Coping with emotions past: the neural bases of regulating affect associated with negative autobiographical memories.
Biological Psychiatry (2009)
- PubMed: 19058792
Available from www.pubmedcentral.nih.gov
or
Abstract
Although the ability to adaptively reflect on negative autobiographical experiences without ruminating is critical to mental health, to our knowledge no research has directly examined the neural systems underlying this process.
Author-supplied keywords
Available from www.pubmedcentral.nih.gov
Page 1
Coping with emotions past: the neural bases of regulating affect associated with negative autobiographical memories.
PRIORITY COMMUNICATION
Coping with Emotions Past: The Neural Bases of
Regulating Affect Associated with Negative
Autobiographical Memories
Ethan Kross, Matthew Davidson, Jochen Weber, and Kevin Ochsner
Background: Although the ability to adaptively reflect on negative autobiographical experiences without ruminating is critical to mental
health, to our knowledge no research has directly examined the neural systems underlying this process.
Methods: Sixteen participants were scanned using functional magnetic resonance imaging (fMRI) as they focused on negative autobio-
graphical memories using cognitive strategies designed to facilitate (feel strategy) versus undermine (analyze and accept strategies)
rumination.
Results: Two key findings were obtained. First, consistent with prior emotion regulation research using image-based stimuli, left prefrontal
activity was observed during the implementation of all three strategies. Second, activity in a network of regions involved in self-referential
processing and emotion, including subgenual anterior cingulate cortex and medial prefrontal cortex, was highest in response to the feel
strategy and lowest for the accept strategy. This pattern of activation mirrored participants’ self-reports of negative affect when engaging in
each strategy.
Conclusions: These findings shed light on the brain regions that distinguish adaptive versus maladaptive forms of reflecting on negative
autobiographical memories and offer a novel, ecologically valid route to exploring the neural bases of emotion regulation using fMRI.
Key Words: Autobiographical memory, emotion regulation, fMRI,
reappraisal, rumination, subgenual anterior cingulate cortex
T
he ability to adaptively cope with distressing life experi-
ences is a key self-regulatory challenge. Failing to meet
this challenge can be costly, as intrusive and emotionally
charged thoughts about these experiences contribute to a variety
of clinical disorders (1). Although an explosion of research has
examined the neural bases of consciously regulating negative
emotions triggered in response to normatively aversive visual or
cutaneous shock stimuli (2–19), no research has examined how
these findings generalize to coping with such highly idiosyncratic
negative emotional memories. This is important because some
regions known to be critical to mood disorders have not been
consistently identified in prior neuroimaging research on the use
of cognitive strategies to regulate emotion. Consider, for exam-
ple, research on depression, a mood disorder characterized by
high levels of self-focused rumination (20,21). Although findings
clearly indicate that subgenual anterior cingulate cortex (sgACC)
activity tracks closely with depressive symptoms (22–30), re-
search on emotion regulation strategies thought to be relevant to
cognitive therapies for depression (e.g., reappraisal) rarely report
changes in activity in this region. This discrepancy suggests that
some of the brain regions involved in regulating feelings associ-
ated with emotional memories may be different than those
involved in regulating responses to normatively negative stimuli.
Here, we examined this issue by developing a novel func-
tional magnetic resonance imaging (fMRI) paradigm in which
participants recalled a series of highly arousing negative auto-
biographical memories and then focused on them using strate-
gies designed to facilitate versus undermine adaptive self-reflec-
tion. The first “feel” strategy directed individuals to focus on the
specific feelings that naturally flowed through their mind as they
thought about their recalled experiences. This strategy was used
because prior research indicates that focusing concretely on
negative feelings triggers the kind of negative affect infused,
ruminative episodes that are the hallmark of dysfunctional
coping (31–33). The second “accept” strategy directed individu-
als to recognize that the feelings they experienced during
recollection were passing mental events that were psychologi-
cally distant from the self and did not control them. The
instructions for this strategy were adapted from a form of
cognitive behavioral therapy that teaches people how to mind-
fully focus on negative feeling states in ways that are believed to
buffer against rumination (34–36). The third “analyze” strategy
directed participants to objectively analyze the causes and rea-
sons underlying their feelings and was designed as a memory
analog of cognitive reappraisal strategies used in prior fMRI
studies (12,13,18,19).
Methods and Materials
Twenty-four Columbia University affiliates (15 female sub-
jects; M age ! 20.83, SD ! 3.27) provided informed consent.
