80  
 −28 −56 −22 4.93  
 −54 −26 7.60 23 3 mm 
 −72 −10 4.91 12  
Hypothalamus  – −10 −10 4.17  
Lobe/Region
BA
Hemisphere
Talairach
t
k
Present in Condition × Phase Interaction
x
y
z
Frontal 
Inferior frontal gyrus 47 42 34 −12 6.34 535 10 mm 
13 32 11 −11 5.08 7 mm 
46 50 26 15 4.97 92 2 mm 
45 51 27 4.88  
Medial frontal gyrus −2 16 47 6.41 623 8 mm 
−6 46 34 4.61 22  
−8 42 18 4.47 19  
11 −6 52 −13 5.47 106 4 mm 
10 53 10 4.03  
Middle frontal gyrus 6/9 −46 39 4.21  
Superior frontal gyrus 10 −8 61 19 5.68 118 3 mm 
52 29 4.92 25  
Precentral gyrus 44 −46 10 7.91 1698 6 mm 
 
Medial Temporal 
Hippocampus  32 −16 −14 6.62 30 3 mm 
 26 −33 −8 6.09 46 6 mm 
Parahippocampal gyrus  −22 −37 −7 9.92 3448  
30/19 22 −39 −3 4.68 10  
30 18 −45 3.97  
 
Other Temporal 
Superior temporal gyrus 22 −48 −25 9.23 1307  
Middle temporal gyrus 39 −50 −67 27 4.96 94  
21 55 −6 −13 6.16 314 8 mm 
21 65 −41 4.71 20  
22 46 −35 4.67 56 8 mm 
21/22 61 −48 10 4.41 21  
Fusiform gyrus 37 42 −51 −8 4.10  
 
Parietal 
Superior parietal lobe 28 −61 53 3.92  
Precuneus 28 −52 49 3.76  
31 14 −65 20 4.15 11  
31 10 −71 22 3.74  
 
Occipital 
Inferior occipital gyrus 18 36 −80 −6 7.40 1311  
Middle occipital gyrus 19 −26 −73 20 4.16  
Superior occipital gyrus 19 −32 −70 31 5.61 23  
19 32 −68 29 4.80 96 6 mm 
Cuneus 23 −6 −71 13 4.64 63  
18 −12 −83 13 3.80  
18 10 −73 17 3.89 11  
 
Limbic 
Amygdala  −30 −4 −12 6.18 2a  
 −28 −17 4.70 4a  
 −18 −6 −13 4.26 3a  
 30 −17 5.16 7a  
 30 −17 5.16  
Cingulate gyrus 31 −2 −29 38 7.00 92 9 mm 
24 −4 −4 28 3.97  
24 27 6.71 71  
31 −35 29 4.77 36  
 
Other 
Basal ganglia  −6 −2 5.13  
 −18 −6 −6 5.10 17  
Cerebellum  −4 −60 −36 4.69  
 −26 −68 −39 4.80  
 −28 −56 −22 4.93  
 −54 −26 7.60 23 3 mm 
 −72 −10 4.91 12  
Hypothalamus  – −10 −10 4.17  

Regions that were present in the Condition × Phase interaction examining the onset and elaboration phases are noted in the last column with the distance between the peak evident in the t test and the interaction.

aRegions revealed by a small volume correction applied to an anatomical mask of the bilateral amygdala.

Table 6. 

Group Activations for the Increase > Decrease Onset Contrast

Lobe/Region
BA
Hemisphere
Talairach
t
k
Present in Condition × Phase Interaction
x
y
z
Limbic 
Insula 13 −28 −6 26 4.24 13  
Cingulate gyrus 23 −10 −36 17 6.36  
24 24 15 27 4.25  
 
Parietal 
Postcentral gyrus 3/2/1 57 −24 34 4.24  
 
Other 
Basal ganglia  −22 18 16 6.83 104 6 mm 
 −18 −11 23 5.39 18  
 20 14 16 4.59  
 16 −7 19 4.48 11  
Cerebellum  −32 −68 −30 4.78 38  
Thalamus  −6 −3 15 3.96  
 14 −3 13 3.93 10  
Lobe/Region
BA
Hemisphere
Talairach
t
k
Present in Condition × Phase Interaction
x
y
z
Limbic 
Insula 13 −28 −6 26 4.24 13  
Cingulate gyrus 23 −10 −36 17 6.36  
24 24 15 27 4.25  
 
Parietal 
Postcentral gyrus 3/2/1 57 −24 34 4.24  
 
Other 
Basal ganglia  −22 18 16 6.83 104 6 mm 
 −18 −11 23 5.39 18  
 20 14 16 4.59  
 16 −7 19 4.48 11  
Cerebellum  −32 −68 −30 4.78 38  
Thalamus  −6 −3 15 3.96  
 14 −3 13 3.93 10  

Regions that were present in the Condition × Phase interaction examining the onset and elaboration phases are noted in the last column with the distance between the peak evident in the t test and the interaction.

Regulation during Recall: Elaboration Phase

Reappraising versus Maintaining Negative Emotions

Contrasts comparing the reappraisal conditions to the maintain conditions as individuals elaborated upon the details of their negative AMs revealed a pattern opposite to that observed during the memory onset phase. Despite revealing greater activity during the onset phase, the decrease > maintain contrast in the elaboration phase revealed only two regions in pFC (left middle [BA 8] and right superior [BA 9] frontal gyri), one in right middle temporal gyrus (BA 21), and one in left angular gyrus (BA 39) that were more active when decreasing than maintaining the negative emotions associated with AMs. However, the reverse contrast (maintain negative vs. decrease negative) revealed greater activity in regions previously associated with memory retrieval (left-lateralized ventrolateral [BA 44] pFC, bilateral middle frontal gyrus [BA 6], and left inferior pFC [BA 46] and temporal [BA 37] cortices), emotion processing (left medial pFC [BA 6]), and the processing and representation of visual information (bilateral middle occipital gyrus [BA 18 and BA 31], right cuneus [BA 31], bilateral inferior parietal lobe [BA 40], and left fusiform gyrus [BA 37]).