Prospective participants were screened to ensure they were not
currently undergoing treatment from a mental health profes-
sional, taking mental health-related medication (e.g., Prozac),
were claustrophobic, or had metal in their bodies. The sample
consisted of 60% European Americans, 24% Asians, 4% African
Americans, and 12% other.
Stimuli
Similar to prior studies that have used script-driven methods,
cue phrases were used to trigger the recall of negative autobio-
graphical memories in the scanner. To obtain memory cues,
participants were asked to describe in writing nine highly
arousing negative autobiographical experiences during a screen-
ing session and then judge the extent to which thinking about
From the Department of Psychology (EK), University of Michigan, Ann Arbor,
Michigan; and Psychology Department (MD, JW, KO), Columbia Univer-
sity, New York, New York.
Address reprint requests to Ethan Kross, Ph.D., University of Michigan, De-
partment of Psychology, 530 Church Street, Ann Arbor, MI 48109-1043;
E-mail: ekross@umich.edu.
Received July 10, 2008; revised October 6, 2008; accepted October 13, 2008.
BIOL PSYCHIATRY 2009;65:361–3660006-3223/09/$36.00
doi:10.1016/j.biopsych.2008.10.019 © 2009 Society of Biological Psychiatry
Coping with Emotions Past: The Neural Bases of
Regulating Affect Associated with Negative
Autobiographical Memories
Ethan Kross, Matthew Davidson, Jochen Weber, and Kevin Ochsner
Background: Although the ability to adaptively reflect on negative autobiographical experiences without ruminating is critical to mental
health, to our knowledge no research has directly examined the neural systems underlying this process.
Methods: Sixteen participants were scanned using functional magnetic resonance imaging (fMRI) as they focused on negative autobio-
graphical memories using cognitive strategies designed to facilitate (feel strategy) versus undermine (analyze and accept strategies)
rumination.
Results: Two key findings were obtained. First, consistent with prior emotion regulation research using image-based stimuli, left prefrontal
activity was observed during the implementation of all three strategies. Second, activity in a network of regions involved in self-referential
processing and emotion, including subgenual anterior cingulate cortex and medial prefrontal cortex, was highest in response to the feel
strategy and lowest for the accept strategy. This pattern of activation mirrored participants’ self-reports of negative affect when engaging in
each strategy.
Conclusions: These findings shed light on the brain regions that distinguish adaptive versus maladaptive forms of reflecting on negative
autobiographical memories and offer a novel, ecologically valid route to exploring the neural bases of emotion regulation using fMRI.
Key Words: Autobiographical memory, emotion regulation, fMRI,
reappraisal, rumination, subgenual anterior cingulate cortex
T
he ability to adaptively cope with distressing life experi-
ences is a key self-regulatory challenge. Failing to meet
this challenge can be costly, as intrusive and emotionally
charged thoughts about these experiences contribute to a variety
of clinical disorders (1). Although an explosion of research has
examined the neural bases of consciously regulating negative
emotions triggered in response to normatively aversive visual or
cutaneous shock stimuli (2–19), no research has examined how
these findings generalize to coping with such highly idiosyncratic
negative emotional memories. This is important because some
regions known to be critical to mood disorders have not been
consistently identified in prior neuroimaging research on the use
of cognitive strategies to regulate emotion. Consider, for exam-
ple, research on depression, a mood disorder characterized by
high levels of self-focused rumination (20,21). Although findings
clearly indicate that subgenual anterior cingulate cortex (sgACC)
activity tracks closely with depressive symptoms (22–30), re-
search on emotion regulation strategies thought to be relevant to
cognitive therapies for depression (e.g., reappraisal) rarely report
changes in activity in this region. This discrepancy suggests that
some of the brain regions involved in regulating feelings associ-
ated with emotional memories may be different than those
involved in regulating responses to normatively negative stimuli.
Here, we examined this issue by developing a novel func-
tional magnetic resonance imaging (fMRI) paradigm in which
participants recalled a series of highly arousing negative auto-
biographical memories and then focused on them using strate-
gies designed to facilitate versus undermine adaptive self-reflec-
tion. The first “feel” strategy directed individuals to focus on the
specific feelings that naturally flowed through their mind as they
thought about their recalled experiences. This strategy was used
because prior research indicates that focusing concretely on
negative feelings triggers the kind of negative affect infused,
ruminative episodes that are the hallmark of dysfunctional
coping (31–33). The second “accept” strategy directed individu-
als to recognize that the feelings they experienced during
recollection were passing mental events that were psychologi-
cally distant from the self and did not control them. The
instructions for this strategy were adapted from a form of
cognitive behavioral therapy that teaches people how to mind-
fully focus on negative feeling states in ways that are believed to
buffer against rumination (34–36). The third “analyze” strategy
directed participants to objectively analyze the causes and rea-
sons underlying their feelings and was designed as a memory
analog of cognitive reappraisal strategies used in prior fMRI
studies (12,13,18,19).
Methods and Materials
Twenty-four Columbia University affiliates (15 female sub-
jects; M age ! 20.83, SD ! 3.27) provided informed consent.
Prospective participants were screened to ensure they were not
currently undergoing treatment from a mental health profes-
sional, taking mental health-related medication (e.g., Prozac),
were claustrophobic, or had metal in their bodies. The sample
consisted of 60% European Americans, 24% Asians, 4% African
Americans, and 12% other.
Stimuli
Similar to prior studies that have used script-driven methods,
cue phrases were used to trigger the recall of negative autobio-
graphical memories in the scanner. To obtain memory cues,
participants were asked to describe in writing nine highly
arousing negative autobiographical experiences during a screen-
ing session and then judge the extent to which thinking about
From the Department of Psychology (EK), University of Michigan, Ann Arbor,
Michigan; and Psychology Department (MD, JW, KO), Columbia Univer-
sity, New York, New York.
Address reprint requests to Ethan Kross, Ph.D., University of Michigan, De-
partment of Psychology, 530 Church Street, Ann Arbor, MI 48109-1043;
E-mail: ekross@umich.edu.
Received July 10, 2008; revised October 6, 2008; accepted October 13, 2008.
BIOL PSYCHIATRY 2009;65:361–3660006-3223/09/$36.00
doi:10.1016/j.biopsych.2008.10.019 © 2009 Society of Biological Psychiatry
Page 2
each memory made them feel aroused (M ! 6.85; SD ! .65) and
negative (M ! 6.94; SD ! .55) using a 7-point scale in which
higher numbers corresponded to higher levels of arousal and
negativity. Paired sample t tests comparing valence and arousal
ratings for all memories revealed no significant differences
(arousal: ts " 1.87, ps # .08; valence: ts " 1.07, ps # .30).
Training
Upon arrival at the fMRI scanner, participants were reminded
of the negative autobiographical memories they generated dur-
ing the screening session and taught how to quickly recall each
memory in response to specific cue words using a computerized
protocol. In the first part of the protocol, a cue phrase appeared
on screen along with a description of the memory to which it
corresponded. Participants were given as much time as they
needed to pair the cue and memory so that they would be able
to quickly recall each memory when presented with the cue
alone. This process repeated until participants saw a cue-
memory description paring for all nine memories. During the
second phase of the protocol, each cue was randomly presented
on screen and participants were instructed to press the space bar
as soon as they were able to recall the specific negative autobio-
graphical experience it corresponded to. Reaction time data were
examined to ensure that participants recalled each memory in
less than 10 seconds (i.e., the amount of time participants had to
recall their experiences during the experiment). Subsequently,
participants received instructions regarding how to implement
each strategy during scanning (see introduction for summary of
specific strategy instructions).
fMRI Task
Participants viewed three repetitions each of three types of
stimulus blocks (feel, accept, or analyze) whose order was
counterbalanced. Each block was comprised of three 80-second
trials. All trials began with a 10-second cue phrase indicating that
participants should recall the autobiographical memory indicated
by the cue. Subsequently, a strategy cue word appeared on
screen directing them to engage in the feel, accept, or analyze
strategy for 30 seconds. Next, participants indicated how aroused
and negative they felt using a 5-point scale (1 ! not at all
aroused/negative; 5 ! very aroused/negative). Each question
appeared on screen for 5 seconds. Finally, participants engaged
in a 30-second spatial perception task in which they saw an
arrow pointing left or right and were asked to indicate which
direction the arrow was pointing. This task was used as a
baseline condition because pilot testing indicated that when
participants were asked to recollect memories naturally, they
tended to spontaneously engage in the strategies. Therefore, we
sought an active baseline task that would not engage the
regulatory, memory, and emotional processes of interest, and
prior work suggests that this arrows task does not engage these
Figure 1. Regions of lPFC active for each strategy relative to baseline. Bar graphs illustrate parameter estimates of signal intensity for each strategy versus
baseline. Error bars represent SEM. AC, accept; AN, analyze; FE, feel; lPFC, left prefrontal cortex.