The contrast comparing neural activity as individuals elaborated upon negative AMs in the increase (vs. maintain) was more in line with our expectations about how up-regulation might modulate neural activity during recall (see Figure 6B). For example, the increase condition engaged significantly greater activity in regions known to support both memory retrieval and cognitive reappraisal (primarily left-lateralized ventrolateral pFC [BA 11, BA 44/BA 45, and BA 47] and left frontal pole [BA 10]), as well as regions more specific to memory retrieval (right hippocampus and bilateral superior [BA 38 and BA 39] and middle [BA 21 and BA 22] temporal gyri). In addition, as hypothesized, increasing (vs. maintaining) the negative emotions associated with AMs engaged regions associated with emotional processing (left medial pFC [BA 6, BA 8, and BA 9] and left insula [BA 13]) and visual processing (left precuneus [BA 7 and BA 19], left lingual [BA 18] and bilateral occipital [BA 19 and BA 39] gyri, and posterior cingulate gyrus [BA 24]). In contrast, maintaining negative emotions during the elaboration phase engaged fewer regions to a greater extent than increasing, primarily in the left medial (BA 6) and bilateral middle frontal gyrus (BA 6, BA 10, and BA 11), right inferior parietal lobe (BA 40), and bilateral anterior cingulate gyrus (BA 24 and BA 32).

Figure 6. 

(A) Neural activity for the decrease and maintain trials during negative AM elaboration. Saggital slice shows a region of left dorsomedial pFC (Tal: x = −2, y = 8, z = 49) that was more active during the maintain than decrease trials. (B) Neural activity for the increase and maintain trials during negative AM elaboration. Saggital slice shows two regions of right hippocampus (Tal: x = 30, y = −14, z = −16; Tal: x = 30, y = −37, z = 0) that were more active during the increase than maintain trials. (C) Neural activity for the decrease and increase trials during negative AM elaboration. Saggital slice shows a region of left amygdala (Tal: x = −28, y = −6, z = −13) that was more active during the decrease than increase trials. Activity is significant at p < .001 and a 5-voxel threshold extent.

Figure 6. 

(A) Neural activity for the decrease and maintain trials during negative AM elaboration. Saggital slice shows a region of left dorsomedial pFC (Tal: x = −2, y = 8, z = 49) that was more active during the maintain than decrease trials. (B) Neural activity for the increase and maintain trials during negative AM elaboration. Saggital slice shows two regions of right hippocampus (Tal: x = 30, y = −14, z = −16; Tal: x = 30, y = −37, z = 0) that were more active during the increase than maintain trials. (C) Neural activity for the decrease and increase trials during negative AM elaboration. Saggital slice shows a region of left amygdala (Tal: x = −28, y = −6, z = −13) that was more active during the decrease than increase trials. Activity is significant at p < .001 and a 5-voxel threshold extent.

Decreasing versus Increasing Negative Emotions

Directly comparing the decrease > increase conditions as individuals elaborated on the details of their negative AMs (see Figure 6C) confirmed that the increase condition recruited the greatest neural activity during the elaboration phase. Few regions were more engaged during decrease than increase trials; these regions included small clusters of bilateral superior frontal gyrus (BA 9 and BA 10) and right superior temporal gyrus (BA 22; see Table 7).

Table 7. 

Group Activations for the Decrease > Increase Elaboration Contrast

Lobe/Region
BA
Hemisphere
Talairach
t
k
Present in Condition × Phase Interaction
x
y
z
Frontal 
Superior frontal gyrus 10 −32 58 −6 4.48  
20 50 25 3.73  
 
Temporal 
Superior temporal gyrus 22 65 −25 4.48  
 
Other 
Basal ganglia  16 20 5.04 20 3 mm 
Lobe/Region
BA
Hemisphere
Talairach
t
k
Present in Condition × Phase Interaction
x
y
z
Frontal 
Superior frontal gyrus 10 −32 58 −6 4.48  
20 50 25 3.73  
 
Temporal 
Superior temporal gyrus 22 65 −25 4.48  
 
Other 
Basal ganglia  16 20 5.04 20 3 mm 

Regions that were present in the Condition × Phase interaction examining the onset and elaboration phases are noted in the last column with the distance between the peak evident in the t test and the interaction.

The reverse contrast, however, revealed that several regions that were more active as individuals elaborated on their negative AMs that had appeared with increase (vs. decrease) regulation instructions (see Figure 6C; Table 8). These regions included primarily left-lateralized dorsal (BA 45) and ventrolateral (BA 11, BA 44, and BA 47) pFC. In addition, several regions of the MTLs (right hippocampus, left parahippocampal [BA 34], left fusiform gyri, left amygdale), lateral temporal cortices (bilateral middle [BA 21, BA 39/BA 19] and left superior [BA 22 and BA 38] temporal gyri), and posterior cingulate (BA 31 and BA 30/BA 23) were engaged more by the increase than decrease trials during the elaboration phase. The same was true of visual processing regions (bilateral precuneus [BA 31], left cuneus [BA 18], and bilateral middle occipital gyrus [BA 19]).

Table 8. 

Group Activations for the Increase > Decrease Elaboration Contrast

Lobe/Region
BA
Hemisphere
Talairach
t
k
Present in Condition × Phase Interaction
x
y
z
Frontal 
Inferior frontal gyrus 45/44 −38 11 22 6.78 148  
45 −53 22 14 3.87  
47 −34 30 −12 4.83 12  
47 −42 27 −3 4.29 22  
47 −38 21 −13 3.90  
47 28 13 −17 4.54 2 mm 
47 36 31 −2 3.95 4 mm 
Medial frontal gyrus 6/32 −4 10 47 6.27 256 3 mm 
11 −10 48 −12 4.55 16 2 mm 
Middle frontal gyrus −44 44 4.42 20  
Superior frontal gyrus −6 20 52 4.45 14  
 
Medial Temporal 
Hippocampus  26 −12 −15 4.93 20 9 mm 
 28 −33 4.32 2 mm 
Parahippocampal gyrus 34 −16 −10 −15 4.70 15  
 
Other Temporal 
Middle temporal gyrus 21 −53 −31 4.84 28  
21 −50 −10 −10 4.34 23  
21 −53 −20 −2 4.03  
21 53 −17 4.41 7 mm 
39/19 32 −67 20 4.33  
Superior temporal gyrus 22 −50 −46 13 6.24 266 6 mm 
38 −50 −2 −10 4.23 8 mm 
Fusiform gyrus  −46 −37 −12 7.25 682  
 
Parietal 
Precuneus 31 −10 −45 35 4.54 12 2 mm 
31 −65 27 4.65 15  
 
Occipital 
Middle occipital gyrus 19 −32 −91 6.16 381  
19 38 −72 −6 6.28 671  
Cuneus 18 −8 −79 17 3.99  
 
Limbic 
 Amygdala −28 −6 −13 5.00 19  
Cingulate gyrus 31 −2 −67 13 4.39 14  
31 −4 −37 35 4.53 27 0 mm 
30/23 −14 −54 8.66 810 10 mm 
 
Other 
Cerebellum  −54 −28 5.60 13 0 mm 
 −18 25 3.91  
Thalamus  −2 −15 4.63 20 4 mm 
Lobe/Region
BA
Hemisphere
Talairach
t
k
Present in Condition × Phase Interaction
x
y
z
Frontal 
Inferior frontal gyrus 45/44 −38 11 22 6.78 148  
45 −53 22 14 3.87  
47 −34 30 −12 4.83 12  
47 −42 27 −3 4.29 22  
47 −38 21 −13 3.90  
47 28 13 −17 4.54 2 mm 
47 36 31 −2 3.95 4 mm 
Medial frontal gyrus 6/32 −4 10 47 6.27 256 3 mm 
11 −10 48 −12 4.55 16 2 mm 
Middle frontal gyrus −44 44 4.42 20  
Superior frontal gyrus −6 20 52 4.45 14  
 
Medial Temporal 
Hippocampus  26 −12 −15 4.93 20 9 mm 
 28 −33 4.32 2 mm 
Parahippocampal gyrus 34 −16 −10 −15 4.70 15  
 
Other Temporal 
Middle temporal gyrus 21 −53 −31 4.84 28  
21 −50 −10 −10 4.34 23  
21 −53 −20 −2 4.03  
21 53 −17 4.41 7 mm 
39/19 32 −67 20 4.33  
Superior temporal gyrus 22 −50 −46 13 6.24 266 6 mm 
38 −50 −2 −10 4.23 8 mm 
Fusiform gyrus  −46 −37 −12 7.25 682  
 
Parietal 
Precuneus 31 −10 −45 35 4.54 12 2 mm 
31 −65 27 4.65 15  
 
Occipital 
Middle occipital gyrus 19 −32 −91 6.16 381  
19 38 −72 −6 6.28 671  
Cuneus 18 −8 −79 17 3.99  
 
Limbic 
 Amygdala −28 −6 −13 5.00 19  
Cingulate gyrus 31 −2 −67 13 4.39 14  
31 −4 −37 35 4.53 27 0 mm 
30/23 −14 −54 8.66 810 10 mm 
 
Other 
Cerebellum  −54 −28 5.60 13 0 mm 
 −18 25 3.91  
Thalamus  −2 −15 4.63 20 4 mm 

Regions that were present in the Condition × Phase interaction examining the onset and elaboration phases are noted in the last column with the distance between the peak evident in the t test and the interaction.

Condition by Phase Interaction

The results of our t-test analyses for each phase suggested that down- and up-regulation might engage neural regions over a different time course, with down-regulation engaging the greatest neural activity during the memory onset phase and up-regulation during the memory elaboration phase. We further examined this possibility by submitting the first-level reappraisal > maintain negative contrast images to a second-level 2 (Reappraisal Condition: Decrease, Increase) × 3 (Phase: Instruction, Onset, Elaboration) repeated-measures ANOVA. Two follow-up interaction contrasts investigated the interaction of condition and the onset and elaboration phases given that these were the phases in which condition-based patterns differed based on the t-test analyses (see Figure 7). Each contrast used an inclusive mask from the 2 × 3 ANOVA (mask p < .001) and a statistical threshold of p < .001 and a 5-voxel threshold extent. The first contrast examined which regions were more active for the decrease condition in the memory onset phase and increase condition in the memory elaboration phase (i.e., [decrease onset > decrease elaboration] > [increase onset > increase elaboration]). Several of the regions revealed by this contrast were similar to the regions revealed by the t-test analyses and are noted in Tables 5 and 7. Consistent with our t-test analyses, this interaction contrast revealed a widespread set of regions, including left-lateralized medial pFC (BA 6, BA 9, and BA 11) and bilateral ventrolateral pFC (BA 44/BA 45 and BA 47). This interaction contrast also revealed regions throughout the bilateral lateral temporal lobes (BA 20, BA 21, BA 22) and right MTL (hippocampus, parahippocampal gyrus). Also evident were regions of left precuneus (BA 31), right middle occipital gyrus (BA 19), and bilateral posterior cingulate cortex (BA 23 and BA 30).

Figure 7. 

Neural activity present in the interaction contrasts inclusively masked with the Condition (decrease, increase) × Phase (instruction, onset, elaboration) interaction results. Regions in blue were more active for the decrease condition during the elaboration phase and the increase condition in the memory onset phase. Regions in purple were more active for the decrease condition during the memory onset phase and the increase condition in the elaboration phase, including a region of right hippocampus (Tal: x = 32, y = −18, z = −13) evident on the saggital slice.

Figure 7. 

Neural activity present in the interaction contrasts inclusively masked with the Condition (decrease, increase) × Phase (instruction, onset, elaboration) interaction results. Regions in blue were more active for the decrease condition during the elaboration phase and the increase condition in the memory onset phase. Regions in purple were more active for the decrease condition during the memory onset phase and the increase condition in the elaboration phase, including a region of right hippocampus (Tal: x = 32, y = −18, z = −13) evident on the saggital slice.