Table 1. Conjunction Analysis Identifying Regions Commonly Active in
the Feel, Analyze, and Accept Strategy Conditions Relative to an Active
Baseline Task
Region of Activation
Brodmann’s
Area t
TAL Coordinates
Voxelsx y z
Inferior Frontal Gyrus 46 4.46 $51 29 16 218
Cuneus 19 4.46 $12 $88 31 94
Cerebellum 4.11 24 $70 $38 29
Middle Occipital Gyrus 18 3.69 15 $91 10 17
Lingual Gyrus 18 3.89 $6 $73 $2 16
TAL, Talairach.
362 BIOL PSYCHIATRY 2009;65:361–366 E. Kross et al.
www.sobp.org/journal
negative (M ! 6.94; SD ! .55) using a 7-point scale in which
higher numbers corresponded to higher levels of arousal and
negativity. Paired sample t tests comparing valence and arousal
ratings for all memories revealed no significant differences
(arousal: ts " 1.87, ps # .08; valence: ts " 1.07, ps # .30).
Training
Upon arrival at the fMRI scanner, participants were reminded
of the negative autobiographical memories they generated dur-
ing the screening session and taught how to quickly recall each
memory in response to specific cue words using a computerized
protocol. In the first part of the protocol, a cue phrase appeared
on screen along with a description of the memory to which it
corresponded. Participants were given as much time as they
needed to pair the cue and memory so that they would be able
to quickly recall each memory when presented with the cue
alone. This process repeated until participants saw a cue-
memory description paring for all nine memories. During the
second phase of the protocol, each cue was randomly presented
on screen and participants were instructed to press the space bar
as soon as they were able to recall the specific negative autobio-
graphical experience it corresponded to. Reaction time data were
examined to ensure that participants recalled each memory in
less than 10 seconds (i.e., the amount of time participants had to
recall their experiences during the experiment). Subsequently,
participants received instructions regarding how to implement
each strategy during scanning (see introduction for summary of
specific strategy instructions).
fMRI Task
Participants viewed three repetitions each of three types of
stimulus blocks (feel, accept, or analyze) whose order was
counterbalanced. Each block was comprised of three 80-second
trials. All trials began with a 10-second cue phrase indicating that
participants should recall the autobiographical memory indicated
by the cue. Subsequently, a strategy cue word appeared on
screen directing them to engage in the feel, accept, or analyze
strategy for 30 seconds. Next, participants indicated how aroused
and negative they felt using a 5-point scale (1 ! not at all
aroused/negative; 5 ! very aroused/negative). Each question
appeared on screen for 5 seconds. Finally, participants engaged
in a 30-second spatial perception task in which they saw an
arrow pointing left or right and were asked to indicate which
direction the arrow was pointing. This task was used as a
baseline condition because pilot testing indicated that when
participants were asked to recollect memories naturally, they
tended to spontaneously engage in the strategies. Therefore, we
sought an active baseline task that would not engage the
regulatory, memory, and emotional processes of interest, and
prior work suggests that this arrows task does not engage these
Figure 1. Regions of lPFC active for each strategy relative to baseline. Bar graphs illustrate parameter estimates of signal intensity for each strategy versus
baseline. Error bars represent SEM. AC, accept; AN, analyze; FE, feel; lPFC, left prefrontal cortex.
Table 1. Conjunction Analysis Identifying Regions Commonly Active in
the Feel, Analyze, and Accept Strategy Conditions Relative to an Active
Baseline Task
Region of Activation
Brodmann’s
Area t
TAL Coordinates
Voxelsx y z
Inferior Frontal Gyrus 46 4.46 $51 29 16 218
Cuneus 19 4.46 $12 $88 31 94
Cerebellum 4.11 24 $70 $38 29
Middle Occipital Gyrus 18 3.69 15 $91 10 17
Lingual Gyrus 18 3.89 $6 $73 $2 16
TAL, Talairach.
362 BIOL PSYCHIATRY 2009;65:361–366 E. Kross et al.
www.sobp.org/journal
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