The second interaction contrast was the reverse of the first contrast and examined which regions were more active for the decrease condition during the elaboration phase and the increase condition in the memory onset phase (i.e., [decrease elaboration > decrease onset] > [increase elaboration > increase onset]). Consistent with the t-test analyses, this interaction contrast revealed significantly greater activity in only a region of left frontal pole (BA 10) and left caudate (see Tables 6 and 8).

Postscan Behavioral Results

We also examined the effect of regulation condition on the behavioral ratings made about AMs following the scan. A within-subject ANOVA revealed a significant effect of Instruction on postscan emotional intensity ratings, F(3, 60) = 60.95, p < .001, partial η2 = .75 (Table 9). As would be expected, post hoc pairwise comparisons confirmed that neutral AMs continued to be rated as lower in intensity than all of the negative AM regulation conditions, ps < .001. In addition, pairwise comparisons revealed that negative AMs that had been in the decrease condition during the scan continued to be rated as lower in emotional intensity than those in the increase condition, p = .003.

Table 9. 

Postscan Mean Behavioral Characteristics of Negative and Neutral AMs from the Postscan Session that Had Appeared with Decrease, Increase, or Maintain Instructions during the Scan

Trial Type
Postscan Behavioral Ratings
Intensity
Negative
Positive
Vividness
Decrease Neg 4.38 (0.73) 4.79 (0.81) 1.79 (0.88) 5.12 (0.77) 
Increase Neg 4.65 (0.76) 5.28 (0.75) 1.55 (0.75) 5.17 (0.67) 
Maintain Neg 4.53 (0.75) 5.10 (0.62) 1.54 (0.54) 5.20 (0.66) 
Maintain Neutral 2.51 (0.84) 1.34 (0.23) 3.95 (1.39) 4.88 (0.75) 
Trial Type
Postscan Behavioral Ratings
Intensity
Negative
Positive
Vividness
Decrease Neg 4.38 (0.73) 4.79 (0.81) 1.79 (0.88) 5.12 (0.77) 
Increase Neg 4.65 (0.76) 5.28 (0.75) 1.55 (0.75) 5.17 (0.67) 
Maintain Neg 4.53 (0.75) 5.10 (0.62) 1.54 (0.54) 5.20 (0.66) 
Maintain Neutral 2.51 (0.84) 1.34 (0.23) 3.95 (1.39) 4.88 (0.75) 

Standard deviations are presented in parentheses.

There was also a significant main effect of instruction on postscan negative emotion ratings, F(3, 60) = 333.31, p < .001, partial η2 = .94 (Table 9). As with intensity ratings, post hoc pairwise comparisons confirmed that neutral memories were rated as significantly less negative than negative AMs from each of the regulation conditions, ps < .001. More interestingly, participants rated the negativity of their negative AMs in line with what would be predicted based on instruction condition: Negative AMs that had been in the decrease condition during the scan were rated as less negative than negative AMs from both the increase and maintain conditions, ps < .009, and negative AMs that had been in the increase condition during the scan were rated as more negative than AMs from both the decrease and maintain conditions, ps ≤ .05.

A similar pattern was also present for positive emotion ratings, including an overall main effect of Instruction, F(3, 63) = 77.39, p < .001, partial η2 = .80 (Table 9). Pairwise comparisons confirmed that neutral memories were rated higher in positive emotion than negative AMs from any regulation condition, ps < .001. Negative AMs that had appeared in the decrease condition during the scan were rated as higher in positive emotion than those negative AMs from both the increase and maintain conditions, ps < .04, although AMs from the increase and maintain conditions did not differ from one another in positive ratings, p = .91.

Finally, there was a main effect of Instruction for the postscan vividness ratings, F(3, 60) = 4.54, p = .01, partial η2 = .19 (Table 9). Pairwise comparisons revealed that this main effect was driven by neutral memories being rated as less vivid than negative AMs from the increase and maintain conditions, ps < .02; there was also a trend for negative AMs from the decrease condition to be rated as less vivid than the neutral AMs, p = .10.

DISCUSSION

We used a novel cognitive reappraisal paradigm adapted from the emotion regulation literature for use with AMs and asked participants to decrease, increase, or maintain the emotions associated with negative events from their personal pasts while undergoing an fMRI scan. Emotional intensity ratings about the events made during the scan confirmed that participants were reappraising in the instructed direction, as AMs that had appeared with the increase instruction were rated as the most intense, followed by AMs that had appeared with the maintain instruction and then by AMs that had appeared with the decrease instruction. By scanning individuals as they prepared to reappraise or maintain their emotions, accessed events associated with personal cues, and then elaborated upon the AMs they had recalled, the present experiment revealed that a different time course of activation was associated with the down- versus the up-regulation of AMs.

Down-regulation of Negative Emotions

The down-regulation of negative emotions during AM recall recruited the greatest neural activity during the memory onset phase (i.e., the time between the presentation of a memory cue and a button press indicating that the fully formed memory was in mind). As would be expected based on previous reappraisal studies with emotional images (Ochsner & Gross, 2005, 2008), decreasing emotional responses was associated with increased activity in cognitive control regions throughout pFC when compared with maintaining emotional responses. Areas of activation were revealed in dorsolateral pFC regions associated with maintaining and manipulating information in working memory (e.g., Curtis & D'Esposito, 2003); ventrolateral pFC regions associated with AM retrieval (Cabeza & St. Jacques, 2007) and the selection of context-appropriate reappraisals (reviewed by Denny et al., 2009; see also Badre, Poldrack, Pare-Blagoev, Insler, & Wagner, 2005); and medial pFC regions associated with self-referential processing (Kelley et al., 2002), with the flexible assignment of affective value (D'Argembeau, Xue, Lu, Van der Linden, & Bechara, 2008), and with the extinction of conditioned emotional responses (particularly ventromedial pFC; Delgado, Nearing, LeDoux, & Phelps, 2008; Phelps, Delgado, Nearing, & LeDoux, 2004).

Although this pFC activity follows in line with other cognitive reappraisal tasks (reviewed by Ochsner & Gross, 2005, 2008) that have used a maintenance/view condition as a baseline, the disproportionate pFC activity during the memory onset phase for decreasing versus increasing the intensity of AMs was contrary to our hypotheses. Also contrary to expectations, there was disproportionate activation in the MTL (e.g., hippocampus, parahippocampal gyrus) and emotion processing regions, including the insula and amygdala, during down-regulation as compared with up-regulation of negative AMs.

One possible explanation for this pattern of findings for the down-regulation of negative emotions during AM recall may be gleaned from the process model of emotion regulation, which posits that the reappraisal of negative emotions may be especially sensitive to timing effects (Sheppes & Gross, 2011). The model presumes that emotions unfold over time and that down-regulating negative emotions is most effective at early time points before intensity increases. For instance, being instructed to down-regulate emotions about a sad film early during the film is an effective way to reduce negative affect, but reappraisal instructions given later during the film are ineffective, presumably as emotional intensity has passed a “point of no return” (Sheppes & Meiran, 2007).

The timing hypothesis put forth by the process model (Sheppes & Gross, 2011) may apply to down-regulation of AM intensity; just as decreasing negative emotion is most effective at early time points during a film clip, it may also be most effective at early time points during AM recall (i.e., as a memory is initially being accessed) and thus down-regulation of AM may be associated with earlier retrieval-related activity than up-regulation. Indeed, in striking contrast to the memory onset phase, the memory elaboration phase revealed the greatest neural activity for the maintain and increase trials, consistent with the hypothesis that much of the work in down-regulating negative emotions occurred early on in AM recall. This finding dovetails nicely with previous work suggesting that reappraisal (when compared with rumination) did not lead to greater neural activity (Kross et al., 2009) or connectivity (Fabiansson et al., 2012). These studies presented regulation instructions only after AMs were being held in mind (and presumably after emotional appraisal had already occurred), which would correspond with our memory elaboration phase, perhaps explaining why they found few regions associated with reappraisal.

Up-regulation of Negative Emotions

Whereas decreasing emotions was primarily associated with increased neural activity during the AM onset phase, increasing emotions instead was related to increased activity in both the instruction and elaboration phases. Although both down- and up-regulation engaged cognitive control regions in pFC during the instruction phase, up-regulation led to the most extensive pFC engagement in comparison with the maintain instruction phase. Directly comparing the increase and decrease conditions revealed widespread activity in regions previously implicated in the up-regulation of negative images (Ochsner et al., 2004), including in cognitive control regions in pFC and anterior cingulate, visuospatial regions (e.g., cuneus, precuneus), as well as in the insula. This pattern of activity is consistent with prior research demonstrating that pFC, ACC, insula, and amygdala activity is elevated when participants are expecting the presentation of unpleasant stimuli (e.g., Herwig et al., 2007). In addition, this anticipatory activity is in line with behavioral reports from a postscan debriefing questionnaire. Whereas participants reported trying to “relax” and “let go of negative emotions” when viewing the decrease instructions, they reported “tensing up” and preparing to “engage with,” “relive,” and “recall specific details about” the subsequent negative event when viewing the increase instructions.

Despite this anticipatory activity during the instruction phase, there was a relative paucity of activity during the memory onset phase when the increase condition was compared with either the decrease or maintain conditions. As mentioned in the earlier discussion of down-regulation, part of this difference may relate to when, in the time course of memory retrieval, reappraisal-related activity is most effective in altering the intensity of an emotional response: Activity during the onset phase may be more effective for down-regulation than for up-regulation. But another possibility is that the anticipatory activity in emotion and visuospatial regions during the instruction phase enabled participants to more efficiently access the emotional and sensory details about negative events, leading to relatively less neural activity compared with negative AMs that had not been preceded by such anticipatory activity. In other words, adapting a particular mindset to increase negative emotions before recall even occurs may facilitate retrieval of negative AMs.

Neural activity for the up-regulation condition during the time when individuals were elaborating upon their AMs was consistent with our predictions based on prior cognitive reappraisal (Ochsner & Gross, 2005, 2008) and emotional AM (e.g., Botzung et al., 2010) experiments. In particular, regions of medial pFC, MTL (including hippocampus, parahippocampal gyrus, and amygdala), posterior visuospatial regions, and emotion processing regions (including insula) were all more engaged by the increase than decrease or maintain conditions during memory elaboration. These results are in accordance with prior research on the up-regulation of emotions during the presentation of negative images (Ochsner et al., 2004) and on the recall of emotionally intense AMs (Botzung et al., 2010). In addition, the increased activity in visuospatial regions corresponds with the higher vividness ratings for the increase condition; such a relation between vividness ratings and posterior activity was previously found to be specific to the AM elaboration phase (Daselaar et al., 2008).

Interestingly, the increased activity in visuospatial regions and higher vividness ratings may fit with prior findings of increased activity in these regions during the up-regulation of negative images (e.g., Ochsner et al., 2004). One proposed strategy for increasing emotional intensity in response to an emotional image is to imagine oneself as a central figure in the scene and to enhance the subjective feeling of experiencing the sights and sounds associated with that scene (Ochsner et al., 2004); a similar strategy of increasing or decreasing recall of specific sensory details may be a useful regulatory strategy during autobiographical recall. During AM recall, the elaboration phase has specifically been associated with the recall and elaboration of vivid sensory details (Daselaar et al., 2008). A reasonable hypothesis, then, might be that recalling and expounding upon vivid sensory details during the elaboration phase is a useful strategy for successfully up-regulating emotional intensity.

Future Directions

An important next step in the research on emotion regulation and AM is testing how these two processes are linked on a behavioral and neural level in clinical populations, such as individuals with depression. Emotion dysregulation and pervasive maintenance of negative affect are considered defining features of depression, possibly because poor executive functioning leads to deficits in the ability to use cognitively demanding strategies like reappraisal (Gotlib & Joormann, 2010). In line with this hypothesis, participants with major depressive disorder exhibit both increased bilateral pFC (Johnstone, van Reekum, Urry, Kalin, & Davidson, 2007) and increased amygdala and insula activity (Beauregard, Paquette, & Levesque, 2006) during cognitive reappraisal tasks using negative images, perhaps reflecting ineffective compensatory attempts at emotion regulation (see Denny et al., 2009, for similar discussion). Examining neural activity as depressed individuals attempt to down-regulate negative AMs might shed further light on their regulatory deficits: For example, depressed individuals may engage pFC and insula/amygdala while accessing negative AMs (as our healthy participants did) but continue to sustain these activations when elaborating upon the details of their memories. The pervasive sad mood associated with depression might also lead to anticipatory neural responses similar to what we found during the increase instruction phase. In turn, depressed individuals may have greater success in accessing negative and vivid emotional details about events, leading to the perpetuation of their sad mood and depression.

In addition to depression, these questions are also directly relevant to individuals with post-traumatic stress disorder (PTSD). A recent fMRI experiment revealed that individuals with PTSD (vs. controls) engaged the amygdala/hippocampus to a greater extent during a negative AM search phase and the ventromedial pFC to a greater extent during both the search and elaboration phases (St. Jacques, Botzung, Miles, & Rubin, 2011). The authors suggest that this increased recruitment of amygdala and ventromedial pFC and a greater functional coupling between these regions might reflect an up-regulation of negative emotional intensity during recall (St. Jacques et al., 2011). Because PTSD can be characterized by either an undermodulation (i.e., in the case of hyperarousal) or overmodulation (i.e., in the case of a dissociative subtype of PTSD) of emotional intensity (Lanius et al., 2010), an interesting next step would be to differentiate between individuals with these two subtypes of PTSD as they complete an instructed reappraisal task. We might expect individuals with the hyperarousal subtype of PTSD to over-recruit emotional appraisal regions like the amygdala, insula, and medial pFC, whereas individuals with the dissociative subtype might underrecruit these same regions while over-recruiting cognitive control regions like lateral pFC and dACC.

The postscan behavioral ratings suggest a possible long-term influence of regulation instructions on memory characteristics. During the postscan session, participants were given the titles of each event they recalled in the scanner but were not given any reminder of which reappraisal instruction had appeared with which AM. Events that had previously appeared with the decrease instruction continued to be rated as significantly lower in intensity than events that had appeared with the increase instruction, suggesting that there may have been an effect of reappraisal on AM recall that lasted at least across the 0.5-hr delay between the scan and postscan ratings. An important question for future research to examine is how long-lasting reappraisal effects are; this question is of interest from a basic science perspective with regard to the malleability of memory and may have relevance to clinical populations undergoing cognitive behavioral therapy aimed at reducing the emotional intensity associated with cognitions (e.g., Gotlib & Joormann, 2010).

There are also a number of open questions regarding the types of emotional events that individuals are asked to reappraise. For example, it remains to be seen whether the valence of the event being reappraised would lead to differences in which neural regions are engaged during recall. One possibility is that down- and up-regulation modulate neural activity in similar regions over the same time course regardless of the valence of the information that is being regulated. However, recalling positive events has sometimes been associated with greater engagement of medial OFC and MTL compared with negative events (Markowitsch, Vandekerckhove, Lanfermann, & Russ, 2003; Piefke, Weiss, Zilles, Markowitsch, & Fink, 2003; but see St. Jacques et al., 2011), leaving open the possibility that the reappraisal of positive events may modulate activity in these regions to a greater extent than the reappraisal of negative events.

Conclusion

In summary, the present experiment modified a cognitive reappraisal task for use with AMs and asked individuals to decrease, increase, or maintain the emotions associated with negative events while undergoing an fMRI scan. Our results revealed that down- and up-regulation were differentiated by the time course over which they recruited neural activity: Down-regulation primarily engaged greater activity during the memory onset phase, whereas up-regulation engaged greater activity during the instruction and memory elaboration phases. More broadly, this study suggests that invoking goals before the retrieval of AMs can influence the behavioral (e.g., emotional intensity and vividness ratings) and neural correlates associated with recall, in line with Conway's (2005) proposal of the goal-directed constructive nature of AM. Indeed, the ability to flexibly reappraise emotional details may be a critical function of memory and have important implications for the development and treatment of clinical disorders.

Acknowledgments

This research was supported by NIH grant MH080833 to E. A. K. and a National Defense Science and Engineering Graduate Fellowship to A. C. H. We thank Tammy Moran and Ross Mair at the Harvard Center for Brain Science for their assistance with MR data collection and Daniel Schacter, Scott Slotnick, Ehri Ryu, and Donna Rose Addis for helpful discussion. Portions of this research were included in a PhD dissertation by A. C. H.

Reprint requests should be sent to Alisha C. Holland, Department of Psychology, New York University, New York, NY 10003, or via e-mail: alisha.holland@nyu.edu.

REFERENCES

Addis
,
D. R.
,
Moscovitch
,
M.
,
Crawley
,
A. P.
, &
McAndrews
,
M. P.
(
2004
).
Recollective qualities modulate hippocampal activation during autobiographical memory retrieval.
Hippocampus
,
14
,
752
762
.
Addis
,
D. R.
,
Pan
,
L.
,
Vu
,
M. A.
,
Laiser
,
N.
, &
Schacter
,
D. L.
(
2009
).
Constructive episodic simulation of the future and the past: Distinct subsystems of a core brain network mediate imagining and remembering.
Neuropsychologia
,
47
,
2222
2238
.
Addis
,
D. R.
,
Wong
,
A. T.
, &
Schacter
,
D. L.
(
2007
).
Remembering the past and imagining the future: Common and distinct neural substrates during event construction and elaboration.
Neuropsychologia
,
45
,
1363
1377
.
Badre
,
D.
,
Poldrack
,
R. A.
,
Pare-Blagoev
,
E. J.
,
Insler
,
R. Z.
, &
Wagner
,
A. D.
(
2005
).
Dissociable controlled retrieval and generalized selection mechanisms in ventrolateral prefrontal cortex.
Neuron
,
47
,
907
918
.
Beauregard
,
M.
,
Paquette
,
V.
, &
Levesque
,
J.
(
2006
).
Dysfunction in the neural circuitry of emotional self-regulation in major depressive disorder.
NeuroReport
,
17
,
843
846
.
Bluck
,
S.
,
Alea
,
N.
,
Habermas
,
T.
, &
Rubin
,
D. C.
(
2005
).
A tale of three functions: The self-reported uses of autobiographical memory.
Social Cognition
,
23
,
91
117
.
Botzung
,
A.
,
Rubin
,
D. C.
,
Miles
,
A.
,
Cabeza
,
R.
, &
LaBar
,
K. S.
(
2010
).
Mental hoop diaries: Emotional memories of a college basketball game in rival fans.
The Journal of Neuroscience
,
30
,
2130
2137
.
Cabeza
,
R.
, &
St. Jacques
,
P.
(
2007
).
Functional neuroimaging of autobiographical memory.
Trends in Cognitive Sciences
,
11
,
219
227
.
Clark
,
J. M.
, &
Paivio
,
A.
(
2004
).
Extensions of the Paivio, Yuille, and Madigan (1968) norms.
Behavior Research Methods, Instruments, & Computers
,
36
,
371
383
.
Conway
,
M. A.
(
2005
).
Memory and the self.
Journal of Memory and Language
,
53
,
594
628
.
Cooney
,
R. E.
,
Joormann
,
J.
,
Atlas
,
J. Y.
,
Eugène
,
F.
, &
Gotlib
,
I. H.
(
2007
).
Remembering the good times: Neural correlates of affect regulation.
NeuroReport
,
18
,
1771
1774
.
Curtis
,
C. E.
, &
D'Esposito
,
M.
(
2003
).
Persistent activity in the prefrontal cortex during working memory.
Trends in Cognitive Sciences
,
7
,
415
423
.
D'Argembeau
,
A.
,
Xue
,
G.
,
Lu
,
Z.
,
Van der Linden
,
M.
, &
Bechara
,
A.
(
2008
).
Neural correlates of envisioning emotional events in the near and far future.
Neuroimage
,
40
,
398
407
.
Daselaar
,
S. M.
,
Rice
,
H. J.
,
Greenberg
,
D. L.
,
Cabeza
,
R.
,
LaBar
,
K. S.
, &
Rubin
,
D. C.
(
2008
).
The spatio-temporal dynamics of autobiographical memory: Neural correlates of recall, emotional intensity, and reliving.
Cerebral Cortex
,
18
,
217
229
.
Delgado
,
M. R.
,
Nearing
,
K. I.
,
LeDoux
,
J. E.
, &
Phelps
,
E. A.
(
2008
).
Neural circuitry underlying the regulation of conditioned fear and its relation to extinction.
Neuron
,
59
,
829
838
.
Denny
,
B.
,
Silvers
,
J.
, &
Ochsner
,
K. N.
(
2009
).
How we heal what we don't want to feel: The functional neural architecture of emotion regulation.
In A. M. Kring & D. M. Sloan (Eds.)
,
Emotion regulation and psychopathology: A transdiagnostic approach to etiology and treatment
(pp.
59
87
).
New York
:
Guilford Press
.
Fabiansson
,
E. C.
,
Denson
,
T. F.
,
Moulds
,
M. L.
,
Grisham
,
J. R.
, &
Schira
,
M. M.
(
2012
).
Don't look back in anger: Neural correlates of reappraisal, analytical rumination, and angry rumination during recall of an anger-inducing autobiographical memory.
Neuroimage
,
59
,
2974
2981
.
Goldin
,
P. R.
,
McRae
,
K.
,
Ramel
,
W.
, &
Gross
,
J. J.
(
2008
).
The neural bases of emotion regulation: Reappraisal and suppression of negative emotion.
Biological Psychiatry
,
63
,
577
586
.
Gotlib
,
I. H.
, &
Joormann
,
J.
(
2010
).
Cognition and depression: Current status and future directions.
Annual Review in Clinical Psychology
,
6
,
285
312
.
Greenberg
,
D. L.
,
Rice
,
H. J.
,
Cooper
,
J. J.
,
Cabeza
,
R.
,
Rubin
,
D. C.
, &
LaBar
,
K. S.
(
2005
).
Coactivation of the amygdala, hippocampus, and inferior frontal gyrus during autobiographical memory retrieval.
Neuropsychologia
,
43
,
659
674
.
Gross
,
J. J.
, &
Thompson
,
R. A.
(
2007
).
Emotion regulation: Conceptual foundations.
In J. J. Gross (Ed.)
,
Handbook of emotion regulation
(pp.
3
24
).
New York
:
Guilford Press
.
Herwig
,
U.
,
Baumgartner
,
T.
,
Kaffenberger
,
T.
,
Bruhl
,
A.
,
Kottlow
,
M.
,
Schreiter-Gasser
,
U.
,
et al
(
2007
).
Modulation of anticipatory emotion and perception processing by cognitive control.
Neuroimage
,
37
,
652
662
.
Holland
,
A. C.
,
Tamir
,
M.
, &
Kensinger
,
E. A.
(
2010
).
The effect of regulation goals on emotional event specific knowledge.
Memory
,
18
,
504
521
.
Johnstone
,
T.
,
van Reekum
,
C. M.
,
Urry
,
H. L.
,
Kalin
,
N. H.
, &
Davidson
,
R. J.
(
2007
).
Failure to regulate: Counterproductive recruitment of top–down prefrontal-subcortical circuitry in major depression.
The Journal of Neuroscience
,
27
,
8877
8884
.
Joormann
,
J.
,
Cooney
,
R. E.
,
Henry
,
M. L.
, &
Gotlib
,
I. H.
(
2012
).
Neural correlates of automatic mood regulation in girls at high risk for depression.
Journal of Abnormal Psychology
,
121
,
61
72
.
Josephson
,
B. R.
,
Singer
,
J. A.
, &
Salovey
,
P.
(
1996
).
Mood regulation and memory: Repairing sad moods with happy memories.
Cognition and Emotion
,
10
,
437
444
.
Kelley
,
W. M.
,
Macrae
,
C. N.
,
Wyland
,
C. L.
,
Caglar
,
S.
,
Inati
,
S.
, &
Heatherton
,
T. F.
(
2002
).
Finding the self? An event-related fMRI study.
Journal of Cognitive Neuroscience
,
14
,
785
794
.
Kross
,
E.
,
Davidson
,
M.
,
Weber
,
J.
, &
Ochsner
,
K.
(
2009
).
Coping with emotions past: The neural bases of regulating affect associated with negative autobiographical memories.
Biological Psychiatry
,
65
,
361
366
.
Lanius
,
R. A.
,
Vermetten
,
E.
,
Loewenstein
,
R. J.
,
Brand
,
B.
,
Schmahl
,
C.
,
Bremner
,
J. D.
,
et al
(
2010
).
Emotion modulation in PTSD: Clinical and neurobiological evidence for a dissociative subtype.
The American Journal of Psychiatry
,
167
,
640
647
.
Markowitsch
,
H. J.
,
Thiel
,
A.
,
Reinkemeier
,
M.
,
Kessler
,
J.
,
Koyuncu
,
A.
, &
Heiss
,
W. D.
(
2000
).
Right amygdalar and temporofrontal activation during autobiographic, but not during fictitious memory retrieval.
Behavioral Neurology
,
12
,
181
190
.
Markowitsch
,
H. J.
,
Vandekerckhove
,
M. M.
,
Lanfermann
,
H.
, &
Russ
,
M. O.
(
2003
).
Engagement of lateral and medial prefrontal areas in the ecphory of sad and happy autobiographical memories.
Cortex
,
39
,
643
665
.
Ochsner
,
K. N.
,
Bunge
,
S. A.
,
Gross
,
J. J.
, &
Gabrieli
,
J. D.
(
2002
).
Rethinking feelings: An fMRI study of the cognitive regulation of emotion.
Journal of Cognitive Neuroscience
,
14
,
1215
1229
.
Ochsner
,
K. N.
, &
Gross
,
J. J.
(
2005
).
The cognitive control of emotion.
Trends in Cognitive Sciences
,
9
,
242
249
.
Ochsner
,
K.
, &
Gross
,
J. J.
(
2008
).
Cognitive emotion regulation: Insights from social cognitive and affective neuroscience.
Current Directions in Psychological Science
,
17
,
153
158
.
Ochsner
,
K. N.
,
Ray
,
R. D.
,
Cooper
,
J. C.
,
Robertson
,
E. R.
,
Chopra
,
S.
,
Gabrieli
,
J. D. E.
,
et al
(
2004
).
For better or for worse: Neural systems supporting the cognitive down- and up-regulation of negative emotion.
Neuroimage
,
23
,
483
499
.
Phan
,
K. L.
,
Fitzgerald
,
D. A.
,
Nathan
,
P. J.
,
Moore
,
G. J.
,
Uhde
,
T. W.
, &
Tancer
,
M. E.
(
2005
).
Neural substrates for voluntary suppression of negative affect: A functional magnetic resonance imaging study.
Biological Psychiatry
,
57
,
210
219
.
Phelps
,
E. A.
,
Delgado
,
M. R.
,
Nearing
,
K. I.
, &
LeDoux
,
J. E.
(
2004
).
Extinction learning in humans: Role of the amygdala and vmPFC.
Neuron
,
43
,
897
905
.
Piefke
,
M.
,
Weiss
,
P. H.
,
Zilles
,
K.
,
Markowitsch
,
H. J.
, &
Fink
,
G. R.
(
2003
).
Differential remoteness and emotional tone modulate the neural correlates of autobiographical memory.
Brain
,
126
,
650
668
.
Sheppes
,
G.
, &
Gross
,
J. J.
(
2011
).
Is timing everything? Temporal considerations in emotion regulation.
Personality and Social Psychology Review
,
15
,
319
331
.
Sheppes
,
G.
, &
Meiran
,
N.
(
2007
).
Better late than never? On the dynamics of online regulation of sadness using distraction and cognitive reappraisal.
Personality and Social Psychology Bulletin
,
33
,
1518
1532
.
St. Jacques
,
P. L.
,
Botzung
,
A.
,
Miles
,
A.
, &
Rubin
,
D. C.
(
2011
).
Functional neuroimaging of emotionally intense autobiographical memories in post-traumatic stress disorder.
Journal of Psychiatric Research
,
45
,
630
637
.
Steinvorth
,
S.
,
Corkin
,
S.
, &
Halgren
,
E.
(
2006
).
Ecphory of autobiographical memories: An fMRI study of recent and remote memory retrieval.
Neuroimage
,
30
,
285
298
.
Svoboda
,
E.
,
McKinnon
,
M. C.
, &
Levine
,
B.
(
2006
).
The functional neuroanatomy of autobiographical memory: A meta-analysis.
Neuropsychologia
,
44
,
2189
2208
.
Tamir
,
M.
,
Mitchell
,
C.
, &
Gross
,
J. J.
(
2008
).
Hedonic and instrumental motives in anger regulation.
Psychological Science
,
19
,
324
328
.
Urry
,
H. L.
,
van Reekum
,
C. M.
,
Johnstone
,
T.
,
Kalin
,
N. H.
,
Thurow
,
M. E.
,
Schaefer
,
H. S.
,
et al
(
2006
).
Amygdala and ventromedial prefrontal cortex are inversely coupled during regulation of negative affect and predict the diurnal pattern of cortisol secretion among older adults.
The Journal of Neuroscience
,
26
,
4415
4425
.
Walter
,
B.
,
Blecker
,
C.
,
Kirsch
,
P.
,
Sammer
,
G.
,
Schienle
,
A.
,
Stark
,
R.
,
et al
(
2003
).
MARINA: An easy to use tool for the creation of MAsks for Region of INterest Analyses [abstract]
.
Presented at the 9th International Conference on Functional Mapping of the Human Brain, June 19–22, 2003, New York, NY
.
Westermann
,
R.
,
Kordelia
,
S.
,
Stahl
,
G.
, &
Hesse
,
F. W.
(
1996
).
Relative effectiveness and validity of mood induction procedures: A meta-analysis.
European Journal of Social Psychology
,
26
,
557
580
